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. image In Arabidopsis , the transcription factor PIF7 plays a dominant role in ameliorating the impact shade conditions have on fitness. In this study, a PIF7‐ASF1‐HIRA regulatory module is found to mediate H3.3 incorporation at a subset of shade‐responsive loci , leading to shade‐induced gene expression and morphological adaptation. PIF7 recruits the ASF1‐HIRA complex under shade conditions ASF1 and HIRA positively regulate shade‐induced hypocotyl elongation and define changes in gene expression Shade increases ASF1 and H3.3 enrichment in the chromatin of a subset of PIF7 target genes A PIF7‐ASF1‐HIRA regulatory module is responsible for H3.3 incorporation in the shade