Arabidopsis transcription factors SPL1 and SPL12 confer plant thermotolerance at reproductive stage.

Plant reproductive organs are vulnerable to heat, but regulation of heat shock responses (HSRs) in inflorescence is largely uncharacterized. Here, we report that two of the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) transcriptional factors in Arabidopsis, SPL1 and SPL12, act redundantly in thermotolerance at reproductive stage. The spl1-1 spl12-1 inflorescences displayed hypersensitivity to heat stress, whereas overexpression of SPL1 or SPL12 enhanced the thermotolerance in both Arabidopsis and tobacco. RNA-seq revealed 1,939 upregulated and 1,479 downregulated genes in wild-type inflorescence upon heat stress, among which one quarter (1,040) was misregulated in spl1-1 spl12-1, indicating that the two SPLs contribute greatly to the heat-triggered transcriptional reprogramming in inflorescence. Notably, heat stress induced a large number of abscisic acid (ABA) response genes, of which ∼39% were disturbed in heat-induction in spl1-1 spl12-1 inflorescence. Pre-application of ABA and overexpression of SPL1 restored the inflorescence thermotolerance in spl1-1 spl12-1 and the ABA biosynthesis mutant aba2-1, but not the pyl sextuple mutant defected in ABA receptors PYR1/PYL1/PYL2/PYL4/PYL5/PYL8. Thus inflorescence thermotolerance conferred by SPL1 and SPL2 involves the PYL-mediated ABA signaling. The molecular network and the two SPL factors illustrated here shed a new light on the mechanisms of plant thermotolerance at reproductive stage.

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