title: Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis.
abstract: Heat stress commonly leads to inhibition of photosynthesis in higher plants. The transcriptional induction of heat stress-responsive genes represents the first line of inducible defense against imbalances in cellular homeostasis. Although heat stress transcription factor HsfA2 and its downstream target genes are well studied, the regulatory mechanisms by which HsfA2 is activated in response to heat stress remain elusive. Here, we show that chloroplast ribosomal protein S1 (RPS1) is a heat-responsive protein and functions in protein biosynthesis in chloroplast. Knockdown of RPS1 expression in the rps1 mutant nearly eliminates the heat stress-activated expression of HsfA2 and its target genes, leading to a considerable loss of heat tolerance. We further confirm the relationship existed between the downregulation of RPS1 expression and the loss of heat tolerance by generating RNA interference-transgenic lines of RPS1. Consistent with the notion that the inhibited activation of HsfA2 in response to heat stress in the rps1 mutant causes heat-susceptibility, we further demonstrate that overexpression of HsfA2 with a viral promoter leads to constitutive expressions of its target genes in the rps1 mutant, which is sufficient to reestablish lost heat tolerance and recovers heat-susceptible thylakoid stability to wild-type levels. Our findings reveal a heat-responsive retrograde pathway in which chloroplast translation capacity is a critical factor in heat-responsive activation of HsfA2 and its target genes required for cellular homeostasis under heat stress. Thus, RPS1 is an essential yet previously unknown determinant involved in retrograde activation of heat stress responses in higher plants.
authors.affiliation: The National Key Laboratory of Plant Molecular Genetics and National Center for Plant Gene Research (Shanghai), Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
authors.forename: Hai-Dong
authors.initials: HD
authors.lastname: Yu
authors.forename: Xiao-Fei
authors.initials: XF
authors.lastname: Yang
authors.forename: Si-Ting
authors.initials: ST
authors.lastname: Chen
authors.forename: Yu-Ting
authors.initials: YT
authors.lastname: Wang
authors.forename: Ji-Kai
authors.initials: JK
authors.lastname: Li
authors.forename: Qi
authors.initials: Q
authors.lastname: Shen
authors.forename: Xun-Liang
authors.initials: XL
authors.lastname: Liu
authors.forename: Fang-Qing
authors.initials: FQ
authors.lastname: Guo
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000502:physiology; D029681:Arabidopsis Proteins; D060365:Chloroplast Proteins / Q000235:genetics / Q000378:metabolism; D002736:Chloroplasts / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D004268:DNA-Binding Proteins / Q000235:genetics* / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D000076249:Heat Shock Transcription Factors; D006360:Heat-Shock Proteins / Q000235:genetics* / Q000378:metabolism; D018869:Heat-Shock Response / Q000235:genetics; D009154:Mutation; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D030821:Plants, Genetically Modified; D034622:RNA Interference; D012269:Ribosomal Proteins / Q000235:genetics* / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D060365:Chloroplast Proteins; D004268:DNA-Binding Proteins; C000620134:HSFA2 protein, Arabidopsis; D000076249:Heat Shock Transcription Factors; D006360:Heat-Shock Proteins; D010940:Plant Proteins; D012269:Ribosomal Proteins; D014157:Transcription Factors; C015494:ribosomal protein S1