Genome accessibility dynamics in response to phosphate limitation is controlled by the PHR1 family of transcription factors inArabidopsis

Abstract

As phosphorus is one of the most limiting nutrients in many natural and agricultural ecosystems, plants have evolved strategies that cope with its scarcity. Genetic approaches have facilitated the identification of several molecular elements that regulate the phosphate (Pi) starvation response (PSR) of plants, including the master regulator of the transcriptional response to phosphate starvation PHOSPHATE STARVATION RESPONSE1 (PHR1). However, the chromatin modifications underlying the plant transcriptional response to phosphate scarcity remain largely unknown. Here, we present a detailed analysis of changes in chromatin accessibility during phosphate starvation in Arabidopsis thaliana root cells. Root cells undergo a genome-wide remodeling of chromatin accessibility in response to Pi starvation that is often associated with changes in the transcription of neighboring genes. Analysis of chromatin accessibility in the phr1 phl2 double mutant revealed that the transcription factors PHR1 and PHL2 play a key role in remodeling chromatin accessibility in response to Pi limitation. We also discovered that PHR1 and PHL2 play an important role in determining chromatin accessibility and the associated transcription of many genes under optimal Pi conditions, including genes involved in the PSR. We propose that a set of transcription factors directly activated by PHR1 in Pi-starved root cells trigger a second wave of epigenetic changes required for the transcriptional activation of the complete set of low-Pi–responsive genes.

PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis

“…PHR2 supports AM development at LP because it promotes the expression of a number of genes required for AM development and function already in the absence of AMF. This possibly occurs through the effect of PHR2 on chromatin accessibility, as recently shown in Arabidopsis 38 . We detected PHR2 targets using ChIP-Seq in the absence of AMF and these comprise strigolactone biosynthesis genes needed for strigolactone exudation to activate the fungus 31 , 33 , membrane receptors needed for perception of fungal signals 39 , 40 and genes belonging to the common symbiosis signal transduction cascade, which is thought to relay the signals to the nucleus to activate gene expression, and which is required for fungal entry into the root 14 .…”

A phosphorus‐limitation induced, functionally conserved DUF506 protein is a repressor of root hair elongation in plants

“…RHD6‐LIKE4 (RSL4), which is functionally conserved in higher plants, regulates expression of various genes involved in RH outgrowth through direct binding to specific cis ‐elements (RH elements; RHEs) in their proximal promoter regions, and consequently controls RH elongation (Yi et al ., 2010 ; Datta et al ., 2015 ; Kim & Dolan, 2016 ). The MYB TF PHOSPHATE STARVATION RESPONSE1 (PHR1) and its homolog PHR1‐LIKE (PHL1), play central roles in the P starvation response of Arabidopsis (Rubio et al ., 2001 ; Bari et al ., 2006 ; Bustos et al ., 2010 ; Rouached et al ., 2011 ; Sun et al ., 2016 ; Barragán‐Rosillo et al ., 2021 ). Overexpression (OX) of PHR1 significantly increases RH length, whereas in the phr1 phl1 double mutant, RHs are much shorter in P‐limiting conditions (Bustos et al ., 2010 ).…”

PHOSPHATE STARVATION RESPONSE enables arbuscular mycorrhiza symbiosis

“…PHR2 supports AM development at LP because it promotes the expression of a number of genes required for AM development and function already in the absence of AMF. This possibly occurs through the effect of PHR2 on chromatin accessibility, as recently shown in Arabidopsis 38 . We detected direct PHR2 targets using ChIP-Seq in the absence of AMF and these comprise strigolactone biosynthesis genes needed for strigolactone exudation to activate the fungus 31,33 , membrane receptors needed for perception of fungal signals 39,40 and genes belonging to the common symbiosis signal transduction cascade, which is thought to relay the signals to the nucleus to activate gene expression, and which is required for fungal entry into the root 14 .…”