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Activation of stress-response genes by retrograde signaling-mediated destabilization of nuclear importin IMPα-9 and its interactor TPR2
Molecular Plant ( IF 17.1 ) Pub Date : 2024-05-01 , DOI: 10.1016/j.molp.2024.04.008
Liping Zeng 1 , Maria Fernanda Gomez Mendez 1 , Jingzhe Guo 1 , Jishan Jiang 1 , Bailong Zhang 2 , Hao Chen 1 , Brandon Le 1 , Haiyan Ke 1 , Katayoon Dehesh 1
Molecular Plant ( IF 17.1 ) Pub Date : 2024-05-01 , DOI: 10.1016/j.molp.2024.04.008
Liping Zeng 1 , Maria Fernanda Gomez Mendez 1 , Jingzhe Guo 1 , Jishan Jiang 1 , Bailong Zhang 2 , Hao Chen 1 , Brandon Le 1 , Haiyan Ke 1 , Katayoon Dehesh 1
Affiliation
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 mutant, which contains elevated 2-C-methyl-d-erythritol-2,4-cyclopyrophosphate (MEcPP) levels, and identified the gain-of-function mutant , which shows reversed dwarfism and suppressed expression of stress-response genes in the background despite heightened MEcPP. Subsequent genetic and biochemical analyses established that the accumulation of MEcPP initiates an upsurge in 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 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.
中文翻译:
逆行信号介导的核输入素 IMPα-9 及其相互作用体 TPR2 不稳定激活应激反应基因
长期以来,应激诱导的从质体到细胞核的逆行信号传递一直困扰着植物生物学家。为了解决这个问题,我们对突变体进行了抑制筛选,该突变体含有升高的 2-C-甲基-d-赤藓糖醇-2,4-环焦磷酸盐 (MEcPP) 水平升高,并确定了功能获得性突变体,尽管 MEcPP 升高,但显示反向侏儒症和应激反应基因在背景中的表达受到抑制。随后的遗传和生化分析确定,MEcPP 的积累引发了 ASK1) 丰度的激增,ASK1) 丰度是蛋白酶体降解途径的关键组成部分。ASK1 的这种增加促进了 IMPα-9 的降解。此外,我们发现了 IMPα-9 和 TPR2(一种转录共抑制因子)之间的蛋白质-蛋白质相互作用,并发现 IMPα-9 水平的降低与 TPR2 丰度的降低相吻合。值得注意的是,IMPα-9 和 TPR2 之间的相互作用在突变体中被破坏,突出了单个氨基酸改变在维持其结合中的关键作用。它们相互作用的破坏导致 MEcPP 相关表型的逆转。染色质免疫沉淀结合测序分析显示,TPR2 与应激反应基因整体结合,并表明 IMPα-9 与染色质结合。在正常条件下,它们共同发挥作用以抑制应激反应基因的表达,但这种抑制在应激下通过抑制机制的降解而得到缓解。我们发现的生物学相关性在高光照胁迫下得到验证,其特征是 MEcPP 积累、ASK1 水平升高、IMPα-9 降解、TPR2 丰度降低以及随后的应激反应基因网络激活。 总之,我们的研究共同揭示了对植物适应机制的新见解,突出了逆行信号传导、蛋白酶体和核运输机制之间错综复杂的相互作用。
更新日期:2024-05-01
中文翻译:
逆行信号介导的核输入素 IMPα-9 及其相互作用体 TPR2 不稳定激活应激反应基因
长期以来,应激诱导的从质体到细胞核的逆行信号传递一直困扰着植物生物学家。为了解决这个问题,我们对突变体进行了抑制筛选,该突变体含有升高的 2-C-甲基-d-赤藓糖醇-2,4-环焦磷酸盐 (MEcPP) 水平升高,并确定了功能获得性突变体,尽管 MEcPP 升高,但显示反向侏儒症和应激反应基因在背景中的表达受到抑制。随后的遗传和生化分析确定,MEcPP 的积累引发了 ASK1) 丰度的激增,ASK1) 丰度是蛋白酶体降解途径的关键组成部分。ASK1 的这种增加促进了 IMPα-9 的降解。此外,我们发现了 IMPα-9 和 TPR2(一种转录共抑制因子)之间的蛋白质-蛋白质相互作用,并发现 IMPα-9 水平的降低与 TPR2 丰度的降低相吻合。值得注意的是,IMPα-9 和 TPR2 之间的相互作用在突变体中被破坏,突出了单个氨基酸改变在维持其结合中的关键作用。它们相互作用的破坏导致 MEcPP 相关表型的逆转。染色质免疫沉淀结合测序分析显示,TPR2 与应激反应基因整体结合,并表明 IMPα-9 与染色质结合。在正常条件下,它们共同发挥作用以抑制应激反应基因的表达,但这种抑制在应激下通过抑制机制的降解而得到缓解。我们发现的生物学相关性在高光照胁迫下得到验证,其特征是 MEcPP 积累、ASK1 水平升高、IMPα-9 降解、TPR2 丰度降低以及随后的应激反应基因网络激活。 总之,我们的研究共同揭示了对植物适应机制的新见解,突出了逆行信号传导、蛋白酶体和核运输机制之间错综复杂的相互作用。