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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.

SUBMITTER: Yu HD

PROVIDER: S-EPMC3342936 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis.

Yu Hai-Dong HD Yang Xiao-Fei XF Chen Si-Ting ST Wang Yu-Ting YT Li Ji-Kai JK Shen Qi Q Liu Xun-Liang XL Guo Fang-Qing FQ

PLoS genetics 20120503 5

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-respon ...[more]

PMID: 22570631

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Project description:The expression of heat-shock proteins (Hsps) induced by a non-lethal heat treatment confers acquired thermotolerance (AT) to organisms against a subsequent challenge of otherwise lethal temperature. After stress signal lifted, AT gradually decayed with the decline of Hsps during recovery period. The duration of AT may be critical for sessile organisms, such as plants, to survive repeated heat stress in the environment. To identify heat-induced genes involved in duration of AT, we took a reverse-genetics approach by screening for Arabidopsis T-DNA insertion mutants that show decreased thermotolerance after a long recovery at non-stress condition following a conditioning treatment. Among the tested mutants corresponding to 47 genes, only the HsfA2 knockout mutant showed significant phenotype. The mutant plants were more sensitive to severe heat stress than the wild type after long but not short recovery following a pretreatment at 37oC, which can be complemented by introducing a wild-type copy of the gene. Quantitative hypocotyl elongation assay also revealed that AT decayed faster in the absence of HsfA2. Significant decline of the transcript levels of several highly heat-induced genes was observed in the HsfA2 knockout plants after a 4-h recovery or after 2 h of prolonged heat stress. Immunoblot anlysis showed that Hsa32 and class I small Hsp were lower in the mutant than in the wild type after a long recovery. Our results suggest that HsfA2 as a heat-induced transactivator sustains the post-stress expression of Hsp genes and extends the duration of AT in Arabidopsis. Experiment Overall Design: Total RNA was isolated from the seedlings of 5-d old wild-type and HsfA2 knockout mutant seedlings (a pool of about 100 plants per treatment in duplicates) harvested immediately after heat shock treatment. In this experiment, total 12 chips were used, 1 each for 2 biological replicates of the control and HS-treated samples for the wild type and mutant plants.

Dataset Information

Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis.

Publications

Downregulation of chloroplast RPS1 negatively modulates nuclear heat-responsive expression of HsfA2 and its target genes in Arabidopsis.

Similar Datasets

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