Arabidopsis Phytochrome A Directly Targets Numerous Promoters for Individualized Modulation of Genes in a Wide Range of Pathways

Abstract

The far-red light (FR) photoreceptor phytochrome A (phyA) contains no DNA binding domain but associates with the CHALCONE SYNTHASE promoter through its chaperone FAR-RED ELONGATED HYPOCOTYL1 and transcription factors. Here, we performed a genome-wide identification of phyA targets using a combination of phyA chromatin immunoprecipitation and RNA sequencing methods in Arabidopsis thaliana. Our results indicate that phyA signaling widely affects gene promoters involved in multiple FR-modulated aspects of plant growth. Furthermore, we observed an enrichment of hormone-and stressresponsive elements in the phyA direct target promoters, indicating that a much broader than expected range of transcription factors is involved in the phyA signaling pathway. To verify our hypothesis that phyA regulates genes other than light-responsive ones through the interaction with corresponding transcription factors, we examined the action of phyA on one of its direct target genes, NAC019, which encodes an abscisic acid-dependent transcription factor. The phyA signaling cascade not only targets two G-boxes on the NAC019 promoter for subsequent transcriptional regulation but also positively coordinates with the abscisic acid signaling response for root elongation inhibition under FR. Our study provides new insight into how plants rapidly fine-tune their growth strategy upon changes in the light environment by escorting photoreceptors to the promoters of hormone-or stress-responsive genes for individualized modulation.

Photoreceptor partner FHY1 has an independent role in gene modulation and plant development under far-red light

“…S1B). Their positions were consistent with that of G-boxes, DNA elements that are critical for phyA-dependent CHS and NAC019 expression (8,9).…”

“…To determine whether phyA and FHY1 associate with the same genes upon FR irradiation, 4-d-old etiolated 35S: GFP-FHY1 fhy1-1 transgenic seedlings (12) were exposed to 3 h FR, the same conditions used for detection of the phyA-associated genes (9). The treated plants were used for ChIP-seq analysis with an anti-FHY1 antibody that exhibits high specificity in the detection of FR-induced FHY1-association events (8).…”

“…Furthermore, genomic analysis suggests that the "phyA-promoter association" model is a universal mechanism of regulation for thousands of phyA-associated genes (9). A wide range of transcription factors may act downstream of phyA for the purpose of recognizing diverse cis-elements that are responsive to multiple internal or external stimuli (9). Therefore, light and other signals are integrated within the cell through phyA.…”

“…The mechanism through which nuclear phyA subsequently regulates a considerable number of FR-modulated genes has been intensively investigated (9,10). It was recently demonstrated that the nuclear phyA-FHY1 complex is recruited to the promoter regions of FR-responsive genes CHS (chalcone synthase) and NAC019 [no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), cup-shaped cotyledon (CUC) 019] through transcription factors to coregulate gene transcription (8,9).…”

“…It was recently demonstrated that the nuclear phyA-FHY1 complex is recruited to the promoter regions of FR-responsive genes CHS (chalcone synthase) and NAC019 [no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), cup-shaped cotyledon (CUC) 019] through transcription factors to coregulate gene transcription (8,9). Furthermore, genomic analysis suggests that the "phyA-promoter association" model is a universal mechanism of regulation for thousands of phyA-associated genes (9). A wide range of transcription factors may act downstream of phyA for the purpose of recognizing diverse cis-elements that are responsive to multiple internal or external stimuli (9).…”