Divergence in MiRNA targeting of AchAco and its role in citrate accumulation in kiwifruit.

IF 4.3 2区 生物学 Q1 PLANT SCIENCES
Li-Zhen Ling, Xiao-Di Hu, Shu-Dong Zhang
{"title":"Divergence in MiRNA targeting of AchAco and its role in citrate accumulation in kiwifruit.","authors":"Li-Zhen Ling, Xiao-Di Hu, Shu-Dong Zhang","doi":"10.1186/s12870-024-05877-w","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>MicroRNA (miRNA) is a crucial post-transcriptional regulatory factor in plant growth and development. Duplicated genes often exhibit functional divergence due to competition for the identical miRNA binding sites. Kiwifruit (Actinidia spp.) is an economically significant horticultural crop renowned for its distinctive flavor, which is largely attributable to elevated citrate levels during fruit development. However, the mechanisms through which miRNA-targeted modules evolve following duplication events and regulate citrate biosynthesis, thereby influencing the unique flavor profile of kiwifruits, remain poorly understood.</p><p><strong>Results: </strong>In this study, we examined the expression patterns of miRNAs and interactions with their targets in kiwifruit fruit samples from various pulp tissues and developmental stages. Our analysis identified 46 miRNAs, comprising 44 known miRNAs and two novel/kiwifruit-specific miRNAs, which targeted a total of 1,474 genes. Correlation analysis revealed weak relationships between the expression levels of miRNAs and their target genes. Among these targets, 27 tandemly duplicated genes, and 782 whole genome duplication (WGD) genes exhibited a loss of miRNA binding sites in one of their duplicated copies. Furthermore, weighted gene co-expression network analysis demonstrated that most duplicated genes clustered into distinct gene modules. These findings suggest that the loss of miRNA targets following duplications contributes to expression divergence among gene duplicates, thereby facilitating stable gene expression within the miRNA-targeted network. For instance, the aconitate hydratase genes AchAco4 and AchAco6 were each targeted by different miRNAs, ach-miR-3774 and ach-miR-10371, respectively. Notably, these genes exhibited distinct expression patterns compared to their duplicated counterparts.</p><p><strong>Conclusions: </strong>This study enhances our understanding of how the miRNA-AchAco module regulates citrate content and provides insights into the molecular network that influences the flavor profile of kiwifruit.</p><p><strong>Clinical trial number: </strong>Not applicable.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"24 1","pages":"1157"},"PeriodicalIF":4.3000,"publicationDate":"2024-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11610084/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"BMC Plant Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1186/s12870-024-05877-w","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Background: MicroRNA (miRNA) is a crucial post-transcriptional regulatory factor in plant growth and development. Duplicated genes often exhibit functional divergence due to competition for the identical miRNA binding sites. Kiwifruit (Actinidia spp.) is an economically significant horticultural crop renowned for its distinctive flavor, which is largely attributable to elevated citrate levels during fruit development. However, the mechanisms through which miRNA-targeted modules evolve following duplication events and regulate citrate biosynthesis, thereby influencing the unique flavor profile of kiwifruits, remain poorly understood.

Results: In this study, we examined the expression patterns of miRNAs and interactions with their targets in kiwifruit fruit samples from various pulp tissues and developmental stages. Our analysis identified 46 miRNAs, comprising 44 known miRNAs and two novel/kiwifruit-specific miRNAs, which targeted a total of 1,474 genes. Correlation analysis revealed weak relationships between the expression levels of miRNAs and their target genes. Among these targets, 27 tandemly duplicated genes, and 782 whole genome duplication (WGD) genes exhibited a loss of miRNA binding sites in one of their duplicated copies. Furthermore, weighted gene co-expression network analysis demonstrated that most duplicated genes clustered into distinct gene modules. These findings suggest that the loss of miRNA targets following duplications contributes to expression divergence among gene duplicates, thereby facilitating stable gene expression within the miRNA-targeted network. For instance, the aconitate hydratase genes AchAco4 and AchAco6 were each targeted by different miRNAs, ach-miR-3774 and ach-miR-10371, respectively. Notably, these genes exhibited distinct expression patterns compared to their duplicated counterparts.

Conclusions: This study enhances our understanding of how the miRNA-AchAco module regulates citrate content and provides insights into the molecular network that influences the flavor profile of kiwifruit.

Clinical trial number: Not applicable.

针对AchAco的MiRNA分化及其在猕猴桃柠檬酸积累中的作用。
背景:MicroRNA (miRNA)是植物生长发育过程中重要的转录后调控因子。由于竞争相同的miRNA结合位点,重复基因经常表现出功能分化。猕猴桃(Actinidia spp.)是一种经济上重要的园艺作物,以其独特的风味而闻名,这在很大程度上归因于果实发育过程中柠檬酸水平的升高。然而,mirna靶向模块在重复事件发生后进化并调节柠檬酸盐生物合成的机制,从而影响猕猴桃独特的风味特征,目前尚不清楚。结果:在本研究中,我们研究了猕猴桃不同果肉组织和发育阶段样品中mirna的表达模式及其与靶点的相互作用。我们的分析鉴定了46个mirna,包括44个已知的mirna和2个新的/猕猴桃特异性mirna,总共针对1474个基因。相关分析显示mirna的表达水平与其靶基因之间的相关性较弱。在这些靶标中,27个串联复制基因和782个全基因组重复(WGD)基因在其中一个重复拷贝中表现出miRNA结合位点的缺失。此外,加权基因共表达网络分析表明,大多数重复基因聚集成不同的基因模块。这些发现表明,重复后miRNA靶点的缺失有助于基因重复之间的表达差异,从而促进miRNA靶向网络内基因的稳定表达。例如,乌头酸水合酶基因AchAco4和AchAco6分别被不同的mirna ach-miR-3774和ach-miR-10371靶向。值得注意的是,与重复的基因相比,这些基因表现出不同的表达模式。结论:本研究增强了我们对miRNA-AchAco模块如何调节柠檬酸盐含量的理解,并为影响猕猴桃风味特征的分子网络提供了见解。临床试验号:不适用。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
BMC Plant Biology
BMC Plant Biology 生物-植物科学
CiteScore
8.40
自引率
3.80%
发文量
539
审稿时长
3.8 months
期刊介绍: BMC Plant Biology is an open access, peer-reviewed journal that considers articles on all aspects of plant biology, including molecular, cellular, tissue, organ and whole organism research.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信