Arabidopsis Transcription Factors SPL1 and SPL12 Confer Plant Thermotolerance at Reproductive Stage

Abstract

Plant reproductive organs are vulnerable to heat, but regulation of heat-shock responses 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 the 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 sequencing revealed 1939 upregulated and 1479 downregulated genes in wild-type inflorescence upon heat stress, among which one-quarter (1,040) was misregulated in spl1-1 spl12-1, indicating that SPL1 and SPL12 contribute greatly to the heat-triggered transcriptional reprogramming in inflorescence. Notably, heat stress induced a large number of abscisic acid (ABA) responsive genes, of which ∼39% were disturbed in heat induction in spl1-1 spl12-1 inflorescence. Preapplication of ABA and overexpression of SPL1 restored the inflorescence thermotolerance in spl1-1 spl12-1 and in the ABA biosynthesis mutant aba2-1, but not in the pyl sextuple mutant defective in ABA receptors PYR1/PYL1/PYL2/PYL4/PYL5/PYL8. Thus, inflorescence thermotolerance conferred by SPL1 and SPL2 involves PYL-mediated ABA signaling. The molecular network consisting of SPL1 and SPL12 illustrated here shed new light on the mechanisms of plant thermotolerance at the reproductive stage.

Do ArabidopsisSquamosa promoter binding Protein‐Likegenes act together in plant acclimation to copper or zinc deficiency?

“…Some flowers along the inflorescences did not develop into siliques (Figure i,l), and this was also reflected in a lower number of siliques per plant and seeds per silique compared to the WT (Figure b,c). This phenotype was previously reported (Chao et al., ), and it was independent of Cu supply under our growth conditions (Figures i‐l and ). Under +Cu conditions, the overall morphology of the spl1 spl7 spl12 triple mutant was intermediate and combined aspects of spl7 and spl1 spl12 (Figure e,m).…”

“…We hypothesized that SPL1 and SPL12 might have functions related to those of SPL7 or CrCRR1 in the regulation of transition metal homeostasis. In response to acute heat stress (1 hr at 42°C), the putative Cu exporter‐encoding gene HMA5 is transcriptionally upregulated in the wild type but not in an spl1 spl12 double mutant (Andrés‐Colás et al., ; Burkhead et al., ; Chao et al., ). This observation provided circumstantial support for a possible association of SPL1 and SPL12 with Cu homeostasis.…”

Molecular mechanisms governing plant responses to high temperatures

“…The observation that only 65% of HS‐upregulated genes were regulated by the HSFA1s suggested that additional transcription factors regulate gene expression in response to HS (Liu et al ). Although studies have revealed a number of transcription factors the expression levels of which in vivo are correlated with the thermotolerance of plants (Davletova et al ; Li et al ; Hsieh et al ; Wang et al ; Guan et al ; Lee et al ; Chao et al ; Liao et al ), it is not clear whether these transcription factors are directly regulated by the HS signaling pathway, or merely the targets of unknown primary transcription factors. Of these transcription factors, the activity of a NAC transcription factor, NAC019, during HS is regulated by protein dephosphorylation (Guan et al ).…”

Do Arabidopsis Squamosa promoter binding Protein-Like genes act together in plant acclimation to copper or zinc deficiency?

“…We hypothesized that SPL1 and SPL12 might have functions related to those of SPL7 or CRR1 in the regulation of transition metal homeostasis. In response to acute heat stress (1h at 42 °C), the putative Cu exporter-encoding gene HMA5 is transcriptionally upregulated in the wild type but not in an spl1 spl12 double mutant (Andres-Colas et al 2006;Burkhead et al 2009;Chao et al 2017). This observation provided circumstantial support for a possible association of SPL1 and SPL12 with Cu homeostasis.…”

“…Arabidopsis spl14 mutants showed increased sensitivity to the fungal toxin fumonisin B1 and altered plant architecture, namely elongated petioles and enhanced serration of the leaf margins (Stone et al 2005). SPL1 and SPL12 were recently implicated in thermotolerance, especially of reproductive tissues (Chao et al 2017). Whereas proteins of the SPL family generally show little amino acid sequence conservation outside of the SBP domain, SPL1 and SPL12 share additional regions of sequence homology with SPL7.…”