Oxidative post-translational modifications of specific chloroplast proteins contribute to the initiation of retrograde signaling.The Arabidopsis thaliana EXECUTER1(EX1)protein,a chloroplast-localized singlet oxygen(^(...Oxidative post-translational modifications of specific chloroplast proteins contribute to the initiation of retrograde signaling.The Arabidopsis thaliana EXECUTER1(EX1)protein,a chloroplast-localized singlet oxygen(^(1)O_(2))sensor,undergoes tryptophan(Trp)643 oxidation by^(1)O_(2),a chloroplast-derived and light-dependent reactive oxygen species.The indole side chain of Trp is vulnerable to^(1)O_(2),leading to the generation of oxidized Trp variants and priming EX1 for degradation by a membrane-bound FtsH protease.The perception of^(1)O_(2)via Trp643 oxidation and subsequent EX1 proteolysis facilitate chloroplast-to-nucleus retrograde signaling.In this study,we discovered that the EX1-like protein EX2 also undergoes^(1)O_(2)-dependent Trp530 oxidation and FtsH-dependent turnover,which attenuates^(1)O_(2)signaling by decelerating EX1-Trp643 oxidation and subsequent EX1 degradation.Consistent with this finding,the loss of EX2 function reinforces EX1-dependent retrograde signaling by accelerating EX1-Trp643 oxidation and subsequent EX1 proteolysis,whereas overexpression of EX2 produces molecular phenotypes opposite to those observed in the loss-of-function mutants of EX2.Intriguingly,phylogenetic analysis suggests that EX2 may have emerged evolutionarily to attenuate the sensitivity of EX1 toward^(1)O_(2).Collectively,these results suggest that EX2 functions as a negative regulator of the EX1 signalosome through its own^(1)O_(2)-dependent oxidation,providing a new mechanistic insight into the regulation of EX1-mediated^(1)O_(2)signaling.展开更多
Plants must coordinate chloroplast biogenesis with environmental conditions during seedling establishment,as failure to do so results in impaired phototrophic growth.Despite the biological importance of this early dev...Plants must coordinate chloroplast biogenesis with environmental conditions during seedling establishment,as failure to do so results in impaired phototrophic growth.Despite the biological importance of this early developmental stage,the influence of environmental factors on chloroplast biogenesis remains poorly understood.Here,we reveal a crucial role for GENOMES UNCOUPLED1(GUN1)-mediated biogenic retrograde signaling in safeguarding chloroplast development and supporting seedling growth under heat stress.Loss of GUN1 causes severe bleaching and impaired photomorphogenesis at elevated temperatures.Genetic interaction analyses show that EXECUTER1(EX1)and EXECUTER2(EX2),key components of chloroplast ROS-associated operational retrograde signaling,modulate the heatsensitive phenotype of gun1 mutants,indicating crosstalk between biogenic and operational retrograde pathways.We further demonstrate that the de-repressed expression of photosynthesisassociated nuclear genes,that is,genomes uncoupled expression,is a major contributor to the heat sensitivity and failed chloroplast biogenesis in gun1 seedlings under heat stress.These findings extend the current understanding of GUN1 function by showing its contribution to chloroplast development and thermotolerance through biogenic retrograde signaling during early seedling growth.展开更多
基金This research was supported by the Strategic Priority Research Program from the Chinese Academy of Sciences(grant no.XDB27040102)the 100-Talent Program of the Chinese Academy of Sciences and the National Natural Science Foundation of China(NSFC)(grant no.31871397)to C.K.Support from a President's International Fellowship Initiative(PIFI)postdoctoral fellowship from the Chinese Academy of Sciences(no.2019PB0066)to V.D.is also acknowledged.
文摘Oxidative post-translational modifications of specific chloroplast proteins contribute to the initiation of retrograde signaling.The Arabidopsis thaliana EXECUTER1(EX1)protein,a chloroplast-localized singlet oxygen(^(1)O_(2))sensor,undergoes tryptophan(Trp)643 oxidation by^(1)O_(2),a chloroplast-derived and light-dependent reactive oxygen species.The indole side chain of Trp is vulnerable to^(1)O_(2),leading to the generation of oxidized Trp variants and priming EX1 for degradation by a membrane-bound FtsH protease.The perception of^(1)O_(2)via Trp643 oxidation and subsequent EX1 proteolysis facilitate chloroplast-to-nucleus retrograde signaling.In this study,we discovered that the EX1-like protein EX2 also undergoes^(1)O_(2)-dependent Trp530 oxidation and FtsH-dependent turnover,which attenuates^(1)O_(2)signaling by decelerating EX1-Trp643 oxidation and subsequent EX1 degradation.Consistent with this finding,the loss of EX2 function reinforces EX1-dependent retrograde signaling by accelerating EX1-Trp643 oxidation and subsequent EX1 proteolysis,whereas overexpression of EX2 produces molecular phenotypes opposite to those observed in the loss-of-function mutants of EX2.Intriguingly,phylogenetic analysis suggests that EX2 may have emerged evolutionarily to attenuate the sensitivity of EX1 toward^(1)O_(2).Collectively,these results suggest that EX2 functions as a negative regulator of the EX1 signalosome through its own^(1)O_(2)-dependent oxidation,providing a new mechanistic insight into the regulation of EX1-mediated^(1)O_(2)signaling.
基金supported by the National Natural Science Foundation of China(NSFC)(grant no.32350710188)the Open Research Fund of the State Key Laboratory of Plant Trait Design(grant no.PDKF001)to C.K。
文摘Plants must coordinate chloroplast biogenesis with environmental conditions during seedling establishment,as failure to do so results in impaired phototrophic growth.Despite the biological importance of this early developmental stage,the influence of environmental factors on chloroplast biogenesis remains poorly understood.Here,we reveal a crucial role for GENOMES UNCOUPLED1(GUN1)-mediated biogenic retrograde signaling in safeguarding chloroplast development and supporting seedling growth under heat stress.Loss of GUN1 causes severe bleaching and impaired photomorphogenesis at elevated temperatures.Genetic interaction analyses show that EXECUTER1(EX1)and EXECUTER2(EX2),key components of chloroplast ROS-associated operational retrograde signaling,modulate the heatsensitive phenotype of gun1 mutants,indicating crosstalk between biogenic and operational retrograde pathways.We further demonstrate that the de-repressed expression of photosynthesisassociated nuclear genes,that is,genomes uncoupled expression,is a major contributor to the heat sensitivity and failed chloroplast biogenesis in gun1 seedlings under heat stress.These findings extend the current understanding of GUN1 function by showing its contribution to chloroplast development and thermotolerance through biogenic retrograde signaling during early seedling growth.
