Coordinated histone variant H2A.Z eviction and H3.3 deposition control plant thermomorphogenesis

Abstract

Summary Plants can sense temperature changes and adjust their development and morphology accordingly in a process called thermomorphogenesis. This phenotypic plasticity implies complex mechanisms regulating gene expression reprogramming in response to environmental alteration. Histone variants often associate with specific chromatin states; yet, how their deposition/eviction modulates transcriptional changes induced by environmental cues remains elusive. In Arabidopsis thaliana, temperature elevation‐induced transcriptional activation at thermo‐responsive genes entails the chromatin eviction of a histone variant H2A.Z by INO80, which is recruited to these loci via interacting with a key thermomorphogenesis regulator PIF4. Here, we show that both INO80 and the deposition chaperones of another histone variant H3.3 associate with ELF7, a critical component of the transcription elongator PAF1 complex. H3.3 promotes thermomorphogenesis and the high temperature‐enhanced RNA Pol II transcription at PIF4 targets, and it is broadly required for the H2A.Z removal‐induced gene activation. Reciprocally, INO80 and ELF7 regulate H3.3 deposition, and are necessary for the high temperature‐induced H3.3 enrichment at PIF4 targets. Our findings demonstrate close coordination between H2A.Z eviction and H3.3 deposition in gene activation induced by high temperature, and pinpoint the importance of histone variants dynamics in transcriptional regulation.

PIF transcription factors-versatile plant epigenome landscapers

“…In addition, asf1ab and hira mutants show also reduced hypocotyl elongation under EAT (Yang et al, 2023;Zhao et al, 2023) which suggest that the PIF-ASF1A/B-HIRA module is also operational during TM. Although a PIF4-ASF1A/B interaction has not been confirmed, ASF1A/B could also be indirectly recruited by PIF4 through the INO80 ATPase that associates with ASF1A/B through the TEF PAF1c (Polymerase-Associated Factor 1 complex) subunit ELF7 (EARLY FLOWERING 7) (Figure 1) (Zhao et al, 2023). These findings highlight again the prominent role of PIFs in initiating epigenomic reprogramming through the recruitment of functionally diverse CRs.…”

“…During SAS, PIF7 recruits ASF1A/B and HIRA to facilitate H3.3 deposition at shade-responsive genes (Figure 1) (Yang et al, 2023). In addition, asf1ab and hira mutants show also reduced hypocotyl elongation under EAT (Yang et al, 2023;Zhao et al, 2023) which suggest that the PIF-ASF1A/B-HIRA module is also operational during TM. Although a PIF4-ASF1A/B interaction has not been confirmed, ASF1A/B could also be indirectly recruited by PIF4 through the INO80 ATPase that associates with ASF1A/B through the TEF PAF1c (Polymerase-Associated Factor 1 complex) subunit ELF7 (EARLY FLOWERING 7) (Figure 1) (Zhao et al, 2023).…”

“…In plants, INO80-C's role in H2A.Z eviction was shown for ethylene-, low R:FR light-, and EAT-induced genes (Zander et al, 2019;Willige et al, 2021;Xue et al, 2021). INO80-C additionally acts as a platform for recruiting other CRs, thereby potentially expanding the functional capabilities of the PIF-INO80-C regulatory module (Shang et al, 2021;Xue et al, 2021;Zhao et al, 2023). Its subunit EEN interacts with WDR5a (WD40 REPEAT 5), an integral component of the COMPASS (Complex Proteins Associated with Set1) histone H3K4 methyltransferase complex, to facilitate trimethylation of histone 3 lysine 4 (H3K4me3) at PIF4 target genes (Figure 1) (Xue et al, 2021).…”

Histone variants shape chromatin states in Arabidopsis

“…How are chromatin states maintained ? In mammalian cells, there is a broad maintenance of the The positive feedback loops that maintain histone modifications become inactive and reversion to active chromatin states becomes possible by the deposition of H3.3 and eviction of H2A.Z by INO80 in response to temperature (Zhao et al, 2023) or to light (Willige et al, 2023).…”

Complex regulation of flowering by high temperatures

“…Whether H2A.Z eviction is connected with the deactivation of the SVP‐FLM complex is unknown, but at some other thermal‐responsive loci, the removal of H2A.Z depends on a transcription factor PIF4 that recruits the INO80 chromatin remodelling complex. H2A.Z eviction per se is not sufficient for transcriptional activation, rather, it is linked with the deposition of another histone variant H3.3 and an active histone modification H3K4me3 (Xue et al, 2021; Zhao et al, 2023). These findings highlight the coordination of transcription factors with multiple epigenetic modifiers in modulating the transcription of temperature‐responsive genes.…”