Activation of stress-response genes by retrograde signaling-mediated destabilization of nuclear importin IMPα-9 and its interactor TPR2  

作　　者：Liping Zeng Maria Fernanda Gomez Mendez Jingzhe Guo Jishan Jiang Bailong Zhang Hao Chen Brandon Le Haiyan Ke Katayoon Dehesh 

机构地区：[1]Department of Botany and Plant Sciences,Institute of Integrative Genome Biology,University of California,Riverside,Riverside,CA 92521,USA [2]School of Medicine,University of California,Riverside,Riverside,CA 92521,USA

出　　处：《Molecular Plant》2024年第6期884-899,共16页分子植物（英文版）

基　　金：supported by National Institutes of Health National Institutes of Health(NIH)R01GM107311-8;National Science Foundation National Science Foundation(NSF)2104365 grants;by Dr.John W.Leibacher and Mrs.Kathy Cookson endowed chair funds to K.D.

摘　　要：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.

关 键 词：plastidial retrograde signal MEcPP ASK1 impα-9 TPR2 

分 类 号：Q943.2[生物学—植物学]