Recent insights into the metabolic adaptations of phosphorus-deprived plants

Abstract

Orthophosphate (H2PO4 −, Pi) is an essential macronutrient required for many fundamental processes in plants, including photosynthesis and respiration, as well as nucleic acid, protein, and membrane phospholipid synthesis. The immense use of Pi-containing fertilizers in agriculture demonstrates how the soluble Pi levels of most soils are suboptimal for crop growth. The aim of this review is to explore recent and exciting advances concerning our understanding of adaptive metabolic processes that plants have evolved to alleviate the negative impact of nutritional Pi deficiency. Plant Pi starvation responses arise from complex signaling pathways that integrate altered gene expression with post-transcriptional and post-translational mechanisms. The resultant remodeling of the transcriptome, proteome, and metabolome enhances the efficiency of root Pi acquisition from the soil, as well as the use of assimilated Pi throughout the plant. We emphasize how the upregulation of high affinity Pi transporters and intra- and extracellular Pi scavenging and recycling enzymes, organic acid anion efflux, membrane remodeling, and the remarkable flexibility of plant metabolism and bioenergetics contribute to the survival of Pi-deficient plants. This research field is enabling development of a broad range of innovative and promising strategies for engineering P-efficient crops. Such cultivars are urgently needed to reduce inputs of unsustainable and nonrenewable Pi fertilizers for maximum agronomic benefit, and long-term global food security and ecosystem preservation.

Phosphate and phosphite have a differential impact on the proteome and phosphoproteome of Arabidopsis suspension cell cultures

“…We also employed immunoblotting using phosphorylation site-specific antibodies (anti-pSer11) to monitor the phosphorylation status of phosphoenolpyruvate carboxylase (PEPC) (Tripodi et al, 2005). This is a tightly regulated enzyme situated at a key branch point of cytosolic glycolysis, and it plays important roles in the metabolic adaptations of ÀPi plants (Dissanayaka et al, 2020;Gregory et al, 2009;Plaxton and Tran, 2011). The anti-pSer11 antibodies detect the well-characterized and highly conserved N-terminal seryl phosphorylation site of plant-type PEPCs (PTPC), which when present is a specific indicator of PTPC activation (Tripodi et al, 2005).…”

“…Plants deprived of Pi also upregulate a suite of hydrolytic enzymes to scavenge Pi from extra-and intracellular Pi esters (Tran et al, 2010a). These include lipases that facilitate the plastidial production of galacto-and sulfolipids for cell-wide replacement of membrane phospholipids (Dissanayaka et al, 2020). Correspondingly, we observed significant downregulation of NON-SPECIFIC PHOSPHOLIPASE C3 (NPC3; AT3G03520) (+Pi, À0.78 log 2 FC; +Phi, À0.66 log 2 FC) and PHOSPHOLIPASE 2 (PLC2; AT3G08510) (+Pi, À2.33 log 2 FC; +Phi, À1.35 log 2 FC) in both +Pi and +Phi conditions.…”

“…During prolonged Pi stress, depletion of vacuolar Pi pools leads to a marked reduction in the cytoplasmic concentrations of Pi and organic P metabolites, including nucleotide Ps such as ATP and ADP (Dissanayaka et al, 2020). This decline is believed to restrict the activity of several enzymes in classical glycolysis and mitochondrial respiration that are dependent on ATP, ADP and/or Pi as co-substrates.…”

“…In plants, numerous studies have indicated extensive protein phosphorylation across multiple tissues, organs and developmental stages (Uhrig et al, 2019;Mergner et al, 2020) as well as in response to nutrient stress (Engelsberger and Schulze, 2012;Duan et al, 2013;Li et al, 2014;Menz et al, 2016;Yang et al, 2019;Saito and Uozumi, 2020). As protein phosphorylation is integral to plant cell functionality, deciphering the dynamics of protein phosphorylation under Pi-limiting versus Pi-replete conditions is essential to understanding how gene expression and metabolism are controlled during plant acclimation to Pi-deficient soils, in addition to the key signaling events that convey changes in Pi nutritional status (Dissanayaka et al, 2020). Furthermore, due to the dependence of protein kinase signaling on Pi through ATP availability, studying how Pi nutrition affects protein phosphorylation could potentially delineate essential versus non-essential signaling events when plants respond to nutrient stress.…”

“…Although these adaptations are by no means identical in all plants, certain aspects are conserved in a broad variety of species from diverse environments. The PSR arises from coordinated changes in gene and protein expression, along with various post-translational controls, that lead to reprioritization of internal Pi use while enhancing external Pi acquisition (Dissanayaka et al, 2020). For example, Pi deficiency results in altered root phenotypes (e.g.…”