A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis

Abstract

Plants respond to different stresses by inducing or repressing transcription of partially overlapping sets of genes. In Arabidopsis, the PHR1 transcription factor (TF) has an important role in the control of phosphate (Pi) starvation stress responses. Using transcriptomic analysis of Pi starvation in phr1, and phr1 phr1-like (phl1) mutants and in wild type plants, we show that PHR1 in conjunction with PHL1 controls most transcriptional activation and repression responses to phosphate starvation, regardless of the Pi starvation specificity of these responses. Induced genes are enriched in PHR1 binding sequences (P1BS) in their promoters, whereas repressed genes do not show such enrichment, suggesting that PHR1(-like) control of transcriptional repression responses is indirect. In agreement with this, transcriptomic analysis of a transgenic plant expressing PHR1 fused to the hormone ligand domain of the glucocorticoid receptor showed that PHR1 direct targets (i.e., displaying altered expression after GR:PHR1 activation by dexamethasone in the presence of cycloheximide) corresponded largely to Pi starvation-induced genes that are highly enriched in P1BS. A minimal promoter containing a multimerised P1BS recapitulates Pi starvation-specific responsiveness. Likewise, mutation of P1BS in the promoter of two Pi starvation-responsive genes impaired their responsiveness to Pi starvation, but not to other stress types. Phylogenetic footprinting confirmed the importance of P1BS and PHR1 in Pi starvation responsiveness and indicated that P1BS acts in concert with other cis motifs. All together, our data show that PHR1 and PHL1 are partially redundant TF acting as central integrators of Pi starvation responses, both specific and generic. In addition, they indicate that transcriptional repression responses are an integral part of adaptive responses to stress.

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

“…Since most regulated genes that respond to Pi starvation are under the control of the Myb transcription factor PHR1 and its close homolog PHL1 Bustos et al, 2010;Thibaud et al, 2010;Pant et al, 2015;Sun et al, 2016), we examined the role of these factors in PPsPase1 and PECP1 induction, including MGD3 as a control. By comparing gene induction levels using RT-qPCR in the wild type and phr1 phl1 double mutants , we observed that only a residual induction remained for these three genes in phr1 phl1 (Fig.…”

“…The fugu5-1 through -3 mutants as well as fugu5-1 PromAVP1:IPP1 #8-3 were previously described (Ferjani et al, 2011). The phr1 phl1 double mutant was also previously described (González et al, 2005;Bustos et al, 2010) …”

mRNA-Seq Reveals a Comprehensive Transcriptome Profile of Rice under Phosphate Stress

“…In Arabidopsis, the direct targets of PHR1 are greatly enriched in P1BS-containing Pi starvation-induced genes (Bustos et al 2010). Therefore, PHR1 is maybe upregulated in late stages of −P stress via a P1BS cis-acting element.…”

“…Some transcripts may be regulated through the release from repression of PHO2/ UBC24 or regulated by other factors such as PHL1. Both PHR1 and PHL1 were found to be partially redundant and have a central role in the control of physiological and molecular responses to -P stress (Bustos et al 2010).…”

Phosphate starvation induces DNA methylation in the vicinity of cis-acting elements known to regulate the expression of phosphate–responsive genes

“…A number of transcription factors including the master regulator PHOSPHATE RESPONSE 1 (PHR1), and several members of the MYB and WRKY families of transcription factors have been shown to regulate the transcriptional activation of lowphosphate responsive genes and their corresponding binding sites P1BS, MBS and the W-box, respectively, act as cis-acting elements that mediate Pi starvation-responsive expression. [15][16][17][18][19][20] A search for these cis-acting motifs in Pi-methDEGs showed that 39 of these genes contained P1BS motifs, that present the palindromic 8 base pair sequence (GNATATNC) where PHR1 binds to DNA as a dimer, 15 93 genes had W-box elements which are the cognate binding sites of WRKY transcription factors, which have been characterized as key regulators of several processes in plants, including some members of this family which are specifically involved in the response to low Pi conditions, 17,19,21,22 and 80 genes contained MYB transcription factors Binding sites (MBS) (Fig. 1B).…”