Zifen Lao, Jiali Mao, Runan Chen, Ran Xu, Zhuang Yang, Ying Wang, Junjie Zhou, Zhihua Mu, Hang Xu, Fengmei Li, Dongyi Huang, Yong Xiao, Jie Luo, Wei Xia
{"title":"Genome-wide identification and characterization of BASIC PENTACYSTEINE transcription factors and their binding motifs in coconut palm.","authors":"Zifen Lao, Jiali Mao, Runan Chen, Ran Xu, Zhuang Yang, Ying Wang, Junjie Zhou, Zhihua Mu, Hang Xu, Fengmei Li, Dongyi Huang, Yong Xiao, Jie Luo, Wei Xia","doi":"10.3389/fpls.2024.1491139","DOIUrl":null,"url":null,"abstract":"<p><strong>Introduction: </strong><i>BASIC PENTACYSTEINE</i> (<i>BPC</i>) is a small transcription factor family known for its role in various developmental processes in plants, particularly in binding GA motifs and regulating flower and seed development. However, research on the functional characteristics and target genes of <i>BPCs</i> in coconut (<i>Cocos nucifera</i>) is limited.</p><p><strong>Methods: </strong>In this study, we systematically characterized the gene structure, conserved protein domains, gene expansion, and target genes of <i>CnBPCs</i> in the coconut genome. We conducted yeast one-hybrid (Y1H) and dual-luciferase assay to explore gene interactions. We identified genes with the GA motif in their promoter regions and combined this information with a weighted gene co-expression network to identify the target genes of <i>CnBPCs</i>.</p><p><strong>Results: </strong>Eight <i>CnBPCs</i> were identified, including three Class I <i>CnBPCs</i> from triplication, four Class II <i>CnBPCs</i> (with <i>CnBPC6A</i> and <i>CnBPC6B</i> resulting from segmental duplication), and one Class III CnBPC (<i>CnBPC7</i>). Three conserved DNA-binding motifs were detected, exhibiting variation in certain sites. Widespread BPC gene expansion was detected in coconut and other plant species, while only three BPCs were found in the most basal extant flowering plant. Notably, 92% of protein-coding genes contained at least one GA motif, with the (GA)3 motif being most prevalent. Genes containing the GA motif that exhibit a high expression correlation with <i>CnBPCs</i>, tend to interact strongly with the corresponding <i>CnBPCs</i>. Additionally, promoters rich in the GA motif tend to interact with all members of <i>CnBPC</i>. The dual-luciferase assay showed that <i>CnBPCs</i> could activate or repress the transcriptional activities of promoters containing either (GA)3 or (GA)11 motif but with a bias toward certain genes. Furthermore, we constructed co-expressed networks identifying 426 genes with GA motifs as potential <i>CnBPC</i> targets.</p><p><strong>Discussion: </strong>Our findings suggest that <i>CnBPCs</i> may play significant roles in seed germination, flower development, and mesocarp development by interacting with genes such as <i>CnAG1</i>, <i>CnAG2</i>, <i>CnSTK</i>, <i>CnMFT</i>, and <i>CnCS</i>. This study characterized <i>CnBPCs</i>' binding motif and possible target genes, laying a theoretical foundation to reveal <i>CnBPCs</i>' function in flower and seed development.</p>","PeriodicalId":12632,"journal":{"name":"Frontiers in Plant Science","volume":"15 ","pages":"1491139"},"PeriodicalIF":4.1000,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11666369/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Plant Science","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.3389/fpls.2024.1491139","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Introduction: BASIC PENTACYSTEINE (BPC) is a small transcription factor family known for its role in various developmental processes in plants, particularly in binding GA motifs and regulating flower and seed development. However, research on the functional characteristics and target genes of BPCs in coconut (Cocos nucifera) is limited.
Methods: In this study, we systematically characterized the gene structure, conserved protein domains, gene expansion, and target genes of CnBPCs in the coconut genome. We conducted yeast one-hybrid (Y1H) and dual-luciferase assay to explore gene interactions. We identified genes with the GA motif in their promoter regions and combined this information with a weighted gene co-expression network to identify the target genes of CnBPCs.
Results: Eight CnBPCs were identified, including three Class I CnBPCs from triplication, four Class II CnBPCs (with CnBPC6A and CnBPC6B resulting from segmental duplication), and one Class III CnBPC (CnBPC7). Three conserved DNA-binding motifs were detected, exhibiting variation in certain sites. Widespread BPC gene expansion was detected in coconut and other plant species, while only three BPCs were found in the most basal extant flowering plant. Notably, 92% of protein-coding genes contained at least one GA motif, with the (GA)3 motif being most prevalent. Genes containing the GA motif that exhibit a high expression correlation with CnBPCs, tend to interact strongly with the corresponding CnBPCs. Additionally, promoters rich in the GA motif tend to interact with all members of CnBPC. The dual-luciferase assay showed that CnBPCs could activate or repress the transcriptional activities of promoters containing either (GA)3 or (GA)11 motif but with a bias toward certain genes. Furthermore, we constructed co-expressed networks identifying 426 genes with GA motifs as potential CnBPC targets.
Discussion: Our findings suggest that CnBPCs may play significant roles in seed germination, flower development, and mesocarp development by interacting with genes such as CnAG1, CnAG2, CnSTK, CnMFT, and CnCS. This study characterized CnBPCs' binding motif and possible target genes, laying a theoretical foundation to reveal CnBPCs' function in flower and seed development.
期刊介绍:
In an ever changing world, plant science is of the utmost importance for securing the future well-being of humankind. Plants provide oxygen, food, feed, fibers, and building materials. In addition, they are a diverse source of industrial and pharmaceutical chemicals. Plants are centrally important to the health of ecosystems, and their understanding is critical for learning how to manage and maintain a sustainable biosphere. Plant science is extremely interdisciplinary, reaching from agricultural science to paleobotany, and molecular physiology to ecology. It uses the latest developments in computer science, optics, molecular biology and genomics to address challenges in model systems, agricultural crops, and ecosystems. Plant science research inquires into the form, function, development, diversity, reproduction, evolution and uses of both higher and lower plants and their interactions with other organisms throughout the biosphere. Frontiers in Plant Science welcomes outstanding contributions in any field of plant science from basic to applied research, from organismal to molecular studies, from single plant analysis to studies of populations and whole ecosystems, and from molecular to biophysical to computational approaches.
Frontiers in Plant Science publishes articles on the most outstanding discoveries across a wide research spectrum of Plant Science. The mission of Frontiers in Plant Science is to bring all relevant Plant Science areas together on a single platform.