Abstract
PHR2, a central regulator of phosphate signaling in rice, enhanced the expression of phosphate starvation-induced (PSI) genes and resulted in the enhancement of Pi acquisition under Pi deficiency stress. This occurred via PHR2 binding to a cis-element named the PHR1 binding sequences. However, the transcription level of PHR2 was not responsive to Pi starvation. So how is activity of transcription factor PHR2 adjusted to adapt diverse Pi status? Here, we identify an SPX family protein, Os-SPX4 (SPX4 hereafter), involving in Pi starvation signaling and acting as a negative regulator of PHR2. SPX4 is shown to be a fast turnover protein. When Pi is sufficient, through its interaction with PHR2, SPX4 inhibits the binding of PHR2 to its cis-element and reduces the targeting of PHR2 to the nucleus. However, when plants grow under Pi deficiency, the degradation of SPX4 is accelerated through the 26S proteasome pathway, thereby releasing PHR2 into the nucleus and activating the expression of PSI genes. Because the level of SPX4 is responsive to Pi concentration and SPX4 interacts with PHR2 and regulates its activity, this suggests that SPX4 senses the internal Pi concentration under diverse Pi conditions and regulates appropriate responses to maintain Pi homeostasis in plants.
Highlights
It is essential for an organism to sense its ever-changing nutrient status and reprogram its gene expression to achieve the optimal growth and development
To investigate the potential components involved in regulating the activity of PHR2, a Co-IP assay was used to identify the proteins interacting with PHR2
Immunoblotting showed successful expression of PHR2 protein and induced phosphate starvation-induced (PSI) gene expression, excessive Pi accumulation, plant growth inhibition, and necrosis in old leaf tips, which was observed in the seedlings of OxPHR2-FLAG under Pi abundant condition (Supplemental Figure 1), showing the same phenotype of PHR2 overexpressing plants (Zhou et al, 2008)
Summary
2010; Ren et al, 2012; Wang et al, 2013). the central regulator itself is not very responsive to Pi starvation. At least three pathways for Pi signaling and Pi homeostasis under the control of the central regulators have been revealed: (1) PHR1 positively regulates IPS1 (a noncoding RNA) and miR399 for reciprocal regulation of the transcript level of PHO2 for an ubiquitin-conjugating E2 enzyme (UBC24). (2) At-PHR1 (PHR2) positively regulates miR827 for cleavage of two target genes, SPX-MFS1 and SPX-MFS2, involved in Pi homeostasis in the vacuole (Lin et al, 2010; Wang et al, 2012), and (3) PHR2 directly regulates Pi transporter genes, such as the lowaffinity Pi transporter gene PT2, which plays a crucial role in rootto-shoot Pi translocation (Ai et al, 2009; Liu et al, 2010). SPX4 antagonizes PHR2 activity in regulating expression of PSI genes and maintaining phosphate homeostasis. Pi starvation accelerates SPX4 degradation via the 26S proteasome pathway, which can facilitate PHR2 translocation into nucleus to its binding to P1BS motifs, triggering Pi starvation signaling
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