PIF7‐mediated epigenetic reprogramming promotes the transcriptional response to shade in Arabidopsis

Abstract

For shade‐intolerant plants, changes in light quality through competition from neighbors trigger shade avoidance syndrome (SAS): a series of morphological and physiological adaptations that are ultimately detrimental to plant health and crop yield. Phytochrome‐interacting factor 7 (PIF7) is a major transcriptional regulator of SAS in Arabidopsis; however, how it regulates gene expression is not fully understood. Here, we show that PIF7 directly interacts with the histone chaperone anti‐silencing factor 1 (ASF1). The ASF1‐deprived asf1ab mutant showed defective shade‐induced hypocotyl elongation. Histone regulator homolog A (HIRA), which mediates deposition of the H3.3 variant into chromatin, is also involved in SAS. RNA/ChIP‐sequencing analyses identified the role of ASF1 in the direct regulation of a subset of PIF7 target genes. Furthermore, shade‐elicited gene activation is accompanied by H3.3 enrichment, which is mediated by the PIF7‐ASF1‐HIRA regulatory module. Collectively, our data reveal that PIF7 recruits ASF1‐HIRA to increase H3.3 incorporation into chromatin to promote gene transcription, thus enabling plants to effectively respond to environmental shade.

PIF transcription factors-versatile plant epigenome landscapers

“…Secondly, most epigenome features can be directly and simultaneously governed by functionally diverse PIF-CR complexes. Thirdly, several PIF-CR modules, such as PIF-INO80-C, PIF-MRG1/2, and PIF-ASF1-HIRA are operational in multiple response pathways like SAS and TM (Shang et al, 2021;Willige et al, 2021;Yang et al, 2023;Zhao et al, 2023;Zhou et al, 2024), indicating that these complexes belong to the general repertoire of PIF-mediated transcriptional regulation.…”

“…The deposition of H3.3 is in part mediated by the histone chaperones ASF1A (ANTI-SILENCING FUNCTION 1A) and ASF1B in conjunction with the histone chaperone HIRA (HISTONE REGULATORY HOMOLOG A) (Tagami et al, 2004;Zhu et al, 2011;Nie et al, 2014;Duc et al, 2015;Zhong et al, 2022). 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.…”

“…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).…”

Molecular mechanisms underlying coordinated responses of plants to shade and environmental stresses

“…Dephosphorylated PIF7 was recently shown to interact with the EIN6 ENHANCER (EEN) subunit of the chromatin remodeling complex INO80, thus facilitating shade‐induced H2A.Z removal from chromatin to promote transcription of PIF7 target genes (Willige et al., 2021). A more recent study showed that dephosphorylated PIF7 could also recruit the complex composed of the histone chaperone anti‐silencing factor 1 (ASF1) and histone regulator homolog A (HIRA) to increase H3.3 incorporation into chromatin, thus promoting gene transcription in response to shade (Yang et al., 2023). In addition, two ubiquitin‐specific proteases, UBIQUITIN‐SPECIFIC PROTEASE12 (UBP12) and UBP13, directly interact with PIF7 to promote its stability through de‐ubiquitination, thereby positively regulating SAS (Zhou et al., 2021).…”

Extra- and intranuclear heat perception and triggering mechanisms in plants

“…Consequently, this activation triggers the transcription of key genes associated with thermomorphogenesis ( Chung et al., 2020 ; Fiorucci et al., 2020 ) ( Figure 2 ). PIF7 has been identified as the predominant transcriptional regulator of thermomorphogenesis and the shade avoidance syndrome in plants ( Burko et al., 2022 ; Yang et al., 2023 ). These findings illustrate a thermosensory mechanism in which the hairpin structure of PIF7 mRNA functions as a heat sensor in the cytoplasm, initiating a conformational change that transduces the thermal signal to the nucleus, ultimately leading to the induction of downstream transcriptional responses.…”