PIF4 Promotes Expression of HSFA2 to Enhance Basal Thermotolerance in Arabidopsis

Abstract

Heat stress (HS) seriously restricts the growth and development of plants. When plants are exposed to extreme high temperature, the heat stress response (HSR) is activated to enable plants to survive. Sessile plants have evolved multiple strategies to sense and cope with HS. Previous studies have established that PHYTOCHROME INTERACTING FACTOR 4 (PIF4) acts as a key component in thermomorphogenesis; however, whether PIF4 regulates plant thermotolerance and the molecular mechanism linking this light transcriptional factor and HSR remain unclear. Here, we show that the overexpression of PIF4 indeed provides plants with a stronger basal thermotolerance and greatly improves the survival ability of Arabidopsis under severe HS. Via phylogenetic analysis, we identified two sets (six) of PIF4 homologs in wheat, and the expression patterns of the PIF4 homologs were conservatively induced by heat treatment in both wheat and Arabidopsis. Furthermore, the PIF4 protein was accumulated under heat stress and had an identical expression level. Additionally, we found that the core regulator of HSR, HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2), was highly responsive to light and heat. Followed by promoter analysis and ChIP-qPCR, we further found that PIF4 can bind directly to the G-box motifs of the HSFA2 promoter. Via effector–reporter assays, we found that PIF4 binding could activate HSFA2 gene expression, thereby resulting in the activation of other HS-inducible genes, such as heat shock proteins. Finally, the overexpression of PIF4 led to a stronger basal thermotolerance under non-heat-treatment conditions, thereby resulting in an enhanced tolerance to severe heat stress. Taken together, our findings propose that PIF4 is linked to heat stress signaling by directly binding to the HSFA2 promoter and triggering the HSR at normal temperature conditions to promote the basal thermotolerance. These functions of PIF4 provide a candidate direction for breeding heat-resistant crop cultivars.

Conservation of heat stress acclimation by the inositol polyphosphate multikinase, IPMK responsible for 4/6-InsP7production in land plants

“…To gain mechanistic insights, we first tested whether genes encoding members of HSP families, that play role in heat stress acclimation (Hahn et al, 2011; Li et al, 2023; Yang et al, 2022), are differentially expressed in the knockdown lines. Our analyses showed that the expression of different HSP s is largely compromised in the atipk2β -/- atipk2α kd lines when compared to Col-0 plants (" ref-type="fig">Fig.…”

Abiotic Stress in Crop Production

“…The most well-known group of thermoresponsive interacting partners is the phytochrome-interacting factor (PIF) family [ 67 ]. The importance of PIFs for thermomorphogenesis has been observed in Arabidopsis and members of this family have also been identified in wheat, tomatoes, and rice [ 68 , 69 , 70 , 71 ], whereas increased expression levels of PIFs under high temperatures have been confirmed in maize [ 72 ]. The activity of PIF4 can influence the function of the heat-responsive gene EARLY FLOWERING 3 ( ELF3) in Arabidopsis , barley, and wheat [ 73 , 74 , 75 ].…”

Molecular Genetics Enhances Plant Breeding

“…Several teams pursued this goal as part of the current Special Issue. For example, Yang et al [ 19 ] and Zhang et al [ 20 ] used the Columbia-0 (Col) A. thaliana ecotype to validate the functional roles of PIF4 and AtEAU ( 1 and 2 ) genes, respectively, through transcriptomic tools as boosters and repressors of basal thermotolerance and ABA response. Meanwhile, Kong et al [ 21 ] and Zhang et al [ 22 ], respectively, implemented epigenomics and qRT-PCR in cabbage ( B. oleracea ) and Chinese cabbage ( B. rapa ) to study the DNA methylation footprint during microspore embryogenesis induced by heat shock, and the functional role of BrGOLDEN in carotenoid biosynthesis.…”