Cracking the code of plant central phosphate signaling

Topic - Discovery of plant central phosphate signaling


Phosphate (Pi) is involved in numerous metabolic processes and plays a vital role in plant growth. Green plants have evolved intricate molecular bases of Pi-signaling to maintain cellular Pi homeostasis. Here, we summarize recent advances in the molecular and structural bases of central Pi-signaling and discuss pending questions.

Discovery of the core elements involved in P signaling

(A) Key studies uncovering the molecular and structural basis of P signaling machines. The timeline is based on the original publication date. PHOSPHATE STARVATION RESPONSE proteins (PHRs) were first reported in 2001 to be the core transcription factors regulating P starvation response (PSR) genes by binding to their P1BS cis-element in plants [1]. In 2014, two independent works uncovered that a class of SPX (named after SYG1/Pho81/XPR1) -domain-only proteins, SPXs, are direct inhibitors of PHR1 in Arabidopsis and rice [2,3]. Subsequently, Wild and colleagues confirmed that SPX domains provide a primary binding surface for InsPs, and InsPs communicate cytosolic Pi levels to SPX domains, thus controlling the Pi homeostasis [5]. Until 2019, two works in Arabidopsis showed that InsP8 is the signaling translator of cellular P status, and the level of InsP8 is controlled by a bifunctional enzyme VIHs (named after Vip1 homologs), whose functions are sensitive to cellular ATP contents [6,7]. Then, four studies in Arabidopsis and rice decoded the crystal structures of the SPX-InsP-PHR complex and identified the crucial amino acid residues involved in molecular interactions [8–11]. PHRs and SPX-containing proteins mentioned in this figure are from Arabidopsis thaliana (At), Oryza sativa (Os), Saccharomyces cerevisiae (Sc), Homo sapiens (Hs), and Chaetomium thermophilum (Ct). (B) The proposed working model of Pi-signaling machines. Under Pi-sufficient conditions, higher cellular Pi and ATP levels favor the kinase activity of VIHs and result in the accumulation of InsP8, which could trigger the binding of the InsP8-SPX complex with PHRs forming a 2:2:2 complex to repress the PSR via blocking PHR interaction with DNA. In contrast, under Pi starvation, decreased InsP8 results in the dissociation of SPXs from PHRs, thus PHRs form a dimer and bind the P1BS elements of PSR genes to activate their expression.


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