Proposed model integrating genetic and epigenetic controls of heat responses. Genes and proteins are represented in boxes and circles, respectively. The genes and proteins in color are involved in the epigenetic regulation of heat responses. The four putative heat sensors, H2A.Z, the calcium channel in the plasma membrane (CNGCs), two unfolded protein sensors in ER (ER-UPR) and the cytosol (Cyt-UPR), are indicated. The speculative regulatory paths are indicated with broken arrows. (A) Warm temperature mediates the morphological acclimation and acceleration of flowering. Under warm temperatures, the expression of PIF4 could be induced by the eviction of H2A.Z at its promoter. PIF4 binds to the promoters of target genes and plays a central role in the morphological acclimation and acceleration of flowering. Warm temperature also induces the transition from SVP-FLM-β to the competing SVP-FLM-δ complex, the latter is then released from the promoter of FT. The inhibition of ta-siRNAs (green box) through the down-regulation of SGS3 protein (red circle) by warm temperature may be also involved in the morphological acclimation. (B) The genetic mechanisms of temperature entrainment and temperature compensation are proposed. ELF3, PRR7 and PRR9 are involved in temperature entrainment, while CCA1, LHY, PRR7, PRR9, GI, CK2, RVE8, FBH1 and HsfB2b are proved to play roles in temperature compensation. Note that histone modifications of LHY, CCA1, TOC1, PRR7 and PRR9, such as H3K56ac, H3K9/14ac, H3K4me3 and H3K4me2, may (question mark) be regulated by high temperatures. (C) High temperature inhibits R genes-mediated ETI and enhances RNA-silencing mediated resistance. Reduced H2A.Z-containing nucleosome occupancy or other unknown mechanism are likely involved in the modulation of clock (B) and immunity (C). (D) Heat sensors and main signal transduction pathways in heat stress responses (HSR) are shown. Heat stress activates CNGCs, ER-UPR, and Cyt-UPR, and triggers signaling through multiple kinases as well as transcriptional regulators of the HSR, such as HSFs, MBF1c, and Rboh. RPS1 in the chloroplast also responds to heat stress, and generates a retrograde signal to activate HsfA2-dependent heat-responsive genes in the nucleus. Some csRNAs are highly sensitive to heat stress and may regulate RPS1-mediated heat stress responses. Heat stress also affects the production of some ra-siRNAs, miRNAs, ta-siRNAs, nat-siRNAs, and lncRNAs. These non-coding RNAs may regulate HSFs, HSPs, and other target genes that function in heat acclimation. The NRPD2 (olive box) and HDA6 (purple box)-dependent RdDM pathway and the CMT2 (gray box)-dependent CHH methylation may be required for thermotolerance. AtASF1A/B proteins (blue circle) are recruited onto chromatin and facilitate H3K56ac, which promotes the activation of some HSFs and HSPs. The chromatin-remodeling gene CHR12 (light purple box) plays a vital role in mediating the temporary growth arrest of Arabidopsis under heat stress. Repetitive heat stress has also been reported to modulate PTI in a HAC1 (yellow box)-dependent manner. Many unknown steps (?) remain to be recognized in this model.
