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.

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Inositol-requiring enzyme 1 (IRE1) is the most conserved transducer of the unfolded protein response that produces either adaptive or death signals depending on the amplitude and duration of its activation. Here, we report that SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE 6 (SPL6)-deficient plants displayed hyperactivation of the endoplasmic reticulum (ER) stress sensor IRE1, leading to cell death in rice panicles, indicating that SPL6 is an essential survival factor for the suppression of persistent or intense ER stress conditions. Importantly, knockdown of the hyperactivated mRNA level of IRE1 rescues panicle apical abortion in the spl6-1 transgenic plants harbouring the IRE1-RNAi constructs, establishing the genetic linkage between the hyperactivation of IRE1 and cell death in spl6-1. Our findings reveal a novel cell survival machinery in which SPL6 represses the transcriptional activation of the ER stress sensor IRE1 in control of ER stress signalling outputs that hinge on a balance between adaptive and death signals for determining cell fates during ER stress.