Arabidopsis thalianaBBX14 is a target of GLK1 and involved in high-light acclimation, photomorphogenesis and GUN-type retrograde signaling

Abstract

SUMMARYDevelopment of photosynthetically competent seedlings requires both light and retrograde biogenic signaling pathways. The transcription factor GLK1 functions at the interface between these pathways, and receives input from the biogenic-signaling integrator GUN1. BBX14 was previously identified, together with GLK1, in a core module that mediates the response to high light levels and biogenic signaling. To gain insight into the function of BBX14, we generatedBBX14overexpressors and CRISPR/Cas-mediatedbbx14mutant plants, conducted high-light, RT-qPCR and ChIP-Seq experiments, measured photosynthetic parameters, chlorophyll contents and growth rates, and analyzed alterations in transcriptomics. We found that, although overexpression of BBX14 is deleterious under normal growth conditions, BBX14 is needed to acclimate plants to high light stress.BBX14is a direct target of GLK1, and RNA-Seq analysis suggests that BBX14 is involved in the circadian clock. Knockout ofBBX14results in a long-hypocotyl phenotype that depends on a retrograde signal, andBBX14expression during biogenic signaling requires GUN1. Finally, we clarify the role of BBX14 in GUN-type biogenic signaling. We conclude that BBX14 is an integrator of photomorphogenetic and biogenic signals, and suggest that BBX14 is a nuclear target of retrograde signals downstream of the GUN1/GLK1 module.

Natural genetic variation inGLK1-mediated photosynthetic acclimation in response to light

“…To understand the natural diversity and potential adaptation of the nuclear gene regulatory network controlling photosynthetic activity to different natural environments, we characterized the expression variation of GLK1 candidate target genes across 727 Arabidopsis accessions collected from a wide range of habitats. We previously performed chromatin immunoprecipitation followed by high throughput sequencing (ChIP-seq) for GLK1 [14]. As expected, those data show that GLK1 directly binds to genes with central roles in chlorophyll biosynthesis and photosynthesis activity, including genes needed for acclimation to high-light levels.…”

“…GLK1 was predicted to be associated with (in order of importance) GLK2, LZF1, GNC, BEH1, and BCM1. Indeed, GLK2 may cross-regulate with GLK1 as they bind each other’s promoters [14, 18]. LZF1/BBX22 is a B-box protein involved in the positive regulation of photomorphogenesis [35].…”

“…LZF1/BBX22 is a B-box protein involved in the positive regulation of photomorphogenesis [35]. Other B-box TFs are regulated by GLK1 [14, 25]. GNC and GLK1 have overlapping functions coordinating chloroplast development [15].…”

“…GLK1 target gene networks have been characterized previously by us and others [14, 18]. This offers an interesting resource and starting point to investigate natural variation in transcriptional regulatory networks underlying photosynthetic acclimation and its plasticity under different local habitat environments.…”

“…In Arabidopsis, GLK TFs promote the expression of many nuclear-encoded photosynthetic genes that are associated with chlorophyll biosynthesis and light-harvesting antenna proteins [13]. They bind and potentially regulate genes involved in acclimation to high light conditions [14, 15]. The glk1 glk2 double mutant exhibits a reduction in NPQ [15], consistent with lowered Chl b levels.…”