Milestones in understanding transport, sensing, and signaling of the plant nutrient phosphorus

Abstract

As an essential nutrient element, phosphorus (P) is primarily acquired and translocated as inorganic phosphate (Pi) by plant roots. Pi is often sequestered in the soil and becomes limited for plant growth. Plants have developed a sophisticated array of adaptive responses, termed P starvation responses, to cope with P deficiency by improving its external acquisition and internal utilization. Over the past 2 to 3 decades, remarkable progress has been made toward understanding how plants sense and respond to changing environmental P. This review provides an overview of the molecular mechanisms that regulate or coordinate P starvation responses, emphasizing P transport, sensing, and signaling. We present the major players and regulators responsible for Pi uptake and translocation. We then introduce how P is perceived at the root tip, how systemic P signaling is operated, and the mechanisms by which the intracellular P status is sensed and conveyed. Additionally, the recent exciting findings about the influence of P on plant-microbe interactions are highlighted. Finally, the challenges and prospects concerning the interplay between P and other nutrients and strategies to enhance P utilization efficiency are discussed. Insights obtained from this knowledge may guide future research endeavors in sustainable agriculture.

Figure 1.

An overview of adaptive P starvation responses in plants. There are 2 major categories of adaptive PSRs. One is to enhance the acquisition of external P, including root system architecture (RSA) modification; increased Pi release via acid/enzyme secretion; elevated Pi uptake through PHT1 transporters; and facilitated interactions with beneficial microbes such as arbuscular mycorrhizal fungi. The other is to improve utilization of internal P, including increased root-to-shoot growth ratio, PHO1-mediated root-to-shoot Pi reallocation, phospholipid replacement with galacto- and sulfolipids, ATP-conserving metabolic bypasses, and regulation of vacuolar Pi storage/release by PHT5 and VPE. Created with BioRender.com.

Figure 2.

Milestones in understanding the genes involved in P transport, sensing, and signaling pathways. The genes with different roles in Pi uptake and translocation; local (root tip), systemic, and intracellular P sensing and signaling; and P-mediated plant-microbe interactions are depicted along the timeline and chronologically arranged according to the original publication dates.

Figure 3.

Subcellular localization of players in Pi uptake and translocation. Arrows indicate the direction of Pi transport. Plasma membrane-localized PHT1 and SPDT are responsible for Pi uptake. PHT2 (chloroplast), PHT3 (mitochondria), and PHT4 (the Golgi apparatus, chloroplast, and nonphotosynthetic plastid) mediate Pi import or export from the corresponding organelles. Pi influx and efflux through the tonoplast are operated by PHT5 and VPE, respectively. PHO1 protein localizes to the plasma membrane and Golgi bearing the Pi efflux activity for Pi allocation. Pi translocators (PT) localized in the inner envelope membrane of plastids transport Pi in exchange with different substrates, including triose-phosphate/phosphate translocator (TPT), phosphoenolpyruvate/phosphate translocator (PPT), glucose-6-phosphate/phosphate translocator (GPT), and pentose xylulose-5-phosphate/phosphate translocator (XPT). Coupling with proton (H⁺) or sodium (Na⁺) transport is indicated. Created with BioRender.com.

Figure 4.

Intracellular and systemic signaling and local sensing to P availability at root tips. A) During P sufficiency, the synthesis of InsP₈ is favored, which enables the interaction between SPX and PHR, suppressing PSi genes. Excess Pi in the cytosol is transported into the vacuole by PHT5. In the seeds, P is stored as InsP₆ (IP6) in the vacuole by MRP5. PHO2 and NLA promote the degradation of Pi transporters PHT1 and PHO1 via ubiquitination (ub). Upon P deficiency, InsP₈ (IP8) level is reduced. PHR is released and binds to the P1BS element as a dimer to activate PSi genes. PHF1 facilitates the targeting of PHT1 Pi transporters to plasma membranes. miR399 and miR827 repress PHO2 and NLA, respectively, to increase the abundance of PHT1 and PHO1. AT4/IPS1 transcripts can sequester miR399 to antagonize the effects of miR399. As indicated, miR399, miR827, sugar, strigolactone (SL), and cytokinin (tZ and iP) are potential systemic signals traveling via vascular tissues. B) Under P-sufficient conditions, ARSK1 is induced to phosphorylate RAPTOR1B, stabilizing the TOR1 complex and promoting root growth. Under P-deficient conditions, STOP1-ALMT1 modulates LPR1 activity, which controls Fe distribution in the root apical meristem, blocking SHR cell-to-cell movement by callose deposition. Meanwhile, the reception of CLE14 peptide activates POL/PLL1 phosphatases to inhibit root cell proliferation at transcript levels. Abbreviations: CALS, callose synthase; ROS, reactive oxygen species. Created with BioRender.com.

Figure 5.

Versatility of SPX-PHR modules in response to P status and plant-microbe interaction. The SPX-PHR module not only regulates adaptive responses to P availability A) and B), but it also regulates arbuscular mycorrhizal symbiosis C), and the responses to pathogen infection D), through controlling various sets of genes (see text for details). H in a circle represents a proton. Abbreviations: bbreviations: BAK1, BRI1-associated kinase 1; CERK1, Chitin Elicitor Receptor Kinase 1; flg22, flagellin peptide 22; FLS2, FLAGELLIN SENSING 2; MYC, Myc factor; S1P, site-one protease; SL, strigolactone; SYMRK, Symbiosis Receptor-like Kinase.