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Dorsal root ganglion-derived exosomes deteriorate neuropathic pain by activating microglia via the microRNA-16-5p/HECTD1/HSP90 axis

The activated microglia have been reported as pillar factors in neuropathic pain (NP) pathology, but the molecules driving pain-inducible microglial activation require further exploration. In this study, we in...

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MicroRNA-721 regulates gluconeogenesis via KDM2A-mediated epigenetic modulation in diet-induced insulin resistance in C57BL/6J mice

Aberrant gluconeogenesis is considered among primary drivers of hyperglycemia under insulin resistant conditions, with multiple studies pointing towards epigenetic dysregulation. Here we examine the role of mi...

Combined transcriptomics and proteomics unveil the impact of vitamin C in modulating specific protein abundance in the mouse liver

Vitamin C (ascorbate) is a water-soluble antioxidant and an important cofactor for various biosynthetic and regulatory enzymes. Mice can synthesize vitamin C thanks to the key enzyme gulonolactone oxidase (Gul...

Novel role of LLGL2 silencing in autophagy: reversing epithelial-mesenchymal transition in prostate cancer

Prostate cancer (PCa) is a major urological disease that is associated with significant morbidity and mortality in men. LLGL2 is the mammalian homolog of Lgl. It acts as a tumor suppressor in breast and hepati...

Rapid development and mass production of SARS-CoV-2 neutralizing chicken egg yolk antibodies with protective efficacy in hamsters

Despite the record speed of developing vaccines and therapeutics against the SARS-CoV-2 virus, it is not a given that such success can be secured in future pandemics. In addition, COVID-19 vaccination and appl...

High-fat diet, microbiome-gut-brain axis signaling, and anxiety-like behavior in male rats

Obesity, associated with the intake of a high-fat diet (HFD), and anxiety are common among those living in modern urban societies. Recent studies suggest a role of microbiome-gut-brain axis signaling, includin...

General regulatory factors exert differential effects on nucleosome sliding activity of the ISW1a complex

Chromatin dynamics is deeply involved in processes that require access to DNA, such as transcriptional regulation. Among the factors involved in chromatin dynamics at gene regulatory regions are general regula...

Establishment of primary prostate epithelial and tumorigenic cell lines using a non-viral immortalization approach

Research on prostate cancer is mostly performed using cell lines derived from metastatic disease, not reflecting stages of tumor initiation or early progression. Establishment of cancer cell lines derived from...

The effect of diabetes mellitus on differentiation of mesenchymal stem cells into insulin-producing cells

Diabetes mellitus (DM) is a global epidemic with increasing incidences. DM is a metabolic disease associated with chronic hyperglycemia. Aside from conventional treatments, there is no clinically approved cure...

Control of astrocytic Ca 2+ signaling by nitric oxide-dependent S-nitrosylation of Ca 2+ homeostasis modulator 1 channels

Astrocytes Ca 2+ signaling play a central role in the modulation of neuronal function. Activation of metabotropic glutamate receptors (mGluR) by glutamate released during an increase in synaptic activity triggers ...

Increased levels and activation of the IL-17 receptor in microglia contribute to enhanced neuroinflammation in cerebellum of hyperammonemic rats

Patients with liver cirrhosis may show minimal hepatic encephalopathy (MHE) with mild cognitive impairment and motor incoordination. Rats with chronic hyperammonemia reproduce these alterations. Motor incoordi...

Identification and expression analysis of two steamer-like retrotransposons in the Chilean blue mussel ( Mytilus chilensis )

Disseminated neoplasia (DN) is a proliferative cell disorder of the circulatory system of bivalve mollusks. The disease is transmitted between individuals and can also be induced by external chemical agents su...

Noncoding RNAs in skeletal development and disorders

Protein-encoding genes only constitute less than 2% of total human genomic sequences, and 98% of genetic information was previously referred to as “junk DNA”. Meanwhile, non-coding RNAs (ncRNAs) consist of app...

Cx43 hemichannels and panx1 channels contribute to ethanol-induced astrocyte dysfunction and damage

Alcohol, a widely abused drug, significantly diminishes life quality, causing chronic diseases and psychiatric issues, with severe health, societal, and economic repercussions. Previously, we demonstrated that...

Galectins in epithelial-mesenchymal transition: roles and mechanisms contributing to tissue repair, fibrosis and cancer metastasis

Galectins are soluble glycan-binding proteins that interact with a wide range of glycoproteins and glycolipids and modulate a broad spectrum of physiological and pathological processes. The expression and subc...

Glutaminolysis regulates endometrial fibrosis in intrauterine adhesion via modulating mitochondrial function

Endometrial fibrosis, a significant characteristic of intrauterine adhesion (IUA), is caused by the excessive differentiation and activation of endometrial stromal cells (ESCs). Glutaminolysis is the metabolic...

The long-chain flavodoxin FldX1 improves the biodegradation of 4-hydroxyphenylacetate and 3-hydroxyphenylacetate and counteracts the oxidative stress associated to aromatic catabolism in Paraburkholderia xenovorans

Bacterial aromatic degradation may cause oxidative stress. The long-chain flavodoxin FldX1 of Paraburkholderia xenovorans LB400 counteracts reactive oxygen species (ROS). The aim of this study was to evaluate the...

MicroRNA-148b secreted by bovine oviductal extracellular vesicles enhance embryo quality through BPM/TGF-beta pathway

Extracellular vesicles (EVs) and their cargoes, including MicroRNAs (miRNAs) play a crucial role in cell-to-cell communication. We previously demonstrated the upregulation of bta-mir-148b in EVs from oviductal...

YME1L-mediated mitophagy protects renal tubular cells against cellular senescence under diabetic conditions

The senescence of renal tubular epithelial cells (RTECs) is crucial in the progression of diabetic kidney disease (DKD). Accumulating evidence suggests a close association between insufficient mitophagy and RT...

Effects of latroeggtoxin-VI on dopamine and α-synuclein in PC12 cells and the implications for Parkinson’s disease

Parkinson’s disease (PD) is characterized by death of dopaminergic neurons leading to dopamine deficiency, excessive α-synuclein facilitating Lewy body formation, etc. Latroeggtoxin-VI (LETX-VI), a proteinaceo...

Glial-restricted progenitor cells: a cure for diseased brain?

The central nervous system (CNS) is home to neuronal and glial cells. Traditionally, glia was disregarded as just the structural support across the brain and spinal cord, in striking contrast to neurons, alway...

Carbapenem-resistant hypervirulent ST23 Klebsiella pneumoniae with a highly transmissible dual-carbapenemase plasmid in Chile

The convergence of hypervirulence and carbapenem resistance in the bacterial pathogen Klebsiella pneumoniae represents a critical global health concern. Hypervirulent K. pneumoniae (hvKp) strains, frequently from...

Endometrial mesenchymal stromal/stem cells improve regeneration of injured endometrium in mice

The monthly regeneration of human endometrial tissue is maintained by the presence of human endometrial mesenchymal stromal/stem cells (eMSC), a cell population co-expressing the perivascular markers CD140b an...

Embryo development is impaired by sperm mitochondrial-derived ROS

Basal energetic metabolism in sperm, particularly oxidative phosphorylation, is known to condition not only their oocyte fertilising ability, but also the subsequent embryo development. While the molecular pat...

Fibroblasts inhibit osteogenesis by regulating nuclear-cytoplasmic shuttling of YAP in mesenchymal stem cells and secreting DKK1

Fibrous scars frequently form at the sites of bone nonunion when attempts to repair bone fractures have failed. However, the detailed mechanism by which fibroblasts, which are the main components of fibrous sc...

MSC-derived exosomes protect auditory hair cells from neomycin-induced damage via autophagy regulation

Sensorineural hearing loss (SNHL) poses a major threat to both physical and mental health; however, there is still a lack of effective drugs to treat the disease. Recently, novel biological therapies, such as ...

Alpha-synuclein dynamics bridge Type-I Interferon response and SARS-CoV-2 replication in peripheral cells

Increasing evidence suggests a double-faceted role of alpha-synuclein (α-syn) following infection by a variety of viruses, including SARS-CoV-2. Although α-syn accumulation is known to contribute to cell toxic...

Lactadherin immunoblockade in small extracellular vesicles inhibits sEV-mediated increase of pro-metastatic capacities

Tumor-derived small extracellular vesicles (sEVs) can promote tumorigenic and metastatic capacities in less aggressive recipient cells mainly through the biomolecules in their cargo. However, despite recent ad...

Integration of ATAC-seq and RNA-seq identifies MX1-mediated AP-1 transcriptional regulation as a therapeutic target for Down syndrome

Growing evidence has suggested that Type I Interferon (I-IFN) plays a potential role in the pathogenesis of Down Syndrome (DS). This work investigates the underlying function of MX1, an effector gene of I-IFN,...

The novel roles of YULINK in the migration, proliferation and glycolysis of pulmonary arterial smooth muscle cells: implications for pulmonary arterial hypertension

Abnormal remodeling of the pulmonary vasculature, characterized by the proliferation and migration of pulmonary arterial smooth muscle cells (PASMCs) along with dysregulated glycolysis, is a pathognomonic feat...

Electroacupuncture promotes neurogenesis in the dentate gyrus and improves pattern separation in an early Alzheimer's disease mouse model

Impaired pattern separation occurs in the early stage of Alzheimer’s disease (AD), and hippocampal dentate gyrus (DG) neurogenesis participates in pattern separation. Here, we investigated whether spatial memo...

Role of SYVN1 in the control of airway remodeling in asthma protection by promoting SIRT2 ubiquitination and degradation

Asthma is a heterogenous disease that characterized by airway remodeling. SYVN1 (Synoviolin 1) acts as an E3 ligase to mediate the suppression of endoplasmic reticulum (ER) stress through ubiquitination and de...

Advances towards the use of gastrointestinal tumor patient-derived organoids as a therapeutic decision-making tool

In December 2022 the US Food and Drug Administration (FDA) removed the requirement that drugs in development must undergo animal testing before clinical evaluation, a declaration that now demands the establish...

Melatonin alleviates pyroptosis by regulating the SIRT3/FOXO3α/ROS axis and interacting with apoptosis in Atherosclerosis progression

Atherosclerosis (AS), a significant contributor to cardiovascular disease (CVD), is steadily rising with the aging of the global population. Pyroptosis and apoptosis, both caspase-mediated cell death mechanism...

Prenatal ethanol exposure and changes in fetal neuroendocrine metabolic programming

Prenatal ethanol exposure (PEE) (mainly through maternal alcohol consumption) has become widespread. However, studies suggest that it can cause intrauterine growth retardation (IUGR) and multi-organ developmen...

Autologous non-invasively derived stem cells mitochondria transfer shows therapeutic advantages in human embryo quality rescue

The decline in the quantity and quality of mitochondria are closely associated with infertility, particularly in advanced maternal age. Transferring autologous mitochondria into the oocytes of infertile female...

Development of synthetic modulator enabling long-term propagation and neurogenesis of human embryonic stem cell-derived neural progenitor cells

Neural progenitor cells (NPCs) are essential for in vitro drug screening and cell-based therapies for brain-related disorders, necessitating well-defined and reproducible culture systems. Current strategies em...

Heat-responsive microRNAs participate in regulating the pollen fertility stability of CMS-D2 restorer line under high-temperature stress

Anther development and pollen fertility of cytoplasmic male sterility (CMS) conditioned by Gossypium harknessii cytoplasm (CMS-D2) restorer lines are susceptible to continuous high-temperature (HT) stress in sum...

Chemogenetic inhibition of NTS astrocytes normalizes cardiac autonomic control and ameliorate hypertension during chronic intermittent hypoxia

Obstructive sleep apnea (OSA) is characterized by recurrent episodes of chronic intermittent hypoxia (CIH), which has been linked to the development of sympathoexcitation and hypertension. Furthermore, it has ...

SARS-CoV-2 spike protein S1 activates Cx43 hemichannels and disturbs intracellular Ca 2+ dynamics

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes the ongoing coronavirus disease 2019 (COVID-19). An aspect of high uncertainty is whether the SARS-CoV-2 per se or the systemic inflammation ...

The effect of zofenopril on the cardiovascular system of spontaneously hypertensive rats treated with the ACE2 inhibitor MLN-4760

Angiotensin converting enzyme 2 (ACE2) plays a crucial role in the infection cycle of SARS-CoV-2 responsible for formation of COVID-19 pandemic. In the cardiovascular system, the virus enters the cells by bind...

Two murine models of sepsis: immunopathological differences between the sexes—possible role of TGFβ1 in female resistance to endotoxemia

Endotoxic shock (ExSh) and cecal ligature and puncture (CLP) are models that induce sepsis. In this work, we investigated early immunologic and histopathologic changes induced by ExSh or CLP models in female a...

An intracellular, non-oxidative factor activates in vitro chromatin fragmentation in pig sperm

In vitro incubation of epididymal and vas deferens sperm with Mn 2+ induces Sperm Chromatin Fragmentation (SCF), a mechanism that causes double-stranded breaks in toroid-linker regions (TLRs). Whether this mechani...

Focal ischemic stroke modifies microglia-derived exosomal miRNAs: potential role of mir-212-5p in neuronal protection and functional recovery

Ischemic stroke is a severe type of stroke with high disability and mortality rates. In recent years, microglial exosome-derived miRNAs have been shown to be promising candidates for the treatment of ischemic ...

S -Nitrosylation in endothelial cells contributes to tumor cell adhesion and extravasation during breast cancer metastasis

Nitric oxide is produced by different nitric oxide synthases isoforms. NO activates two signaling pathways, one dependent on soluble guanylate cyclase and protein kinase G, and other where NO post-translationa...

Identifying pyroptosis- and inflammation-related genes in intracranial aneurysms based on bioinformatics analysis

Intracranial aneurysm (IA) is the most common cerebrovascular disease, and subarachnoid hemorrhage caused by its rupture can seriously impede nerve function. Pyroptosis is an inflammatory mode of cell death wh...

Drosophila Atlastin regulates synaptic vesicle mobilization independent of bone morphogenetic protein signaling

The endoplasmic reticulum (ER) contacts endosomes in all parts of a motor neuron, including the axon and presynaptic terminal, to move structural proteins, proteins that send signals, and lipids over long dist...

Mucin1 induced trophoblast dysfunction in gestational diabetes mellitus via Wnt/β-catenin pathway

To elucidate the role of Mucin1 (MUC1) in the trophoblast function (glucose uptake and apoptosis) of gestational diabetes mellitus (GDM) women through the Wnt/β-catenin pathway.

Human umbilical cord mesenchymal stem cells (hUC-MSCs) alleviate paclitaxel-induced spermatogenesis defects and maintain male fertility

Chemotherapeutic drugs can cause reproductive damage by affecting sperm quality and other aspects of male fertility. Stem cells are thought to alleviate the damage caused by chemotherapy drugs and to play role...

Exploring the Neandertal legacy of pancreatic ductal adenocarcinoma risk in Eurasians

The genomes of present-day non-Africans are composed of 1–3% of Neandertal-derived DNA as a consequence of admixture events between Neandertals and anatomically modern humans about 50–60 thousand years ago. Ne...

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Page 1 of 24

Upregulated dual oxidase 1-induced oxidative stress and caspase-1-dependent pyroptosis reflect the etiologies of heart failure

Oxidative stress is implicated in the pathogenesis of heart failure. Dual oxidase 1 (DUOX1) might be important in heart failure development through its mediating role in oxidative stress. This study was design...

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Comparing chemical transfection, electroporation, and lentiviral vector transduction to achieve optimal transfection conditions in the Vero cell line

Transfection is an important analytical method for studying gene expression in the cellular environment. There are some barriers to efficient DNA transfection in host cells, including circumventing the plasma ...

High-fat diet enhances cell proliferation and compromises intestinal permeability in a translational canine intestinal organoid model

Emerging evidence underscores the responsiveness of the mammalian intestine to dietary cues, notably through the involvement of LGR5 + intestinal stem cells in orchestrating responses to diet-driven signals. H...

mTOR signaling pathway regulation HIF-1 α effects on LPS induced intestinal mucosal epithelial model damage

Sepsis-induced small-intestinal injury is associated with increased morbidity and mortality. Our previous study and other papers have shown that HIF-1α has a protective effect on intestinal mucosal injury in s...

Long non-coding RNA SOX2OT in tamoxifen-resistant breast cancer

Hormone receptor (HR)-positive breast cancer can become aggressive after developing hormone-treatment resistance. This study elucidated the role of long non-coding RNA (lncRNA) SOX2OT in tamoxifen-resistant (T...

Mice lacking DIO3 exhibit sex-specific alterations in circadian patterns of corticosterone and gene expression in metabolic tissues

Disruption of circadian rhythms is associated with neurological, endocrine and metabolic pathologies. We have recently shown that mice lacking functional type 3 deiodinase (DIO3), the enzyme that clears thyroi...

Optimization of seeding density of OP9 cells to improve hematopoietic differentiation efficiency

OP9 mouse stromal cell line has been widely used to induce differentiation of human embryonic stem cells (hESCs) into hematopoietic stem/progenitor cells (HSPCs). However, the whole co-culture procedure usuall...

Development of an in vitro human alveolar epithelial air-liquid interface model using a small molecule inhibitor cocktail

The alveolar epithelium is exposed to numerous stimuli, such as chemicals, viruses, and bacteria that cause a variety of pulmonary diseases through inhalation. Alveolar epithelial cells (AECs) cultured in vitr...

Mechanical stretch leads to increased caveolin-1 content and mineralization potential in extracellular vesicles from vascular smooth muscle cells

Hypertension-induced mechanical stress on vascular smooth muscle cells (VSMCs) is a known risk factor for vascular remodeling, including vascular calcification. Caveolin-1 (Cav-1), an integral structural compo...

Melatonin reduces lung injury in type 1 diabetic mice by the modulation of autophagy

In recent years, the role of autophagy has been highlighted in the pathogenesis of diabetes and inflammatory lung diseases. In this study, using a diabetic model of mice, we investigated the expression of auto...

TonEBP/NFAT5 expression is associated with cisplatin resistance and migration in macrophage-induced A549 cells

Macrophages promote angiogenesis, metastasis, and drug resistance in several cancers. Similarly, TonEBP/NFAT5 induces metastasis in renal carcinoma and colon cancer cells. However, the role of this transcripti...

Optimizing combination therapy in prostate cancer: mechanistic insights into the synergistic effects of Paclitaxel and Sulforaphane-induced apoptosis

Combination therapies in cancer treatment have demonstrated synergistic or additive outcomes while also reducing the development of drug resistance compared to monotherapy. This study explores the potential of...

CTC together with Shh and Nrf2 are prospective diagnostic markers for HNSCC

The lack of appropriate prognostic biomarkers remains a significant obstacle in the early detection of Head and Neck Squamous Cell Carcinoma (HNSCC), a cancer type with a high mortality rate. Despite considera...

Prioritization of Trypanosoma brucei editosome protein interactions interfaces at residue resolution through proteome-scale network analysis

Trypanosoma brucei is the causative agent for trypanosomiasis in humans and livestock, which presents a growing challenge due to drug resistance. While identifying novel drug targets is vital, the process is dela...

Sumoylation of SAP130 regulates its interaction with FAF1 as well as its protein stability and transcriptional repressor function

Fas-associated factor 1 (FAF1) is a multidomain protein that interacts with diverse partners to affect numerous cellular processes. Previously, we discovered two Small Ubiquitin-like Modifier (SUMO)-interactin...

Loss of Dec1 inhibits alcohol-induced hepatic lipid accumulation and circadian rhythm disorder

Chronic alcohol exposure increases liver damage such as lipid accumulation and hepatitis, resulting in hepatic cirrhosis. Chronic alcohol intake is known to disturb circadian rhythms in humans and animals. DEC...

Association between plasma L-carnitine levels and mitochondrial DNA copy number

Mitochondria are key cytoplasmic organelles in eukaryotic cells that generate adenosine triphosphate (ATP) through the electron transport chain and oxidative phosphorylation. Mitochondrial DNA (mtDNA) copy num...

Effect of Emi1 gene silencing on the proliferation and invasion of human breast cancer cells

Breast cancer is the most common malignant tumour in women. The early silk-splitting inhibitor protein 1 Emi1 is responsible for mediating ubiquitin protein degradation. The present study investigated the effe...

TNFα induces Caspase-3 activity in hematopoietic progenitor cells CD34+, CD33+, and CD41 + of myelodysplastic syndromes

Cytopenia is the primary feature of Myelodysplastic Syndrome, even in the presence of hypercellular bone marrow. TNFα is recognized as both a proinflammatory, and proapoptotic cytokine with a well established ...

From network analysis to experimental validation: identification of regulators of non-muscle myosin II contractility using the folded-gastrulation signaling pathway

The morphogenetic process of apical constriction, which relies on non-muscle myosin II (NMII) generated constriction of apical domains of epithelial cells, is key to the development of complex cellular pattern...

Simple, low-cost, and well-performing method, the outgrowth technique, for the isolation of cells from nasal polyps

Epithelial cells are an important part of the pathomechanism in chronic rhinosinusitis with nasal polyps. It is therefore essential to establish a robust method for the isolation and culture of epithelial cell...

Comprehensive brain tissue metabolomics and biological network technology to decipher the mechanism of hydrogen-rich water on Radiation-induced cognitive impairment in rats

Hydrogen-rich water (HRW) has been shown to prevent cognitive impairment caused by ionizing radiation. This study aimed to investigate the pharmacological effects and mechanisms of HRW on ionizing radiation by...

Mineral elements and adiposity-related consequences in adolescents with intellectual disabilities

Patients with intellectual disabilities are shown to have a limited capacity for cooperation, communication,and other biological consequences, which significantly require a specialized interest in healthcare p...

Glycyrrhizin inhibits LPS-induced inflammatory responses in goat ruminal epithelial cells in vitro

Inflammation plays a crucial role in the progression of Subacute Ruminal Acidosis (SARA). The experiment was designed to investigate anti-inflammatory effects of glycyrrhizin on goats ruminal epithelial cells ...

D-galactose-induced mitochondrial oxidative damage and apoptosis in the cochlear stria vascularis of mice

Age-related hearing loss, known as presbycusis, is the result of auditory system degeneration. Numerous studies have suggested that reactive oxygen species (ROS) and mitochondrial oxidative damage play importa...

Keratin 19 binds and regulates cytoplasmic HNRNPK mRNA targets in triple-negative breast cancer

Heterogeneous nuclear ribonucleoprotein K (HNRNPK) regulates pre-mRNA processing and long non-coding RNA localization in the nucleus. It was previously shown that shuttling of HNRNPK to the cytoplasm promotes ...

A computational peptide model induces cancer cells’ apoptosis by docking Kringle 5 to GRP78

Cells can die through a process called apoptosis in both pathological and healthy conditions. Cancer development and progression may result from abnormal apoptosis. The 78-kDa glucose-regulated protein (GRP78)...

BMP9 maintains the phenotype of HTR-8/Svneo trophoblast cells by activating the SDF1/CXCR4 pathway

Bone morphogenetic protein 9 (BMP9) has been shown to regulate processes such as angiogenesis, endothelial dysfunction, and tumorigenesis. However, the role of BMP9 in preeclampsia (PE) is unclear. The purpose...

Emodin and aloe-emodin, two potential molecules in regulating cell migration of skin cells through the MAP kinase pathway and affecting Caenorhabditis elegans thermotolerance

Emodin and aloe-emodin are two anthraquinones having positive effects in wound healing. However, their mechanism of action of wound healing is not fully understood. The MAP kinase family, which plays an active...

Knockdown of ELF4 aggravates renal injury in ischemia/reperfusion mice through promotion of pyroptosis, inflammation, oxidative stress, and endoplasmic reticulum stress

Renal ischemia/reperfusion (I/R) injury is a major cause of acute kidney injury (AKI). Dysfunction of E74-like ETS transcription factor 4 (ELF4) leads to inflammation. This research intended to look into the f...

Janus Kinase 3 phosphorylation and the JAK/STAT pathway are positively modulated by follicle-stimulating hormone (FSH) in bovine granulosa cells

Janus kinase 3 (JAK3) is a member of the JAK family of tyrosine kinase proteins involved in cytokine receptor-mediated intracellular signal transduction through the JAK/STAT signaling pathway. JAK3 was previou...

Genetic and protein interaction studies between the ciliary dyslexia candidate genes DYX1C1 and DCDC2

DYX1C1 (DNAAF4) and DCDC2 are two of the most replicated dyslexia candidate genes in genetic studies. They both have demonstrated roles in neuronal migration, in cilia growth and function and they both are cytosk...

SUMOylation of PDGF receptor α affects signaling via PLCγ and STAT3, and cell proliferation

The platelet-derived growth factor (PDGF) family of ligands exerts their cellular effects by binding to α- and β-tyrosine kinase receptors (PDGFRα and PDGFRβ, respectively). SUMOylation is an important posttra...

Myogenic differentiation of human myoblasts and Mesenchymal stromal cells under GDF11 on Poly-ɛ-caprolactone-collagen I-Polyethylene-nanofibers

For the purpose of skeletal muscle engineering, primary myoblasts (Mb) and adipogenic mesenchymal stem cells (ADSC) can be co-cultured and myogenically differentiated. Electrospun composite nanofiber scaffolds...

Computational analysis of missense variant CYP4F2*3 (V433M) in association with human CYP4F2 dysfunction: a functional and structural impact

Cytochrome P450 4F2 (CYP4F2) enzyme is a member of the CYP4 family responsible for the metabolism of fatty acids, therapeutic drugs, and signaling molecules such as arachidonic acid, tocopherols, and vitamin K...

Using RNA-seq to identify suitable housekeeping genes for hypoxia studies in human adipose-derived stem cells

Hypoxic culture conditions have been used to study the impact of oxygen deprivation has on gene expression in a number of disease models. However, hypoxia response elements present in the promoter regions of s...

SCAT8/miR-125b-5p axis triggers malignant progression of nasopharyngeal carcinoma through SCARB1

Nasopharyngeal carcinoma is a tumor with high malignancy and poor prognosis, which severely affects the health of the patients. LncRNAs and microRNAs are crucial for the occurrence and development of nasophary...

ARNTL2 upregulation of ACOT7 promotes NSCLC cell proliferation through inhibition of apoptosis and ferroptosis

Recent studies have reported that the circadian transcription factor aryl hydrocarbon receptor nuclear translocator like 2 (ARNTL2) promotes the metastatic progression of lung adenocarcinoma. However, the mole...

Evolutionary relevance of single nucleotide variants within the forebrain exclusive human accelerated enhancer regions

Human accelerated regions (HARs) are short conserved genomic sequences that have acquired significantly more nucleotide substitutions than expected in the human lineage after divergence from chimpanzees. The f...

The DNA demethylation-regulated SFRP2 dictates the progression of endometriosis via activation of the Wnt/β-catenin signaling pathway

Endometriosis cause decreases in life quality and pelvic pain in reproductive-age women. Methylation abnormalities played a functional role in the progression of endometriosis, this study aimed to explore the ...

Pre-treatment with IL-6 potentiates β-cell death induced by pro-inflammatory cytokines

Type I Diabetes mellitus (T1D) is characterized by a specific destruction of β-cells by the immune system. During this process pro-inflammatory cytokines are released in the pancreatic islets and contribute for β...

Role of the human solute carrier family 14 member 1 gene in hypoxia-induced renal cell carcinoma occurrence and its enlightenment to cancer nursing

Hypoxia is considered a critical contributor to renal cell carcinoma progression, including invasion and metastasis. However, the potential mechanisms by which it promotes invasion and metastasis have not yet ...

Cyclic tensile force modifies calvarial osteoblast function via the interplay between ERK1/2 and STAT3

Mechanical therapies, such as distraction osteogenesis, are widely used in dental clinics. During this process, the mechanisms by which tensile force triggers bone formation remain of interest. Herein, we inve...

Urine-derived mesenchymal stem cells-derived exosomes enhances survival and proliferation of aging retinal ganglion cells

This study was designed to investigate to test the effect of exosomes from urine-derived mesenchymal stem cells (USCs) on the survival and viability of aging retinal ganglion cells (RGCs), and explored the pre...

RPL11 promotes non-small cell lung cancer cell proliferation by regulating endoplasmic reticulum stress and cell autophagy

Abnormal biogenesis and ribosome free function of ribosomal proteins (RPs) is important for tumorgenesis and development. Ribosomal protein L11 (RPL11) is a component of ribosomal 60 S large subunit with diffe...

Sperm capacitation and transcripts levels are altered by in vitro THC exposure

Delta-9-tetrahydrocannabinol (THC) is the primary phytocannabinoid responsible for the psychoactive properties of cannabis and is known to interact with the endocannabinoid system, which is functionally presen...

The dual role of Nrf2 in melanoma: a systematic review

Melanoma is the most lethal type of skin cancer that originates from the malignant transformation of melanocytes. Although novel treatments have improved patient survival in melanoma, the overall prognosis rem...

Hyperoxia exposure upregulates Dvl-1 and activates Wnt/β-catenin signaling pathway in newborn rat lung

Bronchopulmonary dysplasia is a serious and lifelong pulmonary disease in premature neonates that influences around one-quarter of premature newborns. The wingless-related integration site /β-catenin signaling...

Circ-ATL1 silencing reverses the activation effects of SIRT5 on smooth muscle cellular proliferation, migration and contractility in intracranial aneurysm by adsorbing miR-455

Alterations in vascular smooth muscle cells (VSMCs) contribute to the pathogenesis of intracranial aneurysms (IAs). However, molecular mechanisms underlying these changes remain unknown. The present study aime...

HMGB1 mediates lipopolysaccharide-induced macrophage autophagy and pyroptosis

Autophagy and pyroptosis of macrophages play important protective or detrimental roles in sepsis. However, the underlying mechanisms remain unclear. High mobility group box protein 1 (HMGB1) is associated with...

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Orcas Just Sank Another Yacht

Orcas have once again attacked and sunk a boat near the Strait of Gibraltar, a behavior that has scientists stumped

Andrea Thompson

Revolutionary Genetics Research Shows RNA May Rule Our Genome

Scientists have recently discovered thousands of active RNA molecules that can control the human body

Philip Ball

Why Insects Are Lured to Lights in the Night

Moths and other insects aren’t drawn to nighttime illumination for the reasons we think they are

Gary Stix, Immy Smith

Stolen Bacterial Genes Helped Whiteflies to Become the Ultimate Pests

Rather than relying on bacteria, whiteflies cut out the middleman and acquired their own genes to process nitrogen

Rohini Subrahmanyam

Belugas Flirt and Fight by Morphing Their Squishy Forehead

Scientists are putting together a catalog of communications from belugas’ forehead “melon”

Monique Brouillette

Puppy-Dog Eyes in Wild Canines Spark Rethink on Dog Evolution

The eyebrows of the African wild dog have scientists wondering whether other canine species besides domestic dogs can make the irresistible “puppy-dog eyes” expression

Gillian Dohrn, Nature magazine

See What Gives Sourdough Its Distinctive Taste and Smell

You can thank yeast and bacteria cultivated over generations for the distinctive taste and smell of the oldest leavened bread in history

Daniel Veghte, The Conversation US

China’s Population Could Shrink to Half by 2100

Is China’s future population drop a crisis or an opportunity?

Lex Rieffel, Xueqing Wang

Can You Eat Cicadas? Can Your Dog Do So?

Here’s what a chef, a vet and two anthropologists have to say about eating periodical cicadas

Meghan Bartels

We Are in the Golden Age of Bird-Watching

There has never been a better time to be or become a birder

How Sugar Gliders Got Their Wings

Several marsupial species, including sugar gliders, independently evolved a way to make membranes that allow them to glide through the air

Viviane Callier

Glow-in-the-Dark Animals May Have Been Around for 540 Million Years

Ancestors of so-called soft corals may have developed bioluminescence in the earliest days of deep-ocean living

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Back to the roots: A focus on plant cell biology

Dolf weijers.

Senior Editor, The Plant Cell and Laboratory of Biochemistry, Wageningen University, Wageningen, The Netherlands

Magdalena Bezanilla

Reviewing Editor, The Plant Cell and Department of Biological Sciences, Dartmouth College, Hanover, NH, USA

Liwen Jiang

Guest Editor, The Plant Cell and School of Life Sciences, Centre for Cell and Developmental Biology, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China

Adrienne H K Roeder

Guest Editor, The Plant Cell and Weil Institute for Cell and Molecular Biology and School of Integrative Plant Sciences, Section of Plant Biology, Cornell University, Ithaca, NY, USA

Mary Williams

Features Editor, The Plant Cell, American Society of Plant Biologists, USA

Defining plant cell biology—especially in multicellular organisms—is not an easy task as it encompasses diverse tissues, organs, and ultimately the whole organism and its interaction with the environment. Events taking place at cellular scale are a consequence of molecular mechanisms that drive myriad processes occurring within and between single cells and their compartments. Perhaps, for this reason, it is fitting that The Plant Cell publishes in a broad range of topics. In this Focus Issue, we go back to the “roots” of the journal, that gave it its name, and turn our attention to the many fascinating facets of plant cell biology. The 11 review papers and 11 original research articles in this issue exemplify the breadth of the field and highlight both established concepts and recent achievements.

Much has changed in the 33 years since The Plant Cell was founded in 1989. Although molecular techniques were well established, researchers still largely studied one gene at a time, using relatively crude assays such as RNA blots to quantify gene expression. Arabidopsis research was gaining traction, but researchers still lacked a complete genome sequence or knock-out libraries. Imaging tools and probes were, by today’s standards, relatively limited; a further 5 years would pass before GFP was developed as a fluorescent protein reporter. Today’s research tools provide extraordinary insights into cell structure and function that were unimaginable in 1989, but also have opened new research avenues such as the ability to view cellular dynamics in real time in living cells and address questions about the roles of stochasticity and emergent properties in cell biology. Thus, we felt it was time to provide readers with an up-to-date view of plant cell biology.

This Focus Issue has two types of review papers: a set of eight traditional review papers, as well as three reviews that each are a collection of vignettes contributed by several authors. In the first of the vignette-style reviews, Kang et al. (2022) offer visual insight into the structures that compose plant cells, and present open questions related to plant cell structure. In the Cheung et al. (2022 ) review, seven eminent plant cell biologists offer first-hand narratives of several seminal discoveries that helped shape the field. Lastly, in Roeder et al. (2022) , experts in a range of areas within the field of plant cell biology formulate important outstanding questions to inspire future investigation.

The remaining reviews cover a broad range of topics at both subcellular and supracellular scales. Gu and Rasmussen (2022) provide an extensive overview of the cell biology underlying primary cell wall biosynthesis. Codjoe et al. (2022) focus on how plant cells sense and respond to physical forces through the mechanobiology of the walls, plasma membrane, and protoplast. Plant cells consist of many internal membrane structures, and Aniento et al. (2022) discuss the endomembrane trafficking processes that organize, maintain, and remodel these internal membrane structures. A notable aspect of the organization of plant cells and their membranes is the ability to define polar membrane domains. Ramalho et al. (2022 ) present an overview of the processes underlying plant cell polarity and its evolution. For any multicellular plant, cell division must be connected to growth and cell identity. Sablowski and Gutierrez (2022) describe the mechanisms that control cell cycle progression, cell growth, and cell fate. Zuch et al. (2022 ) integrate many of the elements in each of these reviews in a developmental context: the leaf epidermis. They discuss how cell division plane, cell cycle, cell polarity, and growth are coordinated to arrive at an organized multicellular structure. Since the development of molecular biology, genomics, and transgenesis, many cell biology studies have used flowering plant models such as tobacco and Arabidopsis. However, many of the developmental processes in flowering plants are derived from ancestral processes in early land plants. Naramoto et al. (2022) discuss the insights gained and open questions in using the bryophytes Physcomitrium patens and Marchantia polymorpha as models. The plant cell biology field has developed with the advent of methodologies that allow visualizing molecules and structures, and their dynamics. Colin et al. (2022 ) discuss the development of methodologies that enable present and future plant cell biologists to obtain a quantitative and dynamic view of plant cells.

Besides insightful and inspiring review papers, the Focus Issue contains 11 original research articles, of which two are Breakthrough Reports. These two Breakthrough Reports present crisp, shorter studies that are of exceptional novelty, or that open new avenues of investigation. Duncombe et al. (2022) describe the use of structured illumination microscopy (SIM) to track Arabidopsis Cellulose Synthase A (CESA) particle movement in the plasma membrane. This super-resolution approach provides new insight into the particle density and velocity, as well as their variation. Hacker et al. (2022) used a strategy revolving around CRISPR/Cas mutant analysis to identify the proteins in Arabidopsis that mediate the repair of DNA breaks and DNA-protein crosslinks induced by stalled topoisomerase 2 cleavage complexes. While this mechanism was suspected to exist in plants, its components had not yet been discovered.

The nine regular original research articles in this Focus Issue span a range of topics at different levels of cellular organization. Noack et al. (2022) describe the identification and characterization of a protein complex that acts as a scaffold to target the Arabidopsis PI4 kinase alpha1 to membrane nanodomains. Genetic analysis demonstrates a central role of this complex, which thus controls local membrane composition, in gametophyte and sporophyte development. Chang et al. (2022) present an extensive cell biological and genetic analysis of the Physcomitrium family of COPII coat proteins belonging to the Sec23 and Sec24 families. Within the Sec23 family, different isoforms have unique localization and functions related to endomembrane trafficking, secretion, and growth and development. The same COPII coat protein complex is linked to PI3P and autophagy in Arabidopsis by Kim et al. (2022) . In this study, the FYVE2 PI3P-binding protein is found to interact both with the COPII regulator SAR1, and with the ATG18A autophagy protein. Ma et al. (2022) report the formation of membrane nanodomains compartments containing Remorin proteins upon pathogen perception in Arabidopsis. Remorin in these clusters appears to undergo condensation, an example of liquid–liquid phase separation. Through interaction, Remorin concentrates the Formin protein, which causes local Actin nucleation. In a second paper from the same team, Minh Tran et al. (2022) report that outer membrane vesicles from the pathogenic bacterium Xanthomonas campestris can fuse with the plasma membrane in Arabidopsis , thus modifying host cell membrane properties. To complete a set of papers on organelles and endomembrane compartments, Liu et al. (2022) report an analysis of the FtsZ protein which is involved in chloroplast division. The authors show that weak membrane association through a newly identified protein motif, coupled to protein polymerization, is sufficient for membrane tethering and function. De Jaeger-Braet et al (2022) used live imaging of male meiocytes in Arabidopsis under normal and heat stress conditions to follow progression of meiosis. Their study revealed the existence of a previously unknown checkpoint that is sensitive to heat stress. Finally, two papers report on aspects of stomatal development and function. Yang et al. (2022a ) reveal an interesting link between cuticle formation and stomatal patterning in Arabidopsis . Analysis of the transcription factor MYB16 revealed that its downregulation by the SPCH transcription factor is necessary to prevent excess cuticle formation and clustering of stomata. Yang et al. (2022b ) describe the analysis of the Arabidopsis stomatal closure-related Actin-binding protein1 (SCAB1). This protein binds the membrane phospholipid PI3P and thereby controls its ability to oligomerize. As such, membrane PI3P influences Actin bundling during ABA-induced stomatal closure.

Beyond this set of papers in the Focus Issue, a larger collection of papers in the area of cell biology, published ∼1 year before or after this issue, will be bundled into a Focus Collection. This Focus Issue, together with the Focus Collection, showcases past and present insights, victories, and successes in this research field. The field has progressed immensely in the past decades, and we wonder what the next 33 years have in store. If one thing has become clear, it is that scientific progress, and thereby the development of a research field, is difficult to predict. Who would have predicted the concepts and findings reported in this Focus Issue 33 years ago? A key element of surprise is the development of new technologies that bring new boundaries into view, and challenges of which previously we were unaware. It seems biology has gotten much more complex, and yet we are also increasingly able to manage this complexity through computational approaches, including artificial intelligence. This latter development is also removing the shackles inherent to the limitations of the human mind in grasping complexity and thinking non-linearly. Perhaps the field of cell biology will be revolutionized by the computer sciences? We leave it to future Focus Issues to tell that story.

Contributor Information

Dolf Weijers, Senior Editor, The Plant Cell and Laboratory of Biochemistry, Wageningen University, Wageningen, The Netherlands.

Magdalena Bezanilla, Reviewing Editor, The Plant Cell and Department of Biological Sciences, Dartmouth College, Hanover, NH, USA.

Liwen Jiang, Guest Editor, The Plant Cell and School of Life Sciences, Centre for Cell and Developmental Biology, State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong, China.

Adrienne H K Roeder, Guest Editor, The Plant Cell and Weil Institute for Cell and Molecular Biology and School of Integrative Plant Sciences, Section of Plant Biology, Cornell University, Ithaca, NY, USA.

Mary Williams, Features Editor, The Plant Cell, American Society of Plant Biologists, USA .

• Aniento F, Sánchez de Medina Hernández V, Dagdas Y, Rojas-Pierce M, Russinova E (2022) Molecular mechanisms of endomembrane trafficking in plants . Plant Cell   34 : 146–173 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Chang M, Wu S-Z, Ryken SE, O’Sullivan JE, Bezanilla M (2022) COPII Sec23 proteins form isoform-specific endoplasmic reticulum exit sites with differential effects on polarized growth . Plant Cell   34 : 333–350 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Cheung AY, Cosgrove DJ, Hara-Nishimura I, Jürgens G, Lloyd C, Robinson DG, Staehelin LA, Weijers D (2022) A rich and bountiful harvest: key discoveries in plant cell biology . Plant Cell   34 : 53–71 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Codjoe JM, Miller K, Haswell ES (2022) Plant cell mechanobiology: greater than the sum of its parts . Plant Cell   34 : 129–145 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Colin L, Martin-Arevalillo R, Bovio S, Bauer A, Vernoux T, Caillaud M-C, Landrein B, Jaillais Y (2022) Imaging the living plant cell: from probes to quantification . Plant Cell   34 : 247–272 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• De Jaeger-Braet J, Krause L, Buchholz A, Schnittger A (2022) Heat stress reveals a specialized variant of the pachytene checkpoint in meiosis of Arabidopsis thaliana . Plant Cell   34 : 433–454 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Duncombe SG, Grama Chethan S, Anderson CT (2022) Super-resolution imaging illuminates new dynamic behaviors of cellulose synthase . Plant Cell   34 : 273–286 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Gu Y, Rasmussen CG (2022) Cell biology of primary cell wall synthesis in plants . Plant Cell   34 : 103–128 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Hacker L, Dorn A, Enderle J, Puchta H (2022) The repair of topoisomerase 2 cleavage complexes in Arabidopsis . Plant Cell   34 : 287–301 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Kang B-H, Anderson CT, Arimura S, Bayer E, Bezanilla M, Botella MA, Brandizzi F, Burch-Smith TM, Chapman KD, Dünser K, et al. (2022) A glossary of plant cell structures: current insights and future questions . Plant Cell   34 : 10–52 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Kim JH, Lee HN, Huang X, Jung H, Otegui MS, Lic F, Chung T (2022) FYVE2, a phosphatidylinositol 3-phosphate effector in Arabidopsis, interacts with COPII machinery to control autophagosome formation . Plant Cell   34 : 351–373 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Liu X, An J, Wang L, Sun Q, An C, Wu B, Hong C, Wang X, Dong S, Guo J, et al. (2022) A new type of amphiphilic motif at the C-terminus of FtsZ1 facilitates chloroplast division . Plant Cell   34 : 419–432 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Ma Z, Sun Y, Zhy X, Yang L, Chen X, Miao Y (2022) Membrane nanodomains modulate formin condensation for actin remodeling in Arabidopsis innate immune reponses . Plant Cell   34 : 374–394 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Minh Tran T, Chng C-P, Pu X, Ma Z, Han X, Liu X, Yang L, Huang C, Miao Y (2022) Potentiation of plant defense by bacterial outer membrane vesicles is mediated by nanodomain assembly . Plant Cell   34 : 395–418 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Naramoto S, Hata Y, Fujita T, Kyozuka J (2022) The bryophytes Physcomitrium patens and Marchantia polymorpha as model systems for studying evolutionary cell and developmental biology in plants . Plant Cell   34 : 228–246 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Noack LC, Bayle V, Armengot L, Rozier F, Mamode-Cassim A, Stevens FD, Caillaud M-C, Munnik T, Mongrand S, Pleskot R, et al. (2022) A nanodomain-anchored scaffolding complex is required for the function and localization of phosphatidylinositol 4-kinase alpha in plants . Plant Cell   34 : 302–332 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Ramalho JJ, Jones VAS, Mutte S, Weijers D (2022) Pole position: how plant cells polarize along the axes . Plant Cell   34 : 174–192 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Roeder AHK, Otegui MS, Dixit R, Anderson CT, Faulkner C, Zhang Y, Harrison MJ, Kirchhelle C, Goshima G, Coate JE, et al. (2022) Fifteen compelling open questions in plant cell biology . Plant Cell   34 : 72–102 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Sablowski R, Gutierrez C (2022) Cycling in a crowd: coordination of plant cell division, growth, and cell fate . Plant Cell   34 : 193–208 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Yang S-L, Tran N, Tsai M-Y, Ho C-MK (2022a) Misregulation of MYB16 expression causes stomatal cluster formation by disrupting polarity during asymmetric cell divisions . Plant Cell   34 : 455–476 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Yang Y, Zhao Y, Zheng W, Zhao Y, Zhao S, Wang Q, Bai L, Zhang T, Huang S, Song C, et al. (2022b) Phosphatidylinositol 3-Phosphate Regulates SCAB1-Mediated F-Actin Reorganization during Stomatal Closure in Arabidopsis . Plant Cell   34 : 477–494 [ PMC free article ] [ PubMed ] [ Google Scholar ]
• Zuch DT, Doyle SM, Majda M, Smith RS, Robert S, Torii KU (2022) Cell biology of the leaf epidermis: fate specification, morphogenesis and coordination . Plant Cell   34 : 209–227 [ PMC free article ] [ PubMed ] [ Google Scholar ]

A Guide to Biology: Find Primary Articles

• Find Primary Articles
• Find Books and Background Information
• Literature Reviews
• Citing Biology Sources/Citation Management

Journals List: Do We Have this Journal?

When you have a source with a bibliography, you can see if a particular article from the bibliography is available by looking the journal's name up at the link below. Then you can use the volume and date information to navigate to the article. If we don't have access to that journal, we usually can get it from another library.

• Search the Journals List: Do We Have this Journal?

Biology Journals in Print

These print-format journals all publish primary research and review articles in the field of biology.

American Midland Naturalist Genes and Development (most current year; earlier volumes in PMC)  Nature Science Wilson Journal of Ornithology

We also subscribe in print to the following biology-related journals and magazines Environment: Science and Policy for Sustainable Development Environmental Ethics Horticulture (current issue on main floor) Loon Minnesota Birding Minnesota Conservation Volunteer National Wildlife New Scientist (current issue on main floor)

Open Access to Biology Research

When searching PubMed, you can narrow the results to "free full text." 

For a single source of open access journal articles in the life sciences, this collection from the National Library of Medicine is hard to beat.

• PubMed Central (digital archive of journal literature) This link opens in a new window Free full text scholarly journal archive of literature in the life and health sciences, managed by the National Center for Biotechnology Information at the National Library of Medicine.

Biology Databases

Often you will hear the phrase "primary articles" when starting biology research, meaning articles written by scientists reporting new research. These typically introduce the research with a review of previous research in the introduction, methodology, results, and discussion and/or conclusion. Journals in biology also publish "review articles" that provide a roundup of recent research on a topic in biology. If you are looking for primary articles or review articles in biology and biomedical topics, these databases will be especially useful.

• Biological Science This link opens in a new window Covers research in all areas of biological science, including animal behavior, biomedicine, zoology, ecology, and others. Coverage is from 1982 to the present. Includes abstracts and citations, as well as access to thousands of full text titles.
• PubMed (citations from MEDLINE and other sources) This link opens in a new window PubMed contains more than 30 million citations and abstracts of biomedical literature. Click the "Find it at Gustavus" button to link to the full text or to make an interlibrary loan request. PubMed was developed and is maintained by the National Institutes of Health.
• Web of Science (Web of Knowledge) This link opens in a new window Science Citation Index Expanded, Social Sciences Citation Index, and Arts & Humanities Citation Index of the Institute for Scientific Information (ISI). Besides indexing a wide range of journals in the sciences, social sciences, and history, this resource allows you to search for articles that cite a specific author or published work. Coverage from 1997 to the present. Click on the "Web of Science" tab to limit your search to one or more specific citation databases.

Annual Reviews

These annual books publish review articles - detailed recaps of research on questions in the field. They are an excellent place to gain a sense of the various approaches to a topic and references to the literature that supports it.

Two series are shelved in the general collection under the following call numbers:

• ADVANCES IN MARINE BIOLOGY v. 1, 1963- (QH 91 .A1 A22)
• ADVANCES IN VIRUS RESEARCH v. 1, 1953- (QR 360 .A3)

Also of interest is WILDLIFE MONOGRAPHS. Current volumes are available online ; volumes from 1956 - 2009 are sheved at QL 1 .W54.

The Annual Reviews series online also includes biology-related review articles.

• Annual Review of Biochemistry
• Annual Review of Cell and Developmental Biology
• Annual Review of Ecology, Evolution, and Systematics
• Annual Review of Entomology
• Annual Review of Genetics
• Annual Review of Genomics and Human Genetics
• Annual Review of Immunology
• Annual Review of Neuroscience

Other Science Databases

• AGRICOLA This link opens in a new window Citations and abstracts for agricultural publications from the 15th century to the present, including articles from over 600 periodicals, USDA and state experiment station and extension publications, and selected books. Subjects include animal and veterinary sciences, entomology, plant sciences, food and human nutrition, and earth and environmental sciences. Many records are linked to full-text documents online. A resource of the National Agricultural Library.
• Google Scholar This link opens in a new window This search engine points toward scholarly research rather than all Web-based sources. It is stronger in the sciences than in the humanities, with social sciences somewhere in between. One interesting feature of Google Scholar is that in includes a link to sources that cite a particular item. Not all of the articles in Google Scholar are free; the library can obtain many of them for you through Interlibrary loan.

How Do I Get the Actual Articles?

If there isn't a PDF available, look for a "find it" link. That will check to see if it's available through another of our databases. If no full text is available, it will give you an opportunity to request the article from another library. You will have to log in using your Gustavus username and password. It usually takes a day or two. Look for an email that will explain how to download the PDF. 

If you're using Google Scholar, look for either a "find it @ Gustavus" link to the right or a "more" link under the reference you're interested in.  

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Biological Sciences: 03-124: Modern Biology Laboratory: Finding Research Articles

• Finding Research Articles
• Popular Science News Resources
• PubMed Tutorial
• Google Scholar Tutorial
• Citation Management with Zotero

Useful Resource for Accessing Articles

The LibKey Nomad browser extension provides one-click access to the Libraries' full text resources as you find research on the web and in databases. Find information on how to install here . 

Types of Scholarly Information

You will encounter many types of articles and it is important to distinguish between these different categories of scholarly literature.  Keep in mind the following definitions.

PRIMARY RESEARCH ARTICLE :   A primary research article describes an empirical study that aims to gain new knowledge on a topic through direct or indirect observation and research.  These include quantitative or qualitative data and analysis. In science, a primary article will often include the following sections:  Abstract, Introduction, Methods, Results, and Discussion.

REVIEW ARTICLE :  In the scientific literature, this is a type of article that provides a synthesis of existing research on a particular topic.  These are useful when you want to get an idea of a body of research that you are not yet familiar with.

PEER-REVIEWED :  Refers to articles that have undergone a rigorous review process by peers in their discipline , often including revisions to the original manuscript, before publication in a scholarly journal. Primary research articles in reputable life science journals are always peer-reviewed. Reviews are often peer-reviewed as well. 

Useful Journals for this Class

• JoVE Biology
• Springer Nature Experiments
• Current Protocols in Cell Biology
• Current Protocols in Molecular Biology

How to Find Research Articles

Research databases.

Research databases are key to conducting comprehensive or specific searches of the scholarly literature across many different publishers and journals. They include special tools and filters to help you narrow and expand your search.

• PubMed :  PubMed is the   most comprehensive source to find scholarly journal articles in biology, health, and medicine.  It is maintained by the National Library of Medicine and contains millions of citations and is updated daily with newly published research.
• Google Scholar : Google Scholar is a freely available search engine to find scholarly literature in all fields and disciplines. It lacks the many built-in filtering capabilities of subject-specific databases, like PubMed, but can be a useful place to start your research when you are trying to narrow your research topic or to search broadly across many subject areas.

ACADEMIC JOURNALS

You can browse the contents of specific journals in a field by going to the publisher's websites. This is a good way to get to know the type of research being conducted in particular fields. The following academic journals have publicly available articles:

• PLOS Biology

To access journals with paid content, you can go directly to the publisher's site and view all the content if you are on campus. If you are off-campus, go to the library homepage and click on Journals & Newspapers. It will give you options for finding articles from different years. You will be prompted to enter you Andrew ID and password but then you can access full-text articles and download PDFs.

Finding Full-Text Articles

Most research articles are not publicly available and require an institutional subscription to access them.  If you have citations for specific articles, search for the article in the Library Catalog  to see if have access to it. The Catalog will show whether or not we have access to the electronic version and/or the print version. If the CMU library collection doesn't have what you're looking for, you can request an article scan via Interlibrary Loan.

Request materials through Interlibrary Loan  by following the instructions for ILLiad.

You can also search for specific articles by putting the article title in the PubMed or Google Scholar databases and following the instructions for finding full-text articles on the PubMed Tutorial and Google Scholar Tutorial tabs of this guide.

If you need help accessing articles, please contact the science librarian team at [email protected].

Search Tips for Finding Relevant Articles

• START WITH A REVIEW ARTICLE . Review articles are excellent resources for finding a lot of primary research articles on a given topic. For example, if I'm interested in the development of visual cortical neurons, I could start my search by reading a recent review article on that topic and then look at the references section of the paper to find primary research articles.
• FIND ONE OR A FEW RELEVANT PRIMARY RESEARCH ARTICLES . Having even a single relevant article of interest can be very useful in performing a literature search. You can look at the References section of that paper to find older related articles.But how do you find more recent articles that have used and cited the article of interest in their work? You can use Google Scholar  to find all of the more recent articles that have cited your article of interest.  This is a great way to understand how your article of interest has built on prior research and how it has influenced more recent research. In Google Scholar, you can find related articles by clicking on the " Related Articles " link. In  PubMed , you can find related articles by clicking on the title of the article and then the " Similar Articles " link in the right column.

Let's look at the example below. I want to find some relevant articles on the development of visual cortical neurons.

Here, you can see my search for "development of visual cortical neurons" on Google Scholar. In this case, I'm interested in finding a relevant article that is fairly recent so I've set a filter on the left so that only articles published between 2016 and 2018 will appear in my search. The first hit, "Microglial P2Y12 is necessary for synaptic plasticity in visual cortex," looks particularly interesting to me.

I can see that 57 articles have cited this paper and I can click on the Cited by 57  link to see all of those articles. When I click on that link, I see the screen below. I can click on Sort by Date on the left and see that the most recent paper that cited " Microglial   P2Y12  is necessary for synaptic plasticity in visual cortex"  was published only two days ago! This is an excellent way of finding very recent relevant material. I can also click on the Related Articles  link to see articles that are on the same topic. PubMed has a similar link that shows up underneath articles called Similar Articles .

Therefore, by finding a single relevant paper, we can easily find many more relevant articles by looking at the Reference section of " Microglial   P2Y12  is necessary for synaptic plasticity in visual cortex" , the Cited by  link, and also the Related Articles  link. Together, all of these articles will help us understand how the article, " Microglial   P2Y12  is necessary for synaptic plasticity in visual cortex,"  has contributed to the collective body of knowledge on this topic.

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• Last Updated: Oct 2, 2023 10:41 PM
• URL: https://guides.library.cmu.edu/modernbiolab

Jessie Ball duPont Library

Biology 233: molecular cell biology.

• Getting Started
• Find Primary Research Articles
• Help with Reading Research Articles
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Browse through Journals

Search biology databases.

• AJP: Cell Physiology
• Biology of the Cell
• BMC Molecular BIology
• Cell Research
• Cellular Microbiology
• Journal of Molecular Biology
• Molecular and Cellular Biology
• Molecular Cell
• More Journals in Molecular, Cellular and Developmental Biology

Search Gale Academic OneFile

Search google scholar for articles.

Search for journals by title or subject

Request an Interlibrary Loan

• Sewanee ILL

Nature: News and Views

Need an example of a News and Views article from the journal, Nature? Take a look at these recent articles:

• News and Views: Suspect that modulates the heartbeat is ensnared
• News and Views: Meet the relatives of our cellular ancestor
• News and Views: An immune-cell signature marks the brain in Alzheimer's disease
• News and Views: Senescent cells feed on their neighbours
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• Last Updated: Jan 24, 2024 2:57 PM
• URL: https://library.sewanee.edu/biol233

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Articles and Primary Literature in Biology

Databases for finding articles.

• Secondary Sources
• Write and Cite in the Sciences
• Sub-discipline Resources
• Chemical and Lab Safety

In the sciences, a primary source describes original research, while a secondary source analyzes or comments on a primary source or sources.   For example, a research article is primary literature because it describes an original experiment and its results, while a review article is secondary literature because it collates multiple research articles to describe the current state of the field.

Examples of primary sources: 

• Research articles
• Theses and dissertations
• Conference proceedings
• Patents 
• Unrefined data sets 

Examples of secondary sources:

• Review articles
• Data compilations

The databases below can help you find primary literature in the sciences. While searching, you can narrow your results to primary literature by using filters on the left of the page.

• Web of Science This link opens in a new window A large interdisciplinary database with a strong collection in the sciences. Filter for primary literature by selecting Article under Document Type on the left of the page. more... less... Easily explore an article bibliography, as well as sources that have cited the article since its publication, via the Citation Network feature. Create a free personal account to keep a comprehensive search history, create search alerts and citation alerts. Additional features related to author and journal profiles are available. Language: English, Russian, French, German, Chinese, Spanish, Japanese, Portuguese, etc. Keywords: Social Science Citation Index Science Citation Index Arts and Humanities Citation Index Conference Proceedings Citation Index Emerging Sources Citation Index WoS Knowledge
• PubMed This link opens in a new window A massive biomedical database run by the NIH, with articles stretching back to the 1950s. Filter primary literature by selecting Clinical Trial under Article Type on the top left of the page. more... less... Includes advanced search tools such as Medical Subject Headings (MeSH) and the Clinical Queries feature. Personalized MyNCBI account features, such as email alerts, are only available by leaving the Library's instance of PubMed and accessing the resource through the open web site (pubmed.gov). Language: English Keywords: Pub Med
• USDA National Agricultural Library This link opens in a new window Why search here? Good for indexed citations from AGRICOLA, PubAg, and the NAL Digital Collections (NALDC) on agriculture topics, food and human nutrition, forestry, aquaculture and fisheries, animal and veterinary sciences. Content type: Abstracts of scholarly articles, book chapters, theses, patents, technical reports. Coverage dates: 1970 - present more... less... Language: English Keywords: Pub Ag U.S. US Department
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• : Feb 19, 2024 3:26 PM
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BIO 191: General Biology I

• Get Ready to Search
• Find Articles
• What is a Scholarly Article?
• What is a Peer-Reviewed Article?

What is a Primary Research Article?

How do you identify primary research articles.

• Cite Your Sources

Librarian for the Sciences

In a primary research article, author(s) present a new set of findings from original research after conducting an original experiment. Think of what you do in any of your various lab activities. If you were to write a scholarly paper on any of your biology labs (like the Flowers and Pollinators lab from BIO 191), it would be a primary research article.

Primary research articles are also referred to as original research or research articles.

How to Identify Primary Research Article

• Did the author(s) of the paper conduct the experiment themselves? This is the most important thing to look for in order to identify primary research. Look for language that indicates that the author(s) devised the experiment, carried it out, and analyzed the resulting data themselves.
• "Methods"/"Materials and Methods"/"Experimental Methods"(different journals title this section in different ways)
• "Results"
• "Discussion"

Here is One Example of a Primary Research Article and How to Determine that it is a Primary Research Article

"Effects of Salinity Stress on Survival, Metabolism, Limb Regeneration, and Ecdysis in UCA PUGNAX"

Read the Abstract

If you read the abstract, you can see that the author(s) themselves conducted an experiment:

• "This study investigated physiological and metabolic changes in the molt cycle of U. pugnax..."
• "For this study, a limb was removed and its regenerative growth was photographed every two days"
• "...crabs were dissected, and the tissues collected were analyzed for their protein and carbohydrate contents."

Read the Headings

• The article has Materials and Methods, Results, and Discussion sections, all which indicate that the authors conducted an experiment and then analyzed the data they found.

Skim the Article

If you skim the article, it is clear that the authors tested a hypothesis using the scientific method. They are only really talking about research that was conducted by others in the "Introduction" section of the article, which is what you would expect for a primary research article.

Look for Textual Evidence

If you skim the article, you can easily find additional evidence that an experiment was conducted by the authors themselves.

• [They collected their sample i.e. crabs.]
• [They exposed their sample to different variables.]
• [They used statistical methods to analyze their data.]
• [They reported the results of their experiment.]
• [They drew a conclusion from their experimental results.]
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Secondary Menu

• Research Articles & Papers

Korunes, KL; Myers, RB; Hardy, R; Noor, MAF

Drosophila pseudoobscura is a classic model system for the study of evolutionary genetics and genomics. Given this long-standing interest, many genome sequences have accumulated for D. pseudoobscura and closely related species D. persimilis, D. miranda, and D. lowei. To facilitate the exploration… read more about this publication  »

Zipple, MN; Roberts, EK; Alberts, SC; Beehner, JC

Bartoš et al. (2021; Mammal Review 51: 143–153; https://doi.org/10.1111/mam.12219) reviewed the mechanisms involved in the ‘Bruce effect’ – a phenomenon originally documented in inseminated female house mice Mus musculus, who block pregnancy following exposure to a novel (non-sire) male. They argue… read more about this publication  »

Byrne, M; Koop, D; Strbenac, D; Cisternas, P; Yang, JYH; Davidson, PL; Wray, G

The molecular mechanisms underlying development of the pentameral body of adult echinoderms are poorly understood but are important to solve with respect to evolution of a unique body plan that contrasts with the bilateral body plan of other deuterostomes. As Nodal and BMP2/4 signalling is involved… read more about this publication  »

Wang, Q; Xu, P; Sanchez, S; Duran, P; Andreazza, F; Isaacs, R; Dong, K

BackgroundInsects rely on their sense of smell to locate food and hosts, find mates and select sites for laying eggs. Use of volatile compounds, such as essential oils (EOs), to repel insect pests and disrupt their olfaction-driven behaviors has great practical significance in integrated pest… read more about this publication  »

Castano-Duque, L; Ghosal, S; Quilloy, FA; Mitchell-Olds, T; Dixit, S

Rice production is shifting from transplanting seedlings to direct sowing of seeds. Following heavy rains, directly sown seeds may need to germinate under anaerobic environments, but most rice (Oryza sativa) genotypes cannot survive these conditions. To identify the genetic architecture of complex… read more about this publication  »

Peng, L; Shan, X; Wang, Y; Martin, F; Vilgalys, R; Yuan, Z

Clitopilus hobsonii (Entolomataceae, Agaricales, Basidiomycetes) is a common soil saprotroph. There is also evidence that C. hobsonii can act as a root endophyte benefitting tree growth. Here, we report the genome assembly of C. hobsonii QYL-10, isolated from ectomycorrhizal root tips of Quercus… read more about this publication  »

Yan, W; Wang, B; Chan, E; Mitchell-Olds, T

The genetic basis of flowering time changes across environments, and pleiotropy may limit adaptive evolution of populations in response to local conditions. However, little information is known about how genetic architecture changes among environments. We used genome-wide association studies (GWAS… read more about this publication  »

Doak, DF; Waddle, E; Langendorf, RE; Louthan, AM; Isabelle Chardon, N; Dibner, RR; Keinath, DA; Lombardi, E; Steenbock, C; Shriver, RK; Linares, C; Begoña Garcia, M; Funk, WC; Fitzpatrick, SW; Morris, WF; Peterson, ML

Structured demographic models are among the most common and useful tools in population biology. However, the introduction of integral projection models (IPMs) has caused a profound shift in the way many demographic models are conceptualized. Some researchers have argued that IPMs, by explicitly… read more about this publication  »

Kim, JH; Hilleary, R; Seroka, A; He, SY

A grand challenge facing plant scientists today is to find innovative solutions to increase global crop production in the context of an increasingly warming climate. A major roadblock to global food sufficiency is persistent loss of crops to plant diseases and insect infestations. The United… read more about this publication  »

Yuan, M; Jiang, Z; Bi, G; Nomura, K; Liu, M; Wang, Y; Cai, B; Zhou, J-M; He, SY; Xin, X-F

The plant immune system is fundamental for plant survival in natural ecosystems and for productivity in crop fields. Substantial evidence supports the prevailing notion that plants possess a two-tiered innate immune system, called pattern-triggered immunity (PTI) and effector-triggered immunity (… read more about this publication  »

Benito-Kwiecinski, S; Giandomenico, SL; Sutcliffe, M; Riis, ES; Freire-Pritchett, P; Kelava, I; Wunderlich, S; Martin, U; Wray, GA; McDole, K; Lancaster, MA

The human brain has undergone rapid expansion since humans diverged from other great apes, but the mechanism of this human-specific enlargement is still unknown. Here, we use cerebral organoids derived from human, gorilla, and chimpanzee cells to study developmental mechanisms driving evolutionary… read more about this publication  »

Lofgren, LA; Nguyen, NH; Vilgalys, R; Ruytinx, J; Liao, H-L; Branco, S; Kuo, A; LaButti, K; Lipzen, A; Andreopoulos, W; Pangilinan, J; Riley, R; Hundley, H; Na, H; Barry, K; Grigoriev, IV; Stajich, JE; Kennedy, PG

While there has been significant progress characterizing the 'symbiotic toolkit' of ectomycorrhizal (ECM) fungi, how host specificity may be encoded into ECM fungal genomes remains poorly understood. We conducted a comparative genomic analysis of ECM fungal host specialists and generalists,… read more about this publication  »

Mitchell, RM; Ames, GM; Wright, JP

Background and aimsUnderstanding impacts of altered disturbance regimes on community structure and function is a key goal for community ecology. Functional traits link species composition to ecosystem functioning. Changes in the distribution of functional traits at community scales in response to… read more about this publication  »

DeMarche, ML; Bailes, G; Hendricks, LB; Pfeifer-Meister, L; Reed, PB; Bridgham, SD; Johnson, BR; Shriver, R; Waddle, E; Wroton, H; Doak, DF; Roy, BA; Morris, WF

Spatial gradients in population growth, such as across latitudinal or elevational gradients, are often assumed to primarily be driven by variation in climate, and are frequently used to infer species' responses to climate change. Here, we use a novel demographic, mixed-model approach to dissect the… read more about this publication  »

Shaw, EC; Fowler, R; Ohadi, S; Bayly, MJ; Barrett, RA; Tibbits, J; Strand, A; Willis, CG; Donohue, K; Robeck, P; Cousens, RD

Aim: If we are able to determine the geographic origin of an invasion, as well as its known area of introduction, we can better appreciate the innate environmental tolerance of a species and the strength of selection for adaptation that colonizing populations have undergone. It also enables us to… read more about this publication  »

Rushworth, CA; Mitchell-Olds, T

Despite decades of research, the evolution of sex remains an enigma in evolutionary biology. Typically, research addresses the costs of sex and asexuality to characterize the circumstances favoring one reproductive mode. Surprisingly few studies address the influence of common traits that are, in… read more about this publication  »

Jorge, JF; Bergbreiter, S; Patek, SN

Small organisms can produce powerful, sub-millisecond impacts by moving tiny structures at high accelerations. We developed and validated a pendulum device to measure the impact energetics of microgram-sized trap-jaw ant mandibles accelerated against targets at 105 m s-2 Trap-jaw ants (… read more about this publication  »

Markunas, AM; Manivannan, PKR; Ezekian, JE; Agarwal, A; Eisner, W; Alsina, K; Allen, HD; Wray, GA; Kim, JJ; Wehrens, XHT; Landstrom, AP

Long QT syndrome (LQTS) is a genetic disease resulting in a prolonged QT interval on a resting electrocardiogram, predisposing affected individuals to polymorphic ventricular tachycardia and sudden death. Although a number of genes have been implicated in this disease, nearly one in four… read more about this publication  »

Stone, DF; Mccune, B; Pardo-De La Hoz, CJ; Magain, N; Miadlikowska, J

The new genus Sinuicella, an early successional lichen, was found on bare soil in Oregon, USA. The thallus is minute fruticose, grey to nearly black, branching isotomic dichotomous, branches round, 20-90 μm wide in water mount. The cortex is composed of interlocking cells shaped like jigsaw puzzle… read more about this publication  »

Oita, S; Ibáñez, A; Lutzoni, F; Miadlikowska, J; Geml, J; Lewis, LA; Hom, EFY; Carbone, I; U'Ren, JM; Arnold, AE

Understanding how species-rich communities persist is a foundational question in ecology. In tropical forests, tree diversity is structured by edaphic factors, climate, and biotic interactions, with seasonality playing an essential role at landscape scales: wetter and less seasonal forests… read more about this publication  »

Hibshman, JD; Webster, AK; Baugh, LR

Standard laboratory culture of Caenorhabditis elegans utilizes solid growth media with a bacterial food source. However, this culture method limits control of food availability and worm population density, factors that impact many life-history traits. Here, we describe liquid-culture protocols for… read more about this publication  »

Caves, EM; Green, PA; Zipple, MN; Bharath, D; Peters, S; Johnsen, S; Nowicki, S

AbstractSensory systems are predicted to be adapted to the perception of important stimuli, such as signals used in communication. Prior work has shown that female zebra finches perceive the carotenoid-based orange-red coloration of male beaks-a mate choice signal-categorically. Specifically,… read more about this publication  »

Reed, PB; Peterson, ML; Pfeifer-Meister, LE; Morris, WF; Doak, DF; Roy, BA; Johnson, BR; Bailes, GT; Nelson, AA; Bridgham, SD

Predicting species' range shifts under future climate is a central goal of conservation ecology. Studying populations within and beyond multiple species' current ranges can help identify whether demographic responses to climate change exhibit directionality, indicative of range shifts, and whether… read more about this publication  »

Sallee, JL; Crawford, JM; Singh, V; Kiehart, DP

Actin filament crosslinking, bundling and molecular motor proteins are necessary for the assembly of epithelial projections such as microvilli, stereocilia, hairs, and bristles. Mutations in such proteins cause defects in the shape, structure, and function of these actin - based protrusions. One… read more about this publication  »

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Biology Resources

• Primary/Secondary Articles

Characteristics of a Primary Article

• Presents original data and ideas from a scientific investigation reported by scientist and written for others in the field.
• Reports the results of experiments, observations, and other scientific investigation.
• Introduction
• Methods (or Materials and Methods)
• Acknowledgements, and  Literature Cited (or References)

Examples of Journals:  Science , Nature , Ecology (although they may have some secondary articles such as reviews or brief news items). Most of the journals from the American Society for Microbiology will include primary articles. 

Example of an article recommended by your professor: "Glutamine cannot support recombinant CHO cell growth and maintenance in the absence of glucose" in Process Biochemistry doi:10.1016/S0032-9592(03)00182-1 .

Characteristics of a Secondary Article

• Synthesizes and summarizes results of original research.
• Describes, interprets, analyzes and evaluates the original research.
• Comments on and discusses the evidence provided by primary sources.
• Written for a scientific audience or for a non-scientific audience.
• Written by experts (scientists) or general writers.
• Published in science magazines and may be published in some science journals.

Examples of Journals:  Scientific American , Science News , Annual Review of Ecology and Systematics .

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• Open access
• Published: 07 May 2024

Integrative analysis of transcriptome and target metabolites uncovering flavonoid biosynthesis regulation of changing petal colors in Nymphaea ‘Feitian 2’

• Xian Zhou 1 , 2 , 3 ,
• Xiaohan Wang 1 , 2 , 3 ,
• Haohui Wei 1 , 2 , 4 ,
• Huijin Zhang 1 , 2 ,
• Qian Wu 1 , 2 &
• Liangsheng Wang 1 , 2 , 3  

BMC Plant Biology volume  24 , Article number:  370 ( 2024 ) Cite this article

139 Accesses

Metrics details

Nymphaea (waterlily) is known for its rich colors and role as an important aquatic ornamental plant globally. Nymphaea atrans and some hybrids, including N . ‘Feitian 2,’ are more appealing due to the gradual color change of their petals at different flower developmental stages. The petals of N. ‘Feitian 2’ gradually change color from light blue-purple to deep rose-red throughout flowering. The mechanism of the phenomenon remains unclear.

In this work, flavonoids in the petals of N. ‘Feitian 2’ at six flowering stages were examined to identify the influence of flavonoid components on flower color changes. Additionally, six cDNA libraries of N . ‘Feitian 2’ over two blooming stages were developed, and the transcriptome was sequenced to identify the molecular mechanism governing petal color changes. As a result, 18 flavonoid metabolites were identified, including five anthocyanins and 13 flavonols. Anthocyanin accumulation during flower development is the primary driver of petal color change. A total of 12 differentially expressed genes (DEGs) in the flavonoid biosynthesis pathway were uncovered, and these DEGs were significantly positively correlated with anthocyanin accumulation. Six structural genes were ultimately focused on, as their expression levels varied significantly across different flowering stages. Moreover, 104 differentially expressed transcription factors (TFs) were uncovered, and three MYBs associated with flavonoid biosynthesis were screened. The RT-qPCR results were generally aligned with high-throughput sequencing results.

Conclusions

This research offers a foundation to clarify the mechanisms underlying changes in the petal color of waterlilies.

Peer Review reports

Flower color is a remarkable and diverse characteristic throughout the plant kingdom. It not only plays a vital role in the success of plant survival or reproduction but also has significant economic benefits for the flower industry [ 1 , 2 ]. Some factors influencing the development of flower color encompass the classes and levels of pigments in the petals, co-pigmentation effects, cell vacuole pH, petal epidermal cell structure, and complexes with metal ions [ 3 ]. Among these, the type and contents of pigments in the petals exert the greatest influence [ 4 ]. Anthocyanins, a class of flavonoids, influence 80% of angiosperms flower colors globally, including yellow, pink, red, purple, and blue [ 5 , 6 , 7 ].

In addition to single-color flowers, some plants possess complex flower color patterns. Some flowers can gradually change color over the course of the flowering period, including Lonicera japonica (white to gold), Xanthoceras sorbifolium (yellow or orange to red), Lantana camara (yellow to orange to scarlet to magenta), Brunfelsia acuminata (deep purple to light purple to white), Hibiscus mutabilis (white to pink to red), Combretum indicum (white to red), and Victoria (white to pink or ruby red). The color change mechanism varies between different flowers. The color change of L. japonica flowers was caused by β-carotene concentrations increasing dramatically in the white to golden flower stages, accompanied by a drop in lutein concentrations [ 8 ]. In B. acuminate , the anthocyanin content decreased, and the petal color changed [ 9 ]. The alteration in petal coloration has been attributed to an elevated concentration of cyanidin derivatives or delphinidin derivatives in the vacuoles of petals [ 10 , 11 , 12 , 13 , 14 ]. The molecular mechanisms underlying color changes are receiving increasing attention. In Paeonia ‘Coral Sunset’, the change in flower color from coral to pink to pale yellow is due to a significant decrease in anthocyanin content. Then, eight structural genes related to anthocyanin synthesis were highly expressed during the S1 period and lowly expressed during other stages, causing petal color changed [ 15 ]. In Nelumbo ‘Qiusanse’, petals color faded during flowering. Researchers have found that the involvement of anthocyanin biosynthesis repressors and degrading genes as well as pH regulators in controlling color fading [ 16 ].

Waterlilies, a general term for plants in the Nymphaea genus, are perennial aquatic plants with high ornamental, cultural, and economic value in the family Nymphaeaceae [ 17 , 18 , 19 ]. They are also the national flower of Egypt, Thailand, and other countries. Waterlilies represent an early diverging clade of flowering plants with unique roles in angiosperm phylogeny [ 20 , 21 , 22 ]. They are the most diverse and widespread genus of the family Nymphaeaceae, including five subgenera, including Lotos , Hydrocallis , Anecphya , Brachyceras , and Nymphaea [ 23 , 24 ]. Waterlilies are globally distributed, with over 50 species, including abundant germplasm resources, with over 1000 cultivars globally.

Waterlilies display various flower colors, including white, yellow, red, purple, and blue, among others. Flavonoids are the primary pigments responsible for floral color in waterlilies. To date, 117 flavonoids have been identified in waterlilies, including 20 anthocyanins [ 25 ]. In examining waterlily flower color, some researchers have focused on the mechanism of blue flower formation [ 22 , 26 ]. In addition to blue flowers, N. atrans and its hybrids can undergo petal color changes throughout the flowering period, resulting in higher ornamental value than others [ 27 ]. The N . ‘Feitian 2,’ intersubgeneric hybrid of N. atrans , perfectly inherits the characteristic of color-changing petals of N. atrans . In addition, its single flower possesses a longer flowering period, its stamen color is deep purple-red instead of yellow, and its petals are more discolored. Petals of N . ‘Feitian 2’ gradually change from light blue-purple to deep rose-red during flowering. However, the mechanism underlying this color change during flowering remains unclear.

To uncover this mechanism, N . ‘Feitian 2’, which changes petal color during flowering, was selected as the experimental subject. In the present study, we identified flavonoids, especially anthocyanins, in flower petals six days after opening via high-performance liquid chromatography (HPLC) and examined the relationship between flower coloration and pigment content. Moreover, transcriptomic analysis of petals from two different flowering stages was conducted to reveal the gene regulation responsible for the N . ‘Feitian 2’ color transition process. This research elucidates the mechanism of flower color change in waterlilies and guides the molecular breeding of ornamental plants.

Materials and methods

Plant materials.

The intersubgeneric day blooming waterlily cultivar N. ‘Feitian 2’ were used as materials in this study. This cultivar was a hybrid of subgenus Anecphya as female parent and subgenus Brachyceras as male parent. Single flower of N. ‘Feitian 2’ could bloom for 6 days (D1 to D6), and the color was different everyday (Fig.  1 A). The petals (inner petals, middle petals, and outer petals) of N. ‘Feitian 2’ from D1 to D6 were collected at China National Botanical Garden/Institute of Botany, the Chinese Academy of Sciences, Beijing, China.

Petal color measurement

The color parameters of fresh petals (inner petals, middle petals, and outer petals) were measured with a spectrophotometer NF555 (Nippon Denshoku Industries Co. Ltd., Japan) at CIE C/28 illumination/viewer conditions. CIELAB was used to measure different aspects of flower color by L * , a * , and b * parameters. An average of five measurements was used. Then petals were snap-frozen in liquid nitrogen and stored at -80°C. Sampling was conducted with three biological replicates, to reduce analysis bias.

Flavonoids extraction, qualitative and quantitative analysis

The flavonoids extraction of petals (D1 to D6, mixture of inner petals, middle petals, and outer petals) was carried out as described by a previous study, with minor modification [ 26 ]. First, samples were freeze-dried before the experiment. Then approximately 0.05 g of freeze-dried petals were pulverized in liquid nitrogen, extracted with 1 mL of extracting solution (99.8:0.2, v/v, methanol: formic acid) in a test tube, sonicated with KQ-500DE ultrasonic cleaner (Ultrasonic instruments, Jiangsu Kunshan, China) at 20°C for 20 min, and then centrifuged in SIGMA 3K30 (SIGMA centrifuger, Germany) with 10,000 g for 10 min. The supernatants were collected into fresh tubes. We repeated the above operation for three times. All extracts were combined and filtered through 0.22 μm reinforced nylon membrane filters (Shanghai ANPEL, Shanghai, China) before the HPLC-DAD and HPLC-MS analyses. Three replicates were made for each sample. All concentrations used in this study were calculated from dry weight (DW).

An Agilent 1260 Infinity II LC system (Agilent Technologies, Santa Clara, CA, USA) was used for the analysis. The HPLC analysis was performed under the following conditions: column, Kromasil 100-5 C 18 column (250 mm × 4.6 mm; AKZO NOBEL, Sweden); solvent system, 2% formic acid aqueous solution (phase A) and 15% methanol acetonitrile (phase B); gradient program, 90:10 phase A/phase B at 0 min, 80:20 Phase A/phase B at 15.0 min, 77:23 phase A/phase B at 25.0 min, 60:40 phase A/phase B at 45.0 min, 10:90 phase A/phase B at 47.0 min, 10:90 phase A/phase B at 50.0 min; flow rate, 0.80 mL/min; temperature, 28 °C; injection volume: 10 µL. Chromatograms of anthocyanins and other flavonoids were acquired at 525 nm and 350 nm, respectively.

An Agilent 1260 Infinity II LC system coupled to an Agilent 6520 accurate-mass Q-TOF-MS/MS (Agilent Technologies, Santa Clara, CA, USA) was used for qualitative analysis. The liquid chromatographic conditions, mobile phase composition, and elution procedure were the same as those mentioned above. The following analysis conditions of mass spectrometry were adopted: the positive-ion (PI) mode for anthocyanins and negative-ion (NI) mode for other flavonoids; capillary voltage of 3.50 kV; nebulizer pressure of 0.103 MPa; desolvation gas (N 2 ) flow of 12 L/min; drying gas temperature of 350°C; scanning range of 50-2000 ( m/z ) units. Data capture and analysis were managed using Masshunter Qualitative Analysis Software B.04.00.

The contents of anthocyanins and other flavonoids were calculated using semi-quantitative standard Cyanidin 3- O -glucoside (Cy3G) and rutin. Mean values and SDs were calculated from three biological replicates.

RNA isolation, library construction and sequencing

Total RNA of D1 and D4 petals (mixture of inner petals, middle petals, and outer petals) was extracted using the E.Z.N.A. Plant RNA Kit (Omega Bio-tek, USA) according the instructions provided by the manufacturer. RNA integrity was assessed using the RNA Nano 6000 Assay Kit of the Agilent Bioanalyzer 2100 system (Agilent Technologies, CA, USA). RNA purity and concentration was measured using NanoDrop 2000 (Thermo Fisher Scientific, Wilmington, DE). A total amount of 1 µg RNA per sample was used as input material for the RNA sample preparations. Sequencing libraries were generated using Hieff NGS Ultima Dual-mode mRNA Library Prep Kit for Illumina (Yeasen Biotechnology (Shanghai) Co., Ltd.) following manufacturer’s recommendations and index codes were added to attribute sequences to each sample. Briefly, mRNA was isolated by Oligo (dT)-attached magnetic beads. Then mRNA was randomly fragmented into short fragments using fragmentation buffer and reverse transcribed into cDNA with random primers. Second-strand cDNA was synthesized with addition of PCR buffer, dNTPs, RNase H and DNA polymerase I. The cDNA fragments were purified with AMPure XP beads, end repaired, ‘A’ base added, and ligated to Illumina sequencing adapters. The ligation products were size selected by AMPure XP beads. In order to ensure the quality of library, Qubit 2.0 and Agilent 2100 were used to examine the concentration of cDNA and insert size. Q-PCR was processed to obtain a more accurate library concentration. At last, six libraries were sequenced on an Illumina NovaSeq platform to generate 150 bp paired-end reads, according to the manufacturer’s instructions (NCBI BioProject accession number: PRJNA1056490). The cDNA library construction and RNA-seq were performed by Biomarker Technologies Co., Ltd. (Beijing, China).

Transcriptome data analysis

Clean reads were obtained by removing reads containing adapter, reads containing ploy-N and low quality reads from raw data. These clean reads were then mapped to the N. colorata reference genome using the default parameters of Hisat2 software [ 22 ]. Gene function was annotated based on the following databases: Nr ( http://www.ncbi.nlm.nih.gov ), Pfam ( https://pfam.xfam.org/ ), KOG/COG ( http://www.ncbi.nlm.nih.gov/COG ), Swiss-Prot ( https://www.expasy.org/ ), KEGG database ( http://www.genome.jp/kegg ), and GO ( http://www.geneontology.org/ ). Fragments per kilobase of transcript per million mapped reads (FPKM) were used for transcription or quantification of gene expression levels. An absolute Log 2 FC ≥ 1 and false discovery rate (FDR) < 0.05 were used as thresholds for the identification of differentially expressed genes (DEGs) using DESeq2 software [ 28 ]. Gene Ontology (GO) enrichment analysis of the DEGs was implemented by the GOseq packages based Wallenius non-central hypergeometric distribution [ 29 ]. KOBAS database and clusterProfiler software were used to test the statistical enrichment of DEGs in KEGG pathways [ 30 ].

RT-qPCR expression analysis of genes involved in flavonoids biosynthesis

For the purpose of gene validation and expression analysis, 16 candidate genes related to flavonoid biosynthesis were subjected to real-time quantitative PCR (RT-qPCR) on ABI StepOnePlus™ Real-Time PCR System (Applied Biosystems, USA). cDNA synthesis and RT-qPCR were performed using EX RT Kit (gDNAremover) and 2×HQ SYBR qPCR Mix (Zomanbio, Beijing, China). Actin 11 was selected as an internal reference gene to normalize the expression data [ 31 ]. The gene-specific primers were shown in Supplementary Table S1 . The 2 −ΔΔCT method was used to quantify gene expression [ 32 ].

Correlation analysis of metabolite profiling and transcriptome

Mean and standard deviation for each sample were obtained from triplicate for further analysis. The heatmaps were performed by using TBtools [ 33 ]. Correlation analysis was performed by calculating the Pearson correlation coefficient (PCC with SPSS 21.0 (SPSS Inc., Chicago, IL)), and the screening criterion was PCC ≥ 0.80 or ≤ -0.80. Cytoscape (The Cytoscape Consortium, USA, version 3.9.1) was used to visualize the interaction networks.

Petal color phenotype analysis of Nymphaea ‘Feitian 2’ at different flowering stages

A single flower of Nymphaea ‘Feitian 2’ bloomed for six days above the water. The color of petals differs across flowering stages; even different petals possess different levels of discoloration (Fig.  1 A). In general, the outer petals change color first, while the inner petals change color beginning on day three after blooming (D3). Therefore, we divided the petals into inner petals, middle petals, and outer petals for color parameter determination. In the CIE L * a * b * color system, the parameter L * describes the lightness of the color, ranging from black (0) to white (100), the parameter a * represents green and red color from negative value to positive value, and the parameter b * represents blue and yellow color from negative value to positive value. The color coordinate values measured ranged across all petals as follows: L * from 38.20 to 84.88, a * from − 4.09 to 36.45, and b * from − 11.22 to 3.11 (Supplementary Table S2 ). In general, a gradual discoloration process for N. ‘Feitian 2’ was observed, as its L * , a * , and b * values were roughly distributed along a three-dimensional curve (Fig.  1 B). The colors of different petals were generally consistent, owing to the a * value and b * value of both inner, middle, and outer petals being consistent (Fig.  1 C).

Various flowering stages and flower color distribution in coordinate systems of N. ‘Feitian 2’. A, Various flowering stages; B, flower color distribution across coordinate systems of trivariate ( L * , a * , and b * ); C, a * and b * value distribution during different flowering stages. (D1-D6 represents the first to the sixth blooming day, respectively)

Identification and quantification of flavonoids

We examined the flavonoid metabolites present in the petals of N . ‘Feitian 2’ across six different flowering stages (D1-D6) to determine the cause of petals becoming increasingly purple-red throughout flowering. A total of 18 flavonoid metabolites were identified, including five anthocyanins and 13 flavonols (Fig.  2 A, Supplementary Table S3 ). The total anthocyanin contents (TA) accumulated constantly during anthesis over the first five days and decreased on the last day, with TA at D5 nearly 53 times higher than that at D1 (Fig.  2 B, C, Supplementary Table S4 ). Only two aglycones of anthocyanidin, delphinidin and cyanidin, were identified. The levels of delphinidin derivatives were higher than cyanidin derivatives, which was the highest in D1, reaching 88.57% of TA, and then gradually decreased, reaching 50% of TA (Supplementary Table S4 ).

Flavonols, including kaempferol derivatives (Km), quercetin derivatives (Qu), and myricetin derivatives (My) were also identified. The total flavonol contents (TF) were approximately 147.46-183.88 mg g − 1 DW, and the highest TF level was detected at D3. The changing trend of TF from D1 to D6 showed a bell curve trend, which first increased and then fell. Myricetin derivatives represented the main components of flavonols, accounting for more than 50% of TF, followed by quercetin derivatives (34.41% of TF at D2 and 36.70% of TF at D6). The levels of kaempferol derivatives were lower in the petals (Supplementary Table S4 ). Unlike anthocyanins, the alterations in flavonol content across different flowering stages were complex. There were three types of change curves for flavonol contents, including an initial decrease followed by an increase, continuously increasing, and initially increasing and then decreasing (Fig.  2 C).

Analysis of flavonoid metabolites in the petals of N. ‘Feitian 2’. A, HPLC chromatograms of flavonoid detected at 525 nm and 350 nm. B, anthocyanin and flavonol content accumulation in petals, encompassing cyanidin derivatives (Cy), delphinidin derivatives (Dp), kaempferol derivatives (Ka) and quercetin derivatives (Qu), and myricetin derivatives (My). Three independent biological experiments were conducted. Values represent means ± SD. C, heatmap diagram of the 18 flavonoid metabolites across six flowering stages

Correlation analysis indicated that 10 flavonoids were significantly correlated with color parameters, including five anthocyanins and five flavonols (Supplementary Figure S1 ). Anthocyanins were significantly negatively correlated with the L * value, positively correlated with the a * value in both inner petals, middle petals and outer petals. And only negatively correlated with the b * value in the inner petals. While there was no significant correlation with the middle or outer petals. The flavonols that were significantly correlated with color parameters were quercetin-3- O -galactoside (f2), myricetin 3- O -(3’’- O -acetyl)-rhamnoside (f4), quercetin 3- O -(3’’- O -acetyl)-rhamnoside (f8), kaempferol 3- O -(3’’- O -acetyl)-rhamnoside (f10), kaempferol 3- O -(3’’- O -malonyl) -rhamnoside (f13). Among them, f2 and f13 were only positively correlated with the a * value of outer petals. In contrast, f4, f8, and f10 were negatively correlated with the L * value and positively correlated with the a * value of all petals.

According to the changes of flavonoids across different stages, all anthocyanins exhibited the largest changes in content. Delphinidin 3’- O -(2’’- O -galloyl-6’’- O -acetyl-galactoside) (a3) exhibited the lowest content among all anthocyanins, and its content increased nearly 5.74-fold, from 0.0629 mg g − 1 DW at D1 to 0.3612 mg g − 1 DW at D6 (Supplementary Table S4 ). In contrast, the five flavonols (f2, f4, f8, f10, and f13) were not changed as considerably as the anthocyanins. These results indicated that N . ‘Feitian 2’ flower color change is closely tied to the accumulation of five anthocyanins.

RNA-Seq analysis

To delve deeper into the molecular mechanism of waterlily flower color changes during anthesis, six libraries (D1-1, D1-2, D1-3, D4-1, D4-2, and D4-3) were developed using N. ‘Feitian 2’ at two different flowering stages, replicated three times. After cleaning and quality control, approximately 64.36 Gb of clean data were obtained, and each library produced no less than 10.33 Gb of clean data. The Q30% of all libraries was over 92% (Supplementary Table S5 ). Between 62.92 and 64.73% of the sequenced reads could be aligned to the waterlily reference genome (Supplementary Table S5 ) [ 22 ]. Using an absolute Log 2 FC ≥ 1 and FDR < 0.01 as filter criteria for differentially expressed genes (DEGs), a total of 2,912 DEGs were found in D1 vs. D4, including 1,220 up-regulated DEGs and 1,692 down-regulated DEGs (Supplementary Figure S2 ). Therefore, a large number of genes may participate in petal color changing in N . ‘Feitian 2’.

To characterize the major functional categories of the DEGs, Gene Ontology (GO) enrichment analysis was performed. In total, 2,912 DEGs were distributed across three gene ontology categories: cellular component, biological process, and molecular function. In detail, the ‘metabolic process,’ ‘cellular process,’ and ‘single-organism process’ were the most enriched terms in biological processes. For the cellular component category, ‘membrane,’ ‘membrane part,’ and ‘cell’ were the most abundant proportions. Under the molecular function category, ‘catalytic activity,’ ‘binding,’ and ‘transporter activity’ were the most represented (Supplementary Figure S3 ).

Pathway analysis assists in understanding biological functions and gene interactions. Our findings demonstrated that pathways with the highest DEG representations were plant hormone signal transduction (ko00340), followed by starch and sucrose metabolism (ko00500) and phenylpropanoid biosynthesis (ko00940). The classification indicated that a large number of genes were enriched in ‘flavonoid biosynthesis’ (ko00941), ‘flavone and flavonol biosynthesis’ (ko00944), and ‘anthocyanin biosynthesis’ (ko00942), which were important for petal coloration (Fig.  3 ).

Bar chart depicting the top 20 genes analyzed using Kyoto Encyclopedia of Genes and Genomes (KEGG) terms enriched in differentially expressed genes (DEGs) in N. ‘Feitian 2’

Combined metabolomic and transcriptomic analysis

By integrating data from metabolomics and transcriptomics analyses, the flavonoid biosynthesis in N. ‘Feitian 2’ petals was revealed. We explored the genes of flavonoids, especially the anthocyanin biosynthesis pathway, and uncovered the key genes of flavonoid metabolism in the petals of N. ‘Feitian 2’ to analyze the mechanism of altered flower color. A total of 159 unigenes encoding nine enzymes involved in the above three pathways were the study focus (Table  1 ). We analyzed transcriptional profiles for the genes involved in flavonoid metabolism between D1 and D4 to identify the key genes for color changing. The results indicated that a total of 26 key unigenes not only had different expression levels but also FPKM values ≥ 10, including 19 up-regulated and seven down-regulated unigenes (Supplementary Table S6 ).

All identified DEGs contained both upstream genes ( CHS , CHI , etc.) and downstream genes ( UFGT , etc.) (Fig.  4 ). The majority of upstream genes, CHS , CHI , and F3H , were expressed higher at D4. However, LOC116265581 ( CHS -2), LOC116245897 ( F3H -1), and LOC116263301 ( F3H -3) had higher expression levels at D1. F3’H , F3’5'H , DFR , and ANS were all expressed more highly at D4, which was consistent with the accumulation of anthocyanins. FLS and UFGT were key enzyme genes for flavonoid biosynthesis and modification. Among them, the expression level of LOC116261229 ( FLS ) was higher at D1, consistent with the trend of flavonol content. Additionally, LOC116249850 ( UFGT -3), LOC116254426 ( UFGT -7), and LOC116265943 ( UFGT -11), whose expression levels were higher at D1, might be the key genes for the modification of flavonol compounds. The expression of the remaining eight genes of UFGT s was higher at D4 than at D1, wherein LOC116247679 ( UFGT- 2), LOC116253945 ( UFGT- 4), and LOC116257005 ( UFGT- 8) possessed higher FPKM values, and may represent the key unigenes related to anthocyanin modification. These suggested that the color alteration of waterlily petals was triggered by the co-expression of many unigenes.

Evaluation of DEGs in the flavonoid biosynthesis pathway. CHS, chalcone synthase; CHI, chalcone isomerase; F3H, flavanone 3-hydroxylase; F3’H, flavonoid 3 '- hydroxylase; F3’5'H, flavonoid 3’5'-hydroxylase; FLS, flavonol synthase; DFR, dihydroflavonol reductase; ANS, anthocyanidin synthase; UFGT, Flavonoid 3- O -glucosyltransferase

Correlation analysis evaluated the correlation between the 26 DEGs mentioned above and five anthocyanins correlated with flower color change. Correlation analysis (Fig.  5 ) indicated that 19 DEGs were significantly positively correlated with five anthocyanins, including one CHS , three CHI , one F3H , one F3’H , two F3’5'H , one DFR , two ANS , and eight UFGT . In contrast, seven DEGs were significantly negatively correlated with five anthocyanins. After analyzing the expression levels of 19 positively correlated genes (Supplementary Table S6 ), we selected 12 candidate key structural genes, including LOC116265292 ( CHS -1), LOC116256153 ( CHI -1), LOC116262004 ( CHI -3), LOC116246718 ( F3H -2), LOC116257842 ( F3’H ), LOC116260989 ( F3’5'H -1), LOC116268364 ( DFR ), LOC116249327 ( ANS -1), LOC116260841 ( ANS -2), LOC116247679 ( UFGT -2), LOC116253945 ( UFGT -4), and LOC116257005 ( UFGT -8).

Co-expression network of DEGs in structure genes and flavonoid metabolism. The dark gray edges indicate a positive correlation, and the light gray indicates a negative correlation. a1, delphinidin 3- O -galactoside; a2, cyanidin-3- O -glucoside; a3, delphinidin 3’- O -(2’’- O -galloyl-6’’- O -acetyl-galactoside); a4, delphinidin-3- O -(6’’- O -acetyl)-galactoside; a5, cyanidin-3- O -(6’’- O -acetyl)-galactoside

RT-qPCR analysis

According to the correlation analysis using key flavonoids and expression level, 12 candidate enzyme genes were selected for RT-qPCR. The expression of these candidate genes increased continuously from D1 to D4 (Fig.  6 ), mirroring the trend measured in the transcriptome, indicating the accuracy of the sequencing data.

Relative expression levels of 12 candidate genes in the flavonoid biosynthetic pathway by RT-qPCR analysis. Data are presented as means ± SD

All 12 candidate genes had similar expression patterns, and their expression curves were “bell curves,” following an upward trend first, reaching the maximum level, and then exhibiting a downward trend. While the expression curves were similar, there were some differences. The expression levels of LOC116265292 ( CHS -1), LOC116256153 ( CHI -1), LOC116249327 ( ANS -1), and LOC116260841 ( ANS -2) were the highest at the D4 stage. The expression levels of LOC116262004 ( CHI -3), LOC116246718 ( F3H -2), LOC116257842 ( F3’H ), LOC116260989 ( F3’5'H -1), LOC116268364 ( DFR ), LOC116247679 ( UFGT -2), and LOC116253945 ( UFGT -4) were the highest at the D5 stage. The expression level of LOC116257005 ( UFGT- 8) was the highest at the D2 stage. This indicates that UFGT -8 may be associated with flavonol synthesis. Among these genes, CHI -3, and F3H -2 had the most rapid change at different stages. Subsequently, F3’H , F3’5'H -1, ANS -1, and ANS -2 rapidly changed at different stages. CHS -1, CHI -1, DFR , UFGT -2, and UFGT -4 exhibited smaller changes during D1 to D6. The differential expression of structural genes could result in different flower colors of N . ‘Feitian 2’ across different flowering stages, among which the most important structural genes were CHI -3, F3H -2, F3’H , F3’5'H -1, ANS -1, and ANS -2.

Specific transcription factor analysis

Transcription factors (TFs) execute critical roles in the growth and development of plants by modulating gene expression. Our data revealed a total of 1,208 unigenes predicted as TFs. A total of 104 transcription factors (FPKM value ≥ 10) with different expression levels were identified (Supplementary Table S7 ). Among these transcription factors, the most abundant were MYB (17), followed by AP2 / ERF (14), bHLH (14), and WRKY (10). The TFs associated with regulating the expression of flavonoid structural genes were mainly MYB, bHLH, and WDR [ 34 , 35 , 36 , 37 ]. A total of 17 MYB , 14 bHLH , and 3 WDR unigenes were identified in our data. By constructing a phylogenetic tree alongside Arabidopsis , three MYBs , including LOC116245731 ( MYB-1 ), LOC116259798 ( MYB-2 ), and LOC1 16261829 ( MYB-3 ) were analyzed as crucial regulatory genes, as they were clustered together with MYB , related to the regulation of flavonoid biosynthesis in Arabidopsis thaliana (S4, S5, S6, and S7) (Fig.  7 A) [ 38 ]. These three candidate regulatory genes were examined through RT-qPCR. These genes exhibited similar expression curves, known as a “bell curve” trend. The expression level of LOC116245731 ( MYB - 1 ) was the highest at the D4 stage, however LOC116259798 ( MYB - 2 ), and LOC116261829 ( MYB - 3 ) were the highest at the D5 stage. LOC116261829 ( MYB - 3 ) exhibited the most rapid change from D1 to D6 among three candidate regulatory genes. MYB may act as the mainly transcription factor in N . ‘Feitian 2’, as phylogenetic tree analysis identified that the candidate bHLHs did not converge with the S29 (IIIf subgroup), related to the regulation of flavonoid biosynthesis in Arabidopsis thaliana (Supplementary Figure S4 ) [ 39 , 40 ].

Phylogenetic tree and relative expression levels of MYB s derived from N. ‘Feitian 2’. A, phylogenetic tree of MYB s with Arabidopsis . B, relative expression levels of three MYB s

Flavonoids, particularly anthocyanins, are vital in plant survival as attractants of pollinators and protectors in various stress situations [ 41 ]. To carry out their roles, they are typically produced transiently, undergoing regulated accumulation or degradation. Anthocyanin degradation causes color changes from deep to light, and the degradation mechanism is more comprehensively understood in Brunfelsia calycina , Brunfelsia acuminata , and Nelumbo ‘Qiusanse’ [ 9 , 16 , 42 , 43 ]. Although much is known about anthocyanin biosynthesis, the mechanism of flower color change in each species differs, and as a basal angiosperm, the mechanism of flower color change in waterlilies remains unclear.

In many plants, the color of flower petals varies from light to deep, primarily due to the accumulation of anthocyanins. In Rhododendron simsii , for instance, the cyanidin biosynthesis pathway is activated to generate a red color [ 44 ]. Similarly, in the Japanese tree peony cultivar ‘Taiyoh,’ the pelargonidin biosynthesis pathway is activated in petals, resulting in a vivid red color [ 45 ]. In Tulipa gesneiana ‘Queen of night,’ the accumulation of anthocyanins (delphinidin 3- O -rutinoside, cyanidin 3- O -rutinoside, and pelargonidin 3- O -rutinoside) triggers a color change from green to black [ 46 ]. The shift in the waterlily cultivar ‘King of Siam’ petal in color from colorless to violet-blue throughout development is believed to have been caused by the cyanidin and delphinidin biosynthesis pathway [ 26 ]. Coloration operates as a gradual process, and many flowers have concluded coloration before opening, while some flowers undergo coloration after receiving certain signals, such as Nymphaea ‘Feitian 2,’ which begins coloration after opening. The anthocyanin accumulation in petals plays a crucial role in the coloration process. This study detected flavonoids in N. ‘Feitian 2’ petals over D1 to D6. A total of 18 flavonoids were characterized, including 13 flavonols and five anthocyanins (Table S3 ). Anthocyanins accumulated from D1 to D5, then reduced at D6, while flavonols accumulated from D1 to D3, then were reduced from D4 to D6 (Fig.  2 ). Only cyanidin derivatives and delphinidin derivatives were identified, which was consistent with the findings of other research [ 25 , 47 , 48 ]. While anthocyanidins are simple, glycosylation and acylation modification of anthocyanins were extensively present, producing rich and varied colors in waterlilies.

Anthocyanins are produced at the end of the phenylpropanoid metabolic pathway, and the precursors of anthocyanin biosynthesis are malonyl-CoA and coumaroyl-CoA. Most anthocyanins are synthesized via CHS and CHI condensation; F3H, F3’H, or F3’5'H oxidation; DFR and ANS/LDOX catalysis; GT, and AT modification [ 4 , 6 ]. In our study, we conducted a transcriptome analysis of N . ‘Feitian 2’ at two stages (D1 and D4), and screened 26 enzyme genes that were significantly differentially expressed (Table  1 ; Fig.  4 ). Among these, 19 were up-regulated genes, and the remaining genes were down-regulated. DFR and ANS act as critical enzymes in the anthocyanin pathway that play an essential role in converting dihydroflavonol to anthocyanidins [ 49 ]. We identified five DFR genes, of which only one gene was up-regulated. Two ANS genes were detected, and all were up-regulated, aligned with the pattern of floral color development. Cyanidin and delphinidin undergo further glycosylation under the action of GTs to achieve stability [ 50 ]. Moreover, GTs make important contributions to flower color formation. The bicolor nature of the lotus ‘Dasajin’ is primarily caused by the defective accumulation of the gene NnUFGT2 in the white portion of its petals, preventing the formation of glycosylated anthocyanins in the final metabolic step for flower color [ 51 ]. In Lobelia erinus , rhamnosylation is an essential process for lobelinin synthesis, and the expression of RT (ABTR2 and ABTR4) is required for the blue color of Lobelia flowers [ 52 ]. The formation of peony red flowers also relies on the action of GTs [ 45 ]. UFGT homologous unigenes were identified in N . ‘Feitian 2,’ with 11 differentially expressed, eight up-regulated, and three down-regulated (Table  1 ). Correlation analysis demonstrated that eight up-regulated unigenes had a positive correlation with flower color formation. Among them, LOC116247679 (UFGT-2), LOC116253945 (UFGT-4), and LOC116257005 (UFGT-8) had higher FPKM values, which may be critical unigenes related to anthocyanin modification.

Anthocyanin biosynthesis is predominantly regulated by transcription factors at the transcriptional level. Currently, many kinds of transcription factors, including MYB, bHLH, WD40, DOF, MADS-box, and WRKY proteins, have been found to modulate anthocyanin biosynthesis [ 53 , 54 , 55 , 56 ]. Among them, MYB transcription factors exert a crucial influence on the regulation of flower color. MYB transcription factors can act independently. For instance, AtPAP1 and AtPAP2 both act as master regulators controlling anthocyanin biosynthesis in Arabidopsis thaliana [ 57 , 58 ]. MYB TFs can also interact with other MYB transcription factors to carry out their functions. For example, PrMYBa1was found to activate PrF3H by interacting with PrMYBa2 to generate an ‘MM’ complex in red-purple blotches formation of Paeonia rockii ‘ShuShengPengMo’ [ 59 ]. In addition, MYB can bind to bHLH or create MBW complexes with bHLH and WDR. In Actinidia chinensis , the AcMYBF110-AcbHLH1-AcWDR1 complex directly targeted the promoters of anthocyanin synthetic genes to promote fruit color formation [ 60 ]. In this study, we examined the transcriptome data and found that 104 important transcription factors, including MYB, AP2/ERF, WRKY, bHLH, WD40, NAC, bZIP, and others, displayed significantly different expression levels between D1 and D4 (Supplementary Table S6 ). MYB transcription factors were chosen for phylogenetic analysis. LOC116245731 ( MYB-1 ), LOC116259798 ( MYB-2 ), and LOC116261829 ( MYB-3 ) were clustered together with MYB, which were associated with the regulation of flavonoid biosynthesis in A. thaliana (Fig.  7 B) [ 38 ]. We speculated that these three transcription factors may be candidate regulators of anthocyanin biosynthesis in N . ‘Feitian’ flowers.

In this study, flavonoids at different flowering stages and transcriptome data were utilized to reveal the discoloration of N. ‘Feitian 2’ petals. There were 18 flavonoids identified in the petals. The variation of the content of five detected anthocyanins was a chemical mechanism that contributed to the change in flower color. Moreover, a total of 26 differentially expressed genes (DEGs) of structural genes in the flavonoid biosynthesis pathway were uncovered. Among them, six structural genes were identified as candidate genes, as they were not only significantly positively correlated with anthocyanin accumulation, but also had rapid change during different flowering stages. Furthermore, 104 differentially expressed transcription factors (TFs) were identified, and three MYBs associated with flavonoid biosynthesis were screened via sequence phylogenetic analysis. These findings can help clarify the molecular mechanism and regulatory networks of flower discoloration in waterlilies and provide a biological basis for the breeding of novel cultivars.

Data availability

All relevant supporting data sets are included in the article and its supplemental files. The raw RNA-seq data have been submitted to the SRA database under accession number PRJNA1056490, and they can also be freely available at: https:// www. ncbi. nlm. nih. gov/sra/PRJNA1056490.

Abbreviations

High-performance liquid chromatography

Fragments per kilobase of exon model per million mapped reads

False discovery rate

Kyoto Encyclopedia of Genes and Genomes

Gene Ontology

Total anthocyanin contents

Total flavonol contents

Cyanidin derivatives

Delphinidin derivatives

Kaempferol derivatives

Quercetin derivatives

Myricetin derivatives

Cyanidin 3- O -glucoside

Chalcone synthase

Chalcone isomerase

Flavanone 3-hydroxylase

Flavonoid 3’-hydroxylase

Flavonoid 3’5'-hydroxylase

Flavonol synthase

Dihydroflavonol 4-reductase

Anthocyanidin synthase

Flavonoid 3- O -glucosyltransferase

Leucoanthocyanin dioxygenase

V-myb avian myeloblastosis viral oncogene homolog

Basic helix-loop-helix

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This study was financially supported by the National Natural Science Foundation of China (Grant No. 32102413) and Biological Resources Programme CAS (KFJ-BRP-017-44).

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Xian Zhou, Xiaohan Wang, Haohui Wei, Huijin Zhang, Qian Wu & Liangsheng Wang

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QW conceived and designed the experiments. XZ performed the experiments. XHW and HHW analyzed the data. HJZ cultivated the waterlily plants. QW and XZ wrote the manuscript. LSW reviewed and edited the manuscript. All authors contributed to the article and approved the final manuscript.

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Zhou, X., Wang, X., Wei, H. et al. Integrative analysis of transcriptome and target metabolites uncovering flavonoid biosynthesis regulation of changing petal colors in Nymphaea ‘Feitian 2’. BMC Plant Biol 24 , 370 (2024). https://doi.org/10.1186/s12870-024-05078-5

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RNA Processing in Chronic Diseases

RNA-binding protein transcripts as potential biomarkers for detecting Primary Sclerosing Cholangitis and predicting its progression to Cholangiocarcinoma Provisionally Accepted

• 1 Department of Veterinary Sciences, School of Agriculture and Veterinary Medicine, University of Turin, Italy
• 2 CNR Institute of Biostructures and Bioimages, Italy

The final, formatted version of the article will be published soon.

Primary Sclerosing Cholangitis (PSC) is a persistent inflammatory liver condition that affects the bile ducts and is commonly diagnosed in young individuals. Despite efforts to incorporate various clinical, biochemical and molecular parameters for diagnosing PSC, it remains challenging, and no biomarkers characteristic of the disease have been identified hitherto. PSC is linked with an uncertain prognosis, and there is a pressing need to explore multiomics databases to establish a new biomarker panel for the early detection of PSC's gradual progression into Cholangiocarcinoma (CCA) and for the development of effective therapeutic interventions. Apart from non-coding RNAs, other components of the Ribonucleoprotein (RNP) complex, such as RNA-Binding Proteins (RBPs), also hold great promise as biomarkers due to their versatile expression in pathological conditions. In the present review, an update on the RBP transcripts that show dysregulated expression in PSC and CCA is provided. Moreover, by utilizing a bioinformatic data mining approach, we give insight into those RBP transcripts that also exhibit differential expression in liver and gall bladder, as well as in body fluids, and are promising as biomarkers for diagnosing and predicting the prognosis of PSC. Expression data were bioinformatically extracted from public repositories usingTCGA Bile Duct Cancer dataset for CCA and specific NCBI GEO datasets for both PSC and CCA; more specifically, RBPs annotations were obtained from RBP World database. Interestingly, our comprehensive analysis shows an elevated expression of the non-canonical RBPs, FANCD2, as well as the microtubule dynamics regulator, ASPM, transcripts in the body fluids of patients with PSC and CCA compared with their respective controls, with the same trend in expression being observed in gall bladder and liver cancer tissues. Consequently, the manipulation of tissue expression of RBP transcripts might be considered as a strategy to mitigate the onset of CCA in PSC patients, and warrants further experimental investigation. The analysis performed herein may be helpful in the identification of non-invasive biomarkers for the early detection of PSC and for predicting its progression into CCA. In conclusion, future clinical research should investigate in more depth the full potential of RBP transcripts as biomarkers for human pathologies.

Keywords: primary sclerosing cholangitis, Cholangiocarcinoma, RNA-Binding Proteins, extracellular vesicles, biomarkers, Data Mining, bioinformatics

Received: 19 Feb 2024; Accepted: 13 May 2024.

Copyright: © 2024 Ala and Fagoonee. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Prof. Ugo Ala, Department of Veterinary Sciences, School of Agriculture and Veterinary Medicine, University of Turin, Turin, Italy Dr. Sharmila Fagoonee, CNR Institute of Biostructures and Bioimages, Turin, Italy

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Annotated primary scientific literature: A pedagogical tool for undergraduate courses

Affiliations Department of Biological Sciences, Florida International University, Miami, Florida, United States of America, STEM Transformation Institute, Florida International University, Miami, Florida, United States of America

* E-mail: [email protected]

• Matthew Kararo, 
• Melissa McCartney

Published: January 9, 2019

• https://doi.org/10.1371/journal.pbio.3000103
• Reader Comments

Annotated primary scientific literature is a teaching and learning resource that provides scaffolding for undergraduate students acculturating to the authentic scientific practice of obtaining and evaluating information through the medium of primary scientific literature. Utilizing annotated primary scientific literature as an integrated pedagogical tool could enable more widespread use of primary scientific literature in undergraduate science classrooms with minimal disruption to existing syllabi. Research is ongoing to determine an optimal implementation protocol, with these preliminary iterations presented here serving as a first look at how students respond to annotated primary scientific literature. The undergraduate biology student participants in our study did not, in general, have an abundance of experience reading primary scientific literature; however, they found the annotations useful, especially for vocabulary and graph interpretation. We present here an implementation protocol for using annotated primary literature in the classroom that minimizes the use of valuable classroom time and requires no additional pedagogical training for instructors.

Citation: Kararo M, McCartney M (2019) Annotated primary scientific literature: A pedagogical tool for undergraduate courses. PLoS Biol 17(1): e3000103. https://doi.org/10.1371/journal.pbio.3000103

Copyright: © 2019 Kararo, McCartney. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This research was supported through National Science Foundation Division of Undergraduate Education 1525596 (MM) and Florida International University College of Arts, Sciences & Education Postdoctoral Fellowship (MM and MK). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Abbreviations: CREATE, consider, read, elucidate the hypotheses, Analyze and interpret the data, and think of the next experiment; FIU, Florida International University; SitC, Science in the Classroom; STEM, science, technology, engineering, and math; TOSLS, Test of Scientific Literacy Skills

Provenance: Not commissioned; externally peer reviewed.

A major output of public research universities is primary scientific literature, in addition to educating students and conferring degrees. It is imperative for researchers and universities to increase the transparency and outreach of the primary research literature they produce. However, most primary scientific literature remains unknown and/or inaccessible to the public, because it is published in journals targeting academics in the same field and is often placed behind journal paywalls [ 1 ].

Public research universities also have a responsibility to produce scientifically literate graduates [ 2 , 3 ]. Many students graduate without an understanding of scientific practices and an acculturation to interpreting scientific communication, especially primary scientific literature [ 4 , 5 ]. One way to potentially improve scientific literacy overall and develop specific skills, such as interpreting scientific communication, is to incorporate primary scientific literature into the undergraduate curricula and provide pedagogical tools that may help bridge the divide between everyday language and the language used by experts [ 6 – 11 ].

The study of primary scientific literature as a pedagogical tool in undergraduate biology courses has led to innovative approaches. The most well-known of these may be the Consider, Read, Elucidate the hypotheses, Analyze and interpret the data, and Think of the next Experiment (CREATE) method, in which faculty redesign their existing courses around primary scientific literature in order to provide an intensive and comprehensive analysis of primary scientific literature for undergraduates [ 6 , 12 – 14 ]. Although this type of a semester-long innovative elective course provided student benefits, adding an entire course to a degree sequence may prove difficult and by definition, does not impact students that choose not to include them in an already credit-crunched plan of study. This credit-crunch is especially prevalent at institutions such as the one in this study, Florida International University (FIU), where any additional credit hours are charged at out-of-state tuition rates. Therefore, it would benefit biology education, and biology as a field of study, to develop innovative ways to utilize primary scientific literature as a pedagogical tool, ideally with a minimal impact to existing plans of study and time investment from course instructors.

A growing body of research shows that less-intensive interventions using primary scientific literature can be valuable and useful in science, technology, engineering, and math (STEM) education, with the greatest amount of research happening at the undergraduate level. Programs include journal clubs, data and figure exploration, and tutorials on how to read primary scientific literature [ 15 – 17 ]. Assessment tools used to evaluate these interventions are equally as diverse, ranging from rubrics to validated surveys [ 18 , 19 ].

Annotated primary scientific literature

Annotated primary scientific literature is designed to help readers interpret complex science by overlaying additional information on a scientific research article. Preserving the original text and its context is what makes annotated primary scientific research literature unique from other genres that modify or rewrite the original text. This preservation is the key difference between annotated primary scientific literature and adapted primary literature, an approach that takes portions of primary scientific literature and rewrites the original content to turn them into pedagogical tools [ 20 ]. Science in the Classroom (SitC; www.scienceintheclassroom.org ) is a highly developed and sophisticated example of annotated primary scientific literature that we decided has potential for classroom pedagogical use.

SitC, a collection of freely available annotated papers, aims to make primary scientific research literature more accessible to students and educators. The repository of annotated primary scientific literature articles is accessible to educators and searchable by keyword, classified by topics, and grouped in collections. The process of reading and deconstructing scientific literature in undergraduate courses has been shown to result in students potentially gaining an understanding of scientific practices, such as how scientists design their experiments and present their results, essentially allowing students to experience the logic behind drawing conclusions from a set of data [ 6 , 7 , 12 – 14 ].

Annotated primary scientific literature uses the original text of research articles along with a “Learning Lens” overlay, designed to provide students tools to use for interpretation. The “Learning Lens” is used to selectively highlight different parts of the text and is composed of seven headings: Glossary, Previous work, Author's experiments, Conclusions, News and policy links, Connect to learning standards, and References and notes, which are color-coded to match the corresponding text of the research article. For example, an annotated glossary term, when clicked on, will produce a pop-up box containing the definition of the word ( Fig 1 ). Annotations contained within the “Learning Lens” have been designed to be at the reading comprehension level of a first-year undergraduate student, and ongoing evaluation efforts have provided evidence that this goal is being met [ 21 ].

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https://doi.org/10.1371/journal.pbio.3000103.g001

Annotated primary literature as a pedagogical tool

Annotations provide an educational scaffold that could help students become more comfortable with reading scientific papers. We propose annotated primary scientific literature as an example of a resource that can be incorporated into existing courses and provide scaffolding that may help undergraduate students develop skills necessary to read primary scientific literature while requiring a minimal time investment from instructors. Using annotated primary scientific literature as a pedagogical tool not only could potentially help universities develop scientifically literate graduates, but it may also broaden the impact of primary scientific research literature produced by faculty.

The previously mentioned pedagogical tools and curriculum transformations can require a substantial investment of time and effort from the university, faculty, and staff. Therefore, additional tools and opportunities should be considered in order to achieve a wider variety of complementary opportunities for teaching with authentic scientific practices and engaging students in reading primary scientific literature [ 22 ]. We hypothesize that the incorporation of annotated primary scientific literature in the classroom represents one of these opportunities.

In this pilot study, we had a goal of developing an implementation protocol that could incorporate annotated primary scientific literature into undergraduate courses with a minimal time investment for instructors and minimal disruption and alteration to existing courses and plans of study.

Implementation of annotated primary scientific literature

All data were collected in accordance with an approved FIU Institutional Review Board protocol #17–0398 and #17–0105. Our initial attempts to develop an implementation protocol for using annotated primary scientific literature as a pedagogical tool had the educational goal of introducing students to the “Learning Lens” annotations and observing how instructors and students used the tool. Initial attempts to incorporate annotated primary scientific literature focused on undergraduate biology courses at FIU, including General Biology II, Ecology, and Plant Life History. The implementation sessions were run iteratively during the same semester, ensuring that students did not overlap, and each class had only one implementation session. We describe two variations of our implementations here.

Students involved in the study self-reported their major, with 76% being biology majors. We did not collect any data on students’ prior knowledge of biology, but the majority of students in these classes are first- or second-year students.

We used the same annotated piece of primary scientific literature for all in-class activities described in this study: “Caffeine in floral nectar enhances a pollinator's memory of reward” ( https://tinyurl.com/k7m329g ). We chose an article that incorporated many different aspects of biology, including evolution, ecosystem interactions, basic botany, learning and memory, and animal behavior in a single study, making this paper applicable in a wide variety of undergraduate courses.

The objectives were to introduce undergraduate students to annotated primary scientific literature and collect baseline data on how students interacted with the annotations themselves. The first implementation involved a one-time intervention, connected to the student’s coursework, conducted by the researchers and began with an approximately 5-minute orientation to annotated primary scientific literature. This orientation included how to use the “Learning Lens” and a brief overview of the importance of primary scientific literature. Students were then given 20 minutes to read the selected piece of annotated primary scientific literature. At the 20-minute time point, a Qualtrics (online survey software; Provo, Utah and Seattle, Washington) link was provided, and if they were done reading, students could begin answering the feedback questionnaire. Students were given an additional 20 minutes to complete the questionnaire. Collecting and analyzing this first round of pilot data allowed for reflection on opportunities for iterative improvement.

In addition to the questionnaire data, feedback was collected through in-class activity observations conducted by the researchers. We kept detailed field notes indicating when students appeared on task, i.e., independently interacting with annotated primary scientific literature. We also noted when alternative tasks were observed, i.e., students checking email or social media, and when task completion appeared to have occurred. During the implementation, our in-class observations estimated an average time on task, i.e., interacting with annotated primary scientific literature, to be 10 minutes, because there was a noticeable increase in classroom noise after this time point. We confirmed this by using Adobe Analytics (Adobe, San Jose, California), which measures the time spent on a website by each user. We measured an average time spent on annotated primary scientific literature of 13 minutes. Due to limitations of Adobe Analytics, we are unable to collect individual data points and were limited to an aggregate average for the entire class. Note that the difference between the observed time spent on the activity and the digital measure can be explained by Adobe Analytics averaging all participants’ time spent on the article page.

The main student feedback was collected through a questionnaire containing both quantitative (content questions) and qualitative items (i.e., “what did you like about this activity?”). One of the key ideas we garnered from the qualitative data was that a one-time intervention was perceived by students as somewhat discordant when a connection between the article they read and the content they were covering at the time in their course was not made explicit by their course instructor ( Table 1 ).

https://doi.org/10.1371/journal.pbio.3000103.t001

When asked if the topic of the paper related to their course, students in this iteration gave feedback such as this activity was “only slightly relevant to the course,” and “no, we[‘re] studying plants” despite the article being explicitly about caffeine production by plants in order to attract pollinators. Additionally, we were uncertain that we had connected with the students as researchers in the same way as the instructor with whom the students had built a relationship.

Although some students may have not perceived a connection between the article content and their course content, in general, students found the annotations useful, especially regarding graphs and vocabulary interpretation. Examples of student responses can be seen in Table 2 .

https://doi.org/10.1371/journal.pbio.3000103.t002

For our second iteration, we decided to address the issues of students feeling discordant by having the course instructors introduce the article and annotated primary scientific literature activity themselves. Additionally, we asked instructors to explicitly connect the annotated paper to current course content. With both of these procedures in place, the average time students engaged with the annotated article, as measured by Adobe Analytics, increased to 19 minutes ( Fig 2 ).

https://doi.org/10.1371/journal.pbio.3000103.g002

This new implementation, in which the instructor introduced the piece of annotated primary scientific literature and annotated primary scientific literature activity, not only appeared to increase the time that students engaged with the material, but it also removed the manpower requirement for the researchers to be present in every classroom in order to describe and implement the activity. This could allow for a more widespread implementation of annotated primary scientific literature as a pedagogical tool. It was also apparent that students introduced to the activity by their course instructor were more readily able to recognize the connections between reading primary scientific research literature and their course content, which can be seen in student responses in Table 3 .

https://doi.org/10.1371/journal.pbio.3000103.t003

When asked if the topic of the paper related to their course, students in this iteration stated “This article related to 3 different courses I am taking this semester,” “yes it most certainly did,” “yes! We’re learning about pollination,” and that “…scientific papers on new experiments …are important.”

During the initial iterations of the implementation protocol, students read the annotated articles and completed an assessment during class time. However, a growing concern was feasibility of an in-class assignment due to the time requirement and allowing for instructor flexibility in scheduling. While observing a senior lecturer at FIU, who was not involved in this current study, and his existing implementation method of students reading primary scientific literature as homework and answering iClicker questions at the beginning of the following class, the researchers noticed an increased enthusiasm among the students during the class discussion. Supporting this observation, the history of research on the use of clickers in the classroom shows an increase in feelings of class involvement [ 23 ] and learning gains in students [ 24 ]. Because of the observations and support from instructors, the decision was made to adopt the homework protocol moving forward with future implementations. The homework protocol allows for more instructor freedom in selecting articles relevant to course content, reduces the class time required for implementation, and separates content questions from a pre–post attitude and motivation questionnaire. Using articles as homework also allows for instructors to utilize as many articles as they wish, but for this project moving forward, in future implementations, we will require a minimum of three articles over the course of a semester. We are currently piloting an implementation protocol using annotated primary scientific literature as a homework assignment and are excited to see how instructors and students use annotated primary scientific literature moving forward.

Advice to others

In the ongoing iterative development of an implementation protocol for annotated primary scientific literature, the most fruitful exercise has been reflection. This is great practice for any educator or educational researcher during the curriculum or pedagogical tool development process. Reflection on early classroom implementations helped us identify the opportunities for improvement in our subsequent protocol iterations and allowed us to make modifications based upon quantitative, qualitative, and observational data. One example of changes coming from reflection was noticing that during an implementation, students were opening the assessment without reading the article and using the “find” feature within the article to find answers to assessment questions. This led to preventing entry into the assessment until the time for reading had elapsed. Our subsequent classroom observations showed us that this forced students to interact with the article and be more thoughtful about their answers to the assessment, i.e., answers were not cut-and-pasted from the article text. We advise others to continue this practice of thoughtful reflection when using annotated primary scientific literature as a pedagogical tool. We also welcome any feedback or alternative uses of annotated primary scientific literature.

Future steps

The latest annotated primary scientific literature implementation protocol iteration is being pilot tested during fall 2018. Focusing more on robust evaluation now that implementation obstacles have been overcome will allow us to determine the effectiveness of annotated primary scientific literature as a pedagogical tool in undergraduate biology classrooms. Future studies are being designed to examine students’ scientific literacy before and after completing the annotated article activities using a previously validated scientific literacy instrument (Test of Scientific Literacy Skills [TOSLS]) [ 2 ]. Additionally, we aim to measure students’ subjective task values with regards to reading primary scientific research literature [ 25 – 28 ], as well as their primary scientific literature reading self-efficacy [ 29 – 32 ].

We hope to spread the word about annotated primary scientific literature and investigate its potential impacts on student learning and motivation as we further refine our implementation protocol and propagate beyond our department and institution.

Acknowledgments

We thank Beth Ruedi and Shelby Lake at AAAS, and Rebecca Vieyra for help editing this manuscript, our FIU colleagues Richard Brinn, Ligia Collado-Vides, Sat Gavassa, John Geiger, Camila Granados-Cifuentes, Zahra Hazari, Suzanne Koptur, and Sparkle Malone for providing us with class time, and all the participating students at FIU.

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Biology and management of wild lupine ( Lupinus perennis L.): a case study for conserving rare plants in edge habitat

• Published: 05 December 2023
• Volume 225 , pages 373–389, ( 2024 )

Cite this article

• Isabella R. Petitta 1 ,
• Margarita M. López-Uribe 1 , 2 &
• Autumn E. Sabo 1 , 3  

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Wild lupine ( Lupinus perennis ) is a perennial plant originally found primarily throughout the United States and Canada in oak savannas, which are considered an ecotone between prairie and forest. Because of primary habitat loss, this early successional plant is declining and now persists in managed edge habitats such as power line rights-of-way and roadsides across much of its range. Many edge populations of wild lupine are small and isolated, which can hinder the reproduction of this pollinator-dependent plant. Here, we synthesize current literature about the biology and management of wild lupine and associated plants and insects. We also highlight current gaps of knowledge to guide future research on wild lupine and, more generally, on savanna-like habitats. The information provided here on lupine serves as a case study for how edge habitat conserves rare plant species reliant on disturbance. Overall, habitat characteristics that seem best for wild lupine include a gradient of canopy cover from moderate to open, well-drained soils, and a low abundance of understory woody plants. Land management, including prescribed burning, mowing, and mechanical thinning, can promote the conservation of wild lupine and other forest edge plants. However, additional research in regards to ideal management regimes and intensity is needed to further plant conservation in forest edge habitat.

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Traditional prescribed burning of coastal heathland provides niches for xerophilous and sun-loving beetles

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Acknowledgements

We thank Kelly Sitch, Andrew Rohrbaugh, Neil Gifford, Pat McElhenny, Brian Williamson, and Roy Brubaker for their land management insights. We also thank Claire Zimmerman of Mt. Cuba Center for information about wild lupine propagation. Thank you to Grace Gutierrez and Nash Turley for guidance on figure development. Finally, we thank editor, Dr. Karen Harper, and two anonymous reviewers for their comments on our manuscript.

This work was supported by the USDA National Institute of Food and Agriculture and McIntire-Stennis Appropriations under Project #PEN04785 and Accession #1027694 and the Pennsylvania’s Department of Conservation and Natural Resources’s Wild Resources Conservation Program Grant No. 21637. IRP was supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE1255832. MMLU was supported by the USDA NIFA Appropriations Projects PEN04716 and PEN04620.

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Petitta, I.R., López-Uribe, M.M. & Sabo, A.E. Biology and management of wild lupine ( Lupinus perennis L.): a case study for conserving rare plants in edge habitat. Plant Ecol 225 , 373–389 (2024). https://doi.org/10.1007/s11258-023-01371-9

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College of Biological Sciences

Cbs students receive prestigious goldwater scholarships.

Three UC Davis students were awarded the scholarships this year, two from CBS

• by Isabella Beristain
• May 14, 2024

Three UC Davis students, including two from the College of Biological Sciences, have won the highly prestigious and competitive Barry Goldwater Scholarship. 

Every year, the Barry Goldwater Scholarship and Excellence in Education Foundation honors fewer than 500 undergraduate second- and third-year students from across the country with scholarships recognizing their science, technology, engineering and mathematics research accomplishments and future potential.

The 2024 UC Davis Goldwater Scholars are: Avantika Gokulnatha, a third-year genetics and genomics major, Madeleine Rose, a second-year cognitive science major, and Shih-Na Liu, an evolution, ecology and biodiversity major. Each of them submitted research spanning multiple STEM fields and topics.

Gokulnatha, who is from San Jose, California, investigates the cellular mechanisms of the human aging process. Rose, who is from Foster City, California, conducts research at the intersection of neuroendocrinology, chronic pain and artificial intelligence. And Liu, from Taoyuan, Taiwan, explores the effects of diet on the body shape evolution of reef fishes.

All three winners intend to continue their research at a graduate level. In the meantime, they’ll work on their ongoing endeavors here at UC Davis, where they began their journeys pursuing research excellence.

Goldwater dynasty

UC Davis has had 35 recipients earn the Goldwater Scholarship throughout the program’s 30-year history. This is the seventh consecutive year that one or more UC Davis students received the coveted Goldwater Scholar title. Only one other UC had more awardees than UC Davis for the 2024-25 scholarship cycle.

Scott Palmer, UC Davis prestigious scholarship advisor, said this number speaks not just to the caliber of students that UC Davis admits but also to the multitude of research opportunities available for undergraduates to pursue.

“At Davis, there are so many ways to get involved with research and the labs conducting it,” Palmer said. “We have a reputation for being collaborative, which not a lot of incoming students are necessarily aware about.” 

From seminar to scholar

Gokulnatha first learned about the scholarship at one of Palmer’s honors program advising seminars during her first quarter at UC Davis.

“In the past, I benefitted significantly from applying to scholarships — not just financially, but also through the doors that these awards open,” Gokulnatha said. “I knew I would need to start exploring research opportunities and immediately the one thing I grasped was that everyone seemed accessible and really invested in us undergraduates learning everything we can both inside and outside the classroom. People really do see themselves in you as a budding researcher.”

Bold actions, rich returns

Rose began her Goldwater journey cold emailing professors, looking for opportunities that best fit her personal research goals.

“The worst response you can get is a no and a no is not the end of the world. You never know what will happen if you do not hit send,” Rose said. “Reaching out to prospective mentors across disciplines is a great way to expand your options and diversify research interests, it’s how I now work with top researchers and clinicians across academic institutions.” 

Opportunities to rethink the way things work

Liu noted there are also many ways to get your research funded.

“Last year, I participated in the EVE Scholars Program . Through the Department of Evolution and Ecology, I was able to make a lot of progress on my research that I then submitted for the Goldwater Scholarship,” she said. “It is a really cool program because they fund you for the whole summer, then you take a research presentation class the following quarter and they even provide you with funding to go to conferences to learn more. It’s the whole research package.”

Gaining invaluable experience

According to Palmer, applying to a prestigious scholarship application, alone, is a huge win for most undergraduate students. “You get the opportunity to write about yourself, clarify your vision and show others why they should invest in you. This is a great skill to practice going into graduate school or for jobs after college,” he said.

Rose put herself through this experience to do exactly that: gain valuable experience to aid her future research endeavors.

“You miss 100% of the shots you do not take. The odds of receiving an award like this are slim and I was aware of this when I first decided to apply,” she said. “The application process was challenging but encouraged me to think critically about the research projects I am leading. Applying for this scholarship strengthened my skills both as a researcher and writer.”

Media Resources

• To learn more about the Goldwater Scholarship and how to apply, visit the Barry M. Goldwater webpage located on the UC Davis Financial Aid and Scholarships webpage.  
• Isabella Beristain is a communications specialist in UC Davis Enrollment Management.

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