Prospects of genetics and breeding for low-phosphate tolerance: an integrated approach from soil to cell

Abstract

Improving phosphorus (P) crop nutrition has emerged as a key factor toward achieving a more resilient and sustainable agriculture. P is an essential nutrient for plant development and reproduction, and phosphate (Pi)-based fertilizers represent one of the pillars that sustain food production systems. To meet the global food demand, the challenge for modern agriculture is to increase food production and improve food quality in a sustainable way by significantly optimizing Pi fertilizer use efficiency. The development of genetically improved crops with higher Pi uptake and Pi-use efficiency and higher adaptability to environments with low-Pi availability will play a crucial role toward this end. In this review, we summarize the current understanding of Pi nutrition and the regulation of Pi-starvation responses in plants, and provide new perspectives on how to harness the ample repertoire of genetic mechanisms behind these adaptive responses for crop improvement. We discuss on the potential of implementing more integrative, versatile, and effective strategies by incorporating systems biology approaches and tools such as genome editing and synthetic biology. These strategies will be invaluable for producing high-yielding crops that require reduced Pi fertilizer inputs and to develop a more sustainable global agriculture.

Fig. 1

Paths toward phosphorus (P) and food security. Science-driven strategies should be implemented to be able to produce enough food to feed the growing population for the coming years. These strategies include for instance: substantial improvement of agricultural practices (i.e., fertile land and water use), development and improvement of technologies for P recycling from agricultural and industrial wastewater, deployment of symbionts, and improvement of crops traits. Improvement of plant P uptake and utilization plays a crucial role toward P and food security. Some elements in this figure were created with BioRender

Fig. 2

Current phosphorus (P) fertilization practices are largely inefficient and determined by several factors besides the P fertilizer amount applied to soil. Heatmap illustrating a the size of the effect that the listed factors can have in limiting the variance of above-ground crop production; b the effect that P fertilization can have in increasing aboveground plant production in function of the properties of the cropland (aridity, climate zone, soil weathering) and the P fertilization regime (amount and fertilizer type); and c P use efficiency in common cereals. P fertilizer use efficiency for grain (left) is calculated as follows: (P content in grain with P fertilization—P content in grain without P fertilization)/P fertilizer amount applied × 100%. P fertilizer use efficiency for above-ground mass production (right) was calculated as follows (P content in aboveground biomass with P fertilizer—P content in aboveground biomass without P fertilizer)/P fertilizer amount × 100%. a, b Heatmaps are based on the data published by Hou et al. (2020). The heatmap presented in (c) is based on the data published by Yu et al. (2021). Heat maps were prepared using ComplexHeatmap R package (Gu et al. 2016b)

Fig. 3

Regulons controlling plant phosphate (Pi) homeostasis. Schematic summary of a cis-NAT mediated control of Pi translocation; b miRNA-mediated control of PHO2 transcript levels; and c ubiquitin-mediated turnover of Pi-transporter proteins in plants. Explanation and discovery of the regulons for Arabidopsis and crops is presented throughout the text

Fig. 4

Control of plant phosphate (Pi) homeostasis by inositol (IP)-signaling and IP-sensing domains. a Schematic representation of SPX-domain regulation on plant PHR transcription factors. See main text for complete explanation. Because SPX-domains are IP-sensing domains conserved among eukaryotes (Wild et al. 2016), the crystal structure of IP₆-bound SPX domain from the fungi Chaetomium thermophilum is presented as an example. b Representation of IP synthesis in plants. Dual phosphatase/pyrophosphate kinases AtVIH1 and AtVIH2 phosphorylate InsP₇ to produce InsP₈ and dephosphorylate InsP₇ to InsP₆. It is currently unknown which enzyme catalyzes the formation of InsP₇. AtIPK1 and AtITPK1 kinases catalyze, respectively, the subsequent phosphorylation of IP₄ to IP₅ and to further IP₆

Fig. 5

Local phosphate (Pi) sensing in the Arabidopsis root tip. a STOP1 accumulates in response to root tip contact with low Pi/Fe ratio and pH < 6; it regulates its own turnover via activation of RAE1/RAH1. MEDIATOR subunit MED16 promotes the STOP1-activation of ALMT1 expression under low-Pi conditions. b STOP1 activates ALMT1 expression which results in the increase of malate exudation to the root apoplast contributing to Pi solubilization, Al chelation, and Fe accumulation/remobilization in the root apical meristem. STOP1-ALMT1 and PDR2-LPR1 modules are essential and cooperate independently for this phenomenon. The tonoplast transporter complex ALS3/STAR1 is involved in the negative regulation of Fe accumulation. MPK6 kinase negatively regulates meristem maintenance in response to the low Pi/Fe ratio. Fe remobilization activates CLE14 expression which leads to the downregulation of meristem maintenance pathways. c Schematic of Fe remobilization in the root meristem (see text for explanation)

Fig. 6

Overview of traits and strategies to develop low-phosphate (Pi) tolerance in crops. Several traits and strategies have potential to develop low Phosphorus (P) tolerant crops. These include strategies related to the deployment and engineering of plant associated microorganisms, the use of alternative P sources like phosphite (Phi), and the improvement of the plant genetics based on current knowledge of the molecular regulation of Pi starvation responses. This latter considers the fine-tuning of different traits such us Pi recycling and remobilization, phytohormones and inositol polyphosphate molecules (IP) levels and modulation of organic acids exudation. The use of the CRISPR/Cas9 technology together with more integrative synthetic biology approaches assisted by biosensor molecules could help speed up this process. Phospholipids (P-lipids), galactolipids (G-lipids), sulfolipid (S-lipids). Some elements in this figure were created with BioRender