FaNAC047-FaNAC058 module coordinately promotes chlorophyll degradation and reactive oxygen species production during heat-induced leaf senescence in tall fescue

IF 9.3 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY
Liwen Cao, Yao Chen, Kai Xiao, Liang Chen
{"title":"FaNAC047-FaNAC058 module coordinately promotes chlorophyll degradation and reactive oxygen species production during heat-induced leaf senescence in tall fescue","authors":"Liwen Cao,&nbsp;Yao Chen,&nbsp;Kai Xiao,&nbsp;Liang Chen","doi":"10.1111/jipb.13897","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>Leaf senescence can be triggered by various abiotic stresses. Among these, heat stress emerges as a pivotal environmental factor, particularly in light of the predicted rise in global temperatures. However, the molecular mechanism underlying heat-induced leaf senescence remains largely unexplored. As a cool-season grass species, tall fescue (<i>Festuca arundinacea</i>) is an ideal and imperative material for investigating heat-induced leaf senescence because heat stress easily triggers leaf senescence to influence its forage yield and turf quality. Here, we investigated the role of <i>FaNAC047</i> in heat-induced leaf senescence. Overexpression of <i>FaNAC047</i> promoted heat-induced leaf senescence in transgenic tall fescue that was evidenced by a more seriously destructive photosystem and higher accumulation of reactive oxygen species (ROS), whereas knockdown of <i>FaNAC047</i> delayed leaf senescence. Further protein–DNA interaction assays indicated that FaNAC047 directly activated the transcriptions of <i>NON-YELLOW COLORING 1</i> (<i>FaNYC1</i>), <i>NYC1-like</i> (<i>FaNOL</i>), and <i>STAY-GREEN</i> (<i>FaSGR</i>) but directly inhibited <i>Catalases 2</i> (<i>FaCAT2</i>) expression, thereby promoting chlorophyll degradation and ROS accumulation. Subsequently, protein–protein interaction assays revealed that FaNAC047 physically interacted with FaNAC058 to enhance its regulatory effect on <i>FaNYC1</i>, <i>FaNOL</i>, <i>FaSGR</i>, and <i>FaCAT2</i>. Additionally, FaNAC047 could transcriptionally activate <i>FaNAC058</i> expression to form a regulatory cascade, driving senescence progression. Consistently, the knockdown of <i>FaNAC058</i> significantly delayed heat-induced leaf senescence. Collectively, our results reveal that FaNAC047-FaNAC058 module coordinately mediates chlorophyll degradation and ROS production to positively regulate heat-induced leaf senescence. The findings illustrate the molecular network of heat-induced leaf senescence for breeding heat-resistant plants.</p></div>","PeriodicalId":195,"journal":{"name":"Journal of Integrative Plant Biology","volume":"67 4","pages":"1009-1027"},"PeriodicalIF":9.3000,"publicationDate":"2025-03-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Integrative Plant Biology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/jipb.13897","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Leaf senescence can be triggered by various abiotic stresses. Among these, heat stress emerges as a pivotal environmental factor, particularly in light of the predicted rise in global temperatures. However, the molecular mechanism underlying heat-induced leaf senescence remains largely unexplored. As a cool-season grass species, tall fescue (Festuca arundinacea) is an ideal and imperative material for investigating heat-induced leaf senescence because heat stress easily triggers leaf senescence to influence its forage yield and turf quality. Here, we investigated the role of FaNAC047 in heat-induced leaf senescence. Overexpression of FaNAC047 promoted heat-induced leaf senescence in transgenic tall fescue that was evidenced by a more seriously destructive photosystem and higher accumulation of reactive oxygen species (ROS), whereas knockdown of FaNAC047 delayed leaf senescence. Further protein–DNA interaction assays indicated that FaNAC047 directly activated the transcriptions of NON-YELLOW COLORING 1 (FaNYC1), NYC1-like (FaNOL), and STAY-GREEN (FaSGR) but directly inhibited Catalases 2 (FaCAT2) expression, thereby promoting chlorophyll degradation and ROS accumulation. Subsequently, protein–protein interaction assays revealed that FaNAC047 physically interacted with FaNAC058 to enhance its regulatory effect on FaNYC1, FaNOL, FaSGR, and FaCAT2. Additionally, FaNAC047 could transcriptionally activate FaNAC058 expression to form a regulatory cascade, driving senescence progression. Consistently, the knockdown of FaNAC058 significantly delayed heat-induced leaf senescence. Collectively, our results reveal that FaNAC047-FaNAC058 module coordinately mediates chlorophyll degradation and ROS production to positively regulate heat-induced leaf senescence. The findings illustrate the molecular network of heat-induced leaf senescence for breeding heat-resistant plants.

Abstract Image

FaNAC047-FaNAC058模块协同促进高羊茅热致叶片衰老过程中叶绿素降解和活性氧的产生。
叶片衰老可由多种非生物胁迫触发。在这些因素中,热应激成为一个关键的环境因素,特别是考虑到预计的全球气温上升。然而,热诱导叶片衰老的分子机制在很大程度上仍未被探索。高羊茅(Festuca arundinacea)作为一种寒季牧草,由于热应激容易引起叶片衰老,影响其饲料产量和草坪质量,因此是研究热致叶片衰老的理想材料。在此,我们研究了FaNAC047在热致叶片衰老中的作用。过表达FaNAC047促进了转基因高羊茅热诱导的叶片衰老,表现为破坏性更强的光系统和更高的活性氧(ROS)积累,而过表达FaNAC047则延缓了叶片衰老。进一步的蛋白- dna相互作用实验表明,FaNAC047直接激活NON-YELLOW COLORING 1 (FaNYC1)、NYC1-like (FaNOL)和STAY-GREEN (FaSGR)的转录,但直接抑制过氧化氢酶2 (FaCAT2)的表达,从而促进叶绿素降解和ROS积累。随后,蛋白相互作用分析显示,FaNAC047与FaNAC058物理相互作用,增强其对FaNYC1、FaNOL、FaSGR和FaCAT2的调控作用。此外,FaNAC047可以转录激活FaNAC058的表达,形成调控级联,推动衰老进程。同样,敲低FaNAC058显著延缓了热诱导的叶片衰老。综上所述,FaNAC047-FaNAC058模块协同调节叶绿素降解和ROS产生,积极调节热致叶片衰老。研究结果说明了耐热植物热致叶片衰老的分子网络。
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
Journal of Integrative Plant Biology
Journal of Integrative Plant Biology 生物-生化与分子生物学
CiteScore
18.00
自引率
5.30%
发文量
220
审稿时长
3 months
期刊介绍: Journal of Integrative Plant Biology is a leading academic journal reporting on the latest discoveries in plant biology.Enjoy the latest news and developments in the field, understand new and improved methods and research tools, and explore basic biological questions through reproducible experimental design, using genetic, biochemical, cell and molecular biological methods, and statistical analyses.
×
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:604180095
Book学术官方微信