逆行信号介导的核导入蛋白 IMPα-9 及其互作因子 TPR2 的不稳定性激活了应激反应基因。

IF 17.1 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Molecular Plant Pub Date : 2024-06-03 Epub Date: 2024-05-01 DOI:10.1016/j.molp.2024.04.008
Liping Zeng, Maria Fernanda Gomez Mendez, Jingzhe Guo, Jishan Jiang, Bailong Zhang, Hao Chen, Brandon Le, Haiyan Ke, Katayoon Dehesh
{"title":"逆行信号介导的核导入蛋白 IMPα-9 及其互作因子 TPR2 的不稳定性激活了应激反应基因。","authors":"Liping Zeng, Maria Fernanda Gomez Mendez, Jingzhe Guo, Jishan Jiang, Bailong Zhang, Hao Chen, Brandon Le, Haiyan Ke, Katayoon Dehesh","doi":"10.1016/j.molp.2024.04.008","DOIUrl":null,"url":null,"abstract":"<p><p>Stress-induced retrograde signal transmission from the plastids to the nucleus has long puzzled plant biologists. To address this, we performed a suppressor screen of the ceh1 mutant, which contains elevated 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate (MEcPP) levels, and identified the gain-of-function mutant impα-9, which shows reversed dwarfism and suppressed expression of stress-response genes in the ceh1 background despite heightened MEcPP. Subsequent genetic and biochemical analyses established that the accumulation of MEcPP initiates an upsurge in Arabidopsis SKP1-like 1 (ASK1) abundance, a pivotal component in the proteasome degradation pathway. This increase in ASK1 prompts the degradation of IMPα-9. Moreover, we uncovered a protein-protein interaction between IMPα-9 and TPR2, a transcriptional co-suppressor and found that a reduction in IMPα-9 levels coincides with a decrease in TPR2 abundance. Significantly, the interaction between IMPα-9 and TPR2 was disrupted in impα-9 mutants, highlighting the critical role of a single amino acid alteration in maintaining their association. Disruption of their interaction results in the reversal of MEcPP-associated phenotypes. Chromatin immunoprecipitation coupled with sequencing analyses revealed that TPR2 binds globally to stress-response genes and suggested that IMPα-9 associates with the chromatin. They function together to suppress the expression of stress-response genes under normal conditions, but this suppression is alleviated in response to stress through the degradation of the suppressing machinery. The biological relevance of our discoveries was validated under high light stress, marked by MEcPP accumulation, elevated ASK1 levels, IMPα-9 degredation, reduced TPR2 abundance, and subsequent activation of a network of stress-response genes. In summary, our study collectively unveils fresh insights into plant adaptive mechanisms, highlighting intricate interactions among retrograde signaling, the proteasome, and nuclear transport machinery.</p>","PeriodicalId":19012,"journal":{"name":"Molecular Plant","volume":null,"pages":null},"PeriodicalIF":17.1000,"publicationDate":"2024-06-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Activation of stress-response genes by retrograde signaling-mediated destabilization of nuclear importin IMPα-9 and its interactor TPR2.\",\"authors\":\"Liping Zeng, Maria Fernanda Gomez Mendez, Jingzhe Guo, Jishan Jiang, Bailong Zhang, Hao Chen, Brandon Le, Haiyan Ke, Katayoon Dehesh\",\"doi\":\"10.1016/j.molp.2024.04.008\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Stress-induced retrograde signal transmission from the plastids to the nucleus has long puzzled plant biologists. To address this, we performed a suppressor screen of the ceh1 mutant, which contains elevated 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate (MEcPP) levels, and identified the gain-of-function mutant impα-9, which shows reversed dwarfism and suppressed expression of stress-response genes in the ceh1 background despite heightened MEcPP. Subsequent genetic and biochemical analyses established that the accumulation of MEcPP initiates an upsurge in Arabidopsis SKP1-like 1 (ASK1) abundance, a pivotal component in the proteasome degradation pathway. This increase in ASK1 prompts the degradation of IMPα-9. Moreover, we uncovered a protein-protein interaction between IMPα-9 and TPR2, a transcriptional co-suppressor and found that a reduction in IMPα-9 levels coincides with a decrease in TPR2 abundance. Significantly, the interaction between IMPα-9 and TPR2 was disrupted in impα-9 mutants, highlighting the critical role of a single amino acid alteration in maintaining their association. Disruption of their interaction results in the reversal of MEcPP-associated phenotypes. Chromatin immunoprecipitation coupled with sequencing analyses revealed that TPR2 binds globally to stress-response genes and suggested that IMPα-9 associates with the chromatin. They function together to suppress the expression of stress-response genes under normal conditions, but this suppression is alleviated in response to stress through the degradation of the suppressing machinery. The biological relevance of our discoveries was validated under high light stress, marked by MEcPP accumulation, elevated ASK1 levels, IMPα-9 degredation, reduced TPR2 abundance, and subsequent activation of a network of stress-response genes. In summary, our study collectively unveils fresh insights into plant adaptive mechanisms, highlighting intricate interactions among retrograde signaling, the proteasome, and nuclear transport machinery.</p>\",\"PeriodicalId\":19012,\"journal\":{\"name\":\"Molecular Plant\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":17.1000,\"publicationDate\":\"2024-06-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular Plant\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1016/j.molp.2024.04.008\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/5/1 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Plant","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.molp.2024.04.008","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/5/1 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

摘要

长期以来,植物生物学家一直困惑于应激诱导的从质体到细胞核的逆行信号传递。为了解决这个问题,我们对 MEcPP 水平升高的 ceh1 突变体进行了抑制剂筛选,发现了功能增益突变体 impα-9,它能逆转矮化现象,并抑制 ceh1 背景下的胁迫响应基因,尽管 MEcPP 水平升高。随后的遗传学和生化分析证实,MEcPP 的积累会导致 ASK1 的丰度飙升,而 ASK1 是蛋白酶体降解途径中的关键成分。ASK1 的增加促进了 IMPα-9 的降解。此外,我们还发现了 IMPα-9 与转录协同抑制因子 TPR2 之间的蛋白质相互作用。IMPα-9 水平的降低与 TPR2 丰度的降低相吻合。值得注意的是,这些相互作用在 impα-9 突变体中被破坏,突出了单个氨基酸改变在维持这些关联中的关键作用。这些相互作用的破坏导致了 MEcPP 相关表型的逆转。ChIP-seq 分析揭示了 TPR2 与应激反应基因的结合以及 IMPα-9 与 DNA 的关联。这些关联在正常情况下共同起到抑制应激基因的作用,但在应激反应中,这种抑制作用会通过抑制机制的降解而得到缓解。这些发现的生物学意义在强光胁迫期间得到了强调,强光胁迫的特点是 MEcPP 积累、ASK1 水平升高、IMPα-9 降解、TPR2 丰度降低以及随后的胁迫响应基因网络激活。总之,我们的研究揭示了逆行信号、蛋白酶体和核转运机制之间复杂的相互作用,并确立了质体作为胁迫响应调控枢纽的地位,从而为植物适应性响应提供了新的视角。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
Activation of stress-response genes by retrograde signaling-mediated destabilization of nuclear importin IMPα-9 and its interactor TPR2.

Stress-induced retrograde signal transmission from the plastids to the nucleus has long puzzled plant biologists. To address this, we performed a suppressor screen of the ceh1 mutant, which contains elevated 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate (MEcPP) levels, and identified the gain-of-function mutant impα-9, which shows reversed dwarfism and suppressed expression of stress-response genes in the ceh1 background despite heightened MEcPP. Subsequent genetic and biochemical analyses established that the accumulation of MEcPP initiates an upsurge in Arabidopsis SKP1-like 1 (ASK1) abundance, a pivotal component in the proteasome degradation pathway. This increase in ASK1 prompts the degradation of IMPα-9. Moreover, we uncovered a protein-protein interaction between IMPα-9 and TPR2, a transcriptional co-suppressor and found that a reduction in IMPα-9 levels coincides with a decrease in TPR2 abundance. Significantly, the interaction between IMPα-9 and TPR2 was disrupted in impα-9 mutants, highlighting the critical role of a single amino acid alteration in maintaining their association. Disruption of their interaction results in the reversal of MEcPP-associated phenotypes. Chromatin immunoprecipitation coupled with sequencing analyses revealed that TPR2 binds globally to stress-response genes and suggested that IMPα-9 associates with the chromatin. They function together to suppress the expression of stress-response genes under normal conditions, but this suppression is alleviated in response to stress through the degradation of the suppressing machinery. The biological relevance of our discoveries was validated under high light stress, marked by MEcPP accumulation, elevated ASK1 levels, IMPα-9 degredation, reduced TPR2 abundance, and subsequent activation of a network of stress-response genes. In summary, our study collectively unveils fresh insights into plant adaptive mechanisms, highlighting intricate interactions among retrograde signaling, the proteasome, and nuclear transport machinery.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
Molecular Plant
Molecular Plant 植物科学-生化与分子生物学
CiteScore
37.60
自引率
2.20%
发文量
1784
审稿时长
1 months
期刊介绍: Molecular Plant is dedicated to serving the plant science community by publishing novel and exciting findings with high significance in plant biology. The journal focuses broadly on cellular biology, physiology, biochemistry, molecular biology, genetics, development, plant-microbe interaction, genomics, bioinformatics, and molecular evolution. Molecular Plant publishes original research articles, reviews, Correspondence, and Spotlights on the most important developments in plant biology.
期刊最新文献
Architecture of the ATP-driven motor for protein import into chloroplasts. Mirids secrete a TOPLESS targeting protein to enhance JA-mediated defense and gossypol accumulation for antagonizing cotton bollworms on cotton plants. On the evolution and genetic diversity of the bread wheat D genome. Sucrose-responsive osmoregulation of plant cell size by a long non-coding RNA. The metal tolerance protein OsMTP11 facilitates cadmium sequestration in the vacuoles of leaf vascular cells for restricting its translocation into rice grains.
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1