Abstract
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.
Highlights
To cope with growth in low-phosphate (Pi) soils, plants have evolved adaptive responses that involve both developmental and metabolic changes
We examined a functional MYC-tagged form of PHOSPHATE STARVATION RESPONSE 1 (PHR1) expressed under the control of its own promoter (PHR1pro::PHR1-MYC), whose activity is Pi-dependent, and found that PHR1-MYC accumulation and its posttranslational modification pattern are relatively unaffected by Pi starvation (Fig. S1 A and B), suggesting that Pi control of PHR1 activity involves an accessory protein
One candidate PHR1 partner was SPX1 (Fig. S2), described as a nuclear protein involved in Pi signaling [34], which has an SPX domain present in yeast Pi sensors
Summary
To cope with growth in low-phosphate (Pi) soils, plants have evolved adaptive responses that involve both developmental and metabolic changes. Since 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. Potential systemic signals that affect Pi starvation have been described, and some components that control local PSRs have been identified genetically [6, 22,23,24,25,26,27] Despite this progress in the dissection of Pi starvation signaling in plants, very little is known of how Pi levels are sensed or of the early steps in this signaling pathway. A role for Pi as a signal has been established [41], in these microorganisms, additional metabolites, such as myo-D-inositol heptakisphosphate, whose synthesis is increased by Pi starvation, act as signals under Pi starvation stress [29]
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