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Starve or share? Phosphate availability shapes plant–microbe interactions
Phosphorus is an essential macronutrient that supports core biological processes such as photosynthesis, respiration, and the biosynthesis of nucleic acids and membranes [1]. Plants take up phosphorus from the soil as inorganic orthophosphate (Pi) [2], yet Pi is poorly available in most soils due to its rapid fixation into insoluble complexes with iron and aluminium in acidic soils, and calcium in alkaline soils [3]. Consequently, Pi availability is a major limitation for plant growth and crop productivity [3]. To cope with Pi deficiency, plants have evolved a highly coordinated network of local and systemic phosphate starvation responses (PSRs) that are rapidly reversed upon Pi resupply. These PSRs involve morphological, transcriptional, and metabolic adjustments. Local responses primarily reshape root system architecture (e.g., inhibition of primary root growth, root hair formation and lateral root formation), systemic responses aim to maintain Pi homeostasis through improved Pi uptake, recycling, and utilisation [3]. In Arabidopsis, systemic PSRs are orchestrated by the MYB-type coiled-coil transcription factor Phosphate Response 1 (PHR1; [4]) and its homologues PHR1-likes (PHLs; [5–7], and orthologs have been described in several plant species [8–12] (Fig 1). These transcription factors activate Pi starvation-induced (PSI) genes by binding to the PHR1 Binding Sequence (P1BS) in their promoters [4] (Fig 1A). Among the targets are genes encoding high-affinity Pi transporters and enzymes involved in membrane phospholipids remodelling [3,5,13,14]. PHR activity is tightly regulated by SYG1/Pho81/XPR1 (SPX) domain-containing proteins. SPX domains act as high-affinity receptors for inositol pyrophosphates (PP-InsPs), which serve as proxies for cellular Pi status and mediate the interaction between SPX and PHR [15–17] thereby inhibiting PHR by sequestering it away from the nucleus or DNA [18–22] (Fig 1A). Interestingly, Pi signalling is not isolated but tightly interconnected with nitrogen status. In rice, under high nitrate conditions, the nitrate sensor Nitrate Transporter 1.1B (NRT1.1B; [23]) interacts with SPX4, promoting SPX4 degradation via the E3 ligase NRT1.1B interacting protein 1 (NBIP1; [24]). As a result, PHR2 and NIN-like protein 3 (NLP3; [25]) are released from SPX-mediated inhibition, translocate into the nucleus and activate PSI and nitrate-response genes, respectively [24]. In Arabidopsis, the expression of several PSI genes is reduced in an nrt1.1 mutant and is influenced not only by Pi but also by nitrate availability [26]. Furthermore, PHR1 and NLPs regulate the expression of Nitrate-Inducible GARP-type Transcriptional Repressor 1 (NIGT1) genes, which encode repressors of specific nitrate-response genes [27] as well as SPX genes [28]. These examples illustrate the tight interconnection between Pi and nitrate signalling, which has been comprehensively reviewed elsewhere [29,30]. MicroRNAs, particularly miR399 and miR827, add additional layers of regulation by downregulating negative regulators of Pi uptake, contributing to a robust and multi-tiered response system [31–35]. Notably, the SPX–PHR regulatory module is evolutionarily conserved across land plants, including early diverging lineages such as Marchantia polymorpha, highlighting its fundamental role in signalling [36].
