Heat Stress Inhibits Pollen Development by Degrading mRNA Capping Enzyme ARCP1 and ARCP2.

IF 6 1区 生物学 Q1 PLANT SCIENCES
Kexin Ning, Xuezhi Li, Jin Yan, Junjie Liu, Zhihua Gao, Wenqiang Tang, Yu Sun
{"title":"Heat Stress Inhibits Pollen Development by Degrading mRNA Capping Enzyme ARCP1 and ARCP2.","authors":"Kexin Ning, Xuezhi Li, Jin Yan, Junjie Liu, Zhihua Gao, Wenqiang Tang, Yu Sun","doi":"10.1111/pce.15178","DOIUrl":null,"url":null,"abstract":"<p><p>Pollen development and germination are critical for successful generation of offspring in plants, yet they are highly susceptible to heat stress (HS). However, the molecular mechanism underlying this process has not been fully elucidated. In this study, we highlight the essential roles of two mRNA capping enzymes, named Arabidopsis mRNA capping phosphatase (ARCP) 1 and 2, in regulating male and female gamete development. The transmission efficiencies of gametes carrying arcp1 arcp2 from arcp1<sup>+/-</sup> arcp2<sup>-/-</sup> and arcp1<sup>-/-</sup> arcp2<sup>+/-</sup> mutants are 30% and zero, respectively. These mutants exhibited a significant increase in misshaped pollen, with germination rates approximately half of those in wild type. ARCP1/2 exhibit RNA triphosphatase and RNA guanylyltransferase activities, which are required for proper pollen development. Through RNA-seq analysis, genes involved in pollen development/germination and HS response were identified as downregulated genes in pollen from arcp1<sup>+/-</sup> arcp2<sup>-/-</sup> mutant. Furthermore, ARCP2 protein is degraded under HS condition, and inducing the expression of ARCP2 can increase the pollen germination rate under elevated temperature. We propose that HS triggers the degradation of mRNA capping enzymes, which in turn disrupts the transcriptome that required for pollen development and pollen germination and ultimately leads to male sterility.</p>","PeriodicalId":222,"journal":{"name":"Plant, Cell & Environment","volume":" ","pages":""},"PeriodicalIF":6.0000,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant, Cell & Environment","FirstCategoryId":"2","ListUrlMain":"https://doi.org/10.1111/pce.15178","RegionNum":1,"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

Pollen development and germination are critical for successful generation of offspring in plants, yet they are highly susceptible to heat stress (HS). However, the molecular mechanism underlying this process has not been fully elucidated. In this study, we highlight the essential roles of two mRNA capping enzymes, named Arabidopsis mRNA capping phosphatase (ARCP) 1 and 2, in regulating male and female gamete development. The transmission efficiencies of gametes carrying arcp1 arcp2 from arcp1+/- arcp2-/- and arcp1-/- arcp2+/- mutants are 30% and zero, respectively. These mutants exhibited a significant increase in misshaped pollen, with germination rates approximately half of those in wild type. ARCP1/2 exhibit RNA triphosphatase and RNA guanylyltransferase activities, which are required for proper pollen development. Through RNA-seq analysis, genes involved in pollen development/germination and HS response were identified as downregulated genes in pollen from arcp1+/- arcp2-/- mutant. Furthermore, ARCP2 protein is degraded under HS condition, and inducing the expression of ARCP2 can increase the pollen germination rate under elevated temperature. We propose that HS triggers the degradation of mRNA capping enzymes, which in turn disrupts the transcriptome that required for pollen development and pollen germination and ultimately leads to male sterility.

热胁迫通过降解mRNA封顶酶ARCP1和ARCP2抑制花粉发育
花粉的发育和萌发是植物成功产生后代的关键,但它们极易受到热胁迫(HS)的影响。然而,这一过程的分子机制尚未完全阐明。在本研究中,我们重点研究了拟南芥两种mRNA封顶酶(mRNA封顶磷酸酶(ARCP)1和2)在调控雌雄配子发育过程中的重要作用。来自arcp1+/-arcp2-/-和arcp1-/-arcp2+/-突变体的携带arcp1 arcp2的配子的传递效率分别为30%和零。这些突变体的畸形花粉显著增加,发芽率约为野生型的一半。ARCP1/2具有RNA三磷酸酶和RNA鸟苷酸转移酶活性,这是花粉正常发育所必需的。通过RNA-seq分析,发现在arcp1+/-arcp2-/-突变体的花粉中,参与花粉发育/萌发和HS反应的基因下调。此外,ARCP2蛋白在HS条件下被降解,而诱导ARCP2的表达可提高花粉在高温条件下的发芽率。我们认为,HS会引发mRNA封顶酶的降解,进而破坏花粉发育和花粉萌发所需的转录组,最终导致雄性不育。
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
Plant, Cell & Environment
Plant, Cell & Environment 生物-植物科学
CiteScore
13.30
自引率
4.10%
发文量
253
审稿时长
1.8 months
期刊介绍: Plant, Cell & Environment is a premier plant science journal, offering valuable insights into plant responses to their environment. Committed to publishing high-quality theoretical and experimental research, the journal covers a broad spectrum of factors, spanning from molecular to community levels. Researchers exploring various aspects of plant biology, physiology, and ecology contribute to the journal's comprehensive understanding of plant-environment interactions.
×
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