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.
To cope with growth in low-phosphate (Pi) soils, plants have evolved adaptive responses that involve both developmental and metabolic changes. PHOSPHATE STARVATION RESPONSE 1 (PHR1) and related transcription factors play a central role in the control of Pi starvation responses (PSRs). How Pi levels control PHR1 activity, and thus PSRs, remains to be elucidated. Here, we identify a direct Pi-dependent inhibitor of PHR1 in Arabidopsis, SPX1, a nuclear protein that shares the SPX domain with yeast Pi sensors and with several Pi starvation signaling proteins from plants. Double mutation of SPX1 and of a related gene, SPX2, resulted in molecular and physiological changes indicative of increased PHR1 activity in plants grown in Pi-sufficient conditions or after Pi refeeding of Pi-starved plants but had only a limited effect on PHR1 activity in Pi-starved plants. These data indicate that SPX1 and SPX2 have a cellular Pi-dependent inhibitory effect on PHR1. Coimmunoprecipitation assays showed that the SPX1/PHR1 interaction in planta is highly Pi-dependent. DNA-binding and pull-down assays with bacterially expressed, affinity-purified tagged SPX1 and ΔPHR1 proteins showed that SPX1 is a competitive inhibitor of PHR1 binding to its recognition sequence, and that its efficiency is highly dependent on the presence of Pi or phosphite, a nonmetabolizable Pi analog that can repress PSRs. The relative strength of the SPX1/PHR1 interaction is thus directly influenced by Pi, providing a link between Pi perception and signaling.phosphate sensor | phosphate starvation signaling S ince the beginning of molecular genetics, phosphate (Pi) starvation rescue systems, especially the Pi starvation rescues systems of bacteria and yeast, have served as emblematic models for studies of regulation of gene activity. In plants, these systems have gained additional interest because of the complexity and multicellular nature of plants (1, 2), and especially due to their potential for improving Pi acquisition and use in crops, a major goal toward sustainable agriculture. Considerable information has been gathered in the past decade on the components of the Pi starvation signaling pathway (reviewed in refs. 3-6). Major findings in plants include (i) identification of PHOSPHATE STARVATION RESPONSE 1 (PHR1) and related transcription factors as master regulators of Pi starvation responses (PSRs) (7-11); (ii) demonstration of the involvement of ubiquitin system components, including PHO2 and NLA, in Pi signaling (12-16); (iii) identification of miRNAs as mobile signals in Pi homeostasis (17, 18); and (iv) identification of Pi starvation-induced (PSI) riboregulators of miRNA activity, based on target mimicry (19) and natural antisense RNA that activates translation of PHO1 mRNA (20). In addition, a singular characteristic of nutrient starvation responses in plants is that several of these responses are at long distance, systemically controlled by plant shoot nutrient status, whereas others are controlled by local nutrient concentration. Transcriptomic a...
SUMMARYPhosphate is a crucial and often limiting nutrient for plant growth. To obtain inorganic phosphate (P i ), which is very insoluble, and is heterogeneously distributed in the soil, plants have evolved a complex network of morphological and biochemical processes. These processes are controlled by a regulatory system triggered by P i concentration, not only present in the medium (external P i ), but also inside plant cells (internal P i ). A 'splitroot' assay was performed to mimic a heterogeneous environment, after which a transcriptomic analysis identified groups of genes either locally or systemically regulated by P i starvation at the transcriptional level. These groups revealed coordinated regulations for various functions associated with P i starvation (including P i uptake, P i recovery, lipid metabolism, and metal uptake), and distinct roles for members in gene families. Genetic tools and physiological analyses revealed that genes that are locally regulated appear to be modulated mostly by root development independently of the internal P i content. By contrast, internal P i was essential to promote the activation of systemic regulation. Reducing the flow of P i had no effect on the systemic response, suggesting that a secondary signal, independent of P i , could be involved in the response. Furthermore, our results display a direct role for the transcription factor PHR1, as genes systemically controlled by low P i have promoters enriched with P1BS motif (PHR1-binding sequences). These data detail various regulatory systems regarding P i starvation responses (systemic versus local, and internal versus external P i ), and provide tools to analyze and classify the effects of P i starvation on plant physiology.
Plants count on a wide variety of metabolic, physiological, and developmental responses to adapt their growth to variations in mineral nutrient availability. To react to such variations plants have evolved complex sensing and signaling mechanisms that allow them to monitor the external and internal concentration of each of these nutrients, both in absolute terms and also relatively to the status of other nutrients. Recent evidence has shown that hormones participate in the control of these regulatory networks. Conversely, mineral nutrient conditions influence hormone biosynthesis, further supporting close interrelation between hormonal stimuli and nutritional homeostasis. In this review, we summarize these evidences and analyze possible transcriptional correlations between hormonal and nutritional responses, as a means to further characterize the role of hormones in the response of plants to limiting nutrients in soil.
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