An Integrative Systems Perspective on Plant Phosphate Research

Abstract

The case for improving crop phosphorus-use-efficiency is widely recognized. Although much is known about the molecular and regulatory mechanisms, improvements have been hampered by the extreme complexity of phosphorus (P) dynamics, which involves soil chemistry; plant-soil interactions; uptake, transport, utilization and remobilization within plants; and agricultural practices. The urgency and direction of phosphate research is also dependent upon the finite sources of P, availability of stocks to farmers and reducing environmental hazards. This work introduces integrative systems approaches as a way to represent and understand this complexity, so that meaningful links can be established between genotype, environment, crop traits and yield. It aims to provide a large set of pointers to potential genes and research practice, with a view to encouraging members of the plant-phosphate research community to adopt such approaches so that, together, we can aid efforts in global food security.

Keywords: global food security; mathematical modelling; phosphorus use efficiency; regulation of phosphate uptake; systems biology.

Figure 1

Integrated overview of phosphate starvation responses. The responses and signalling mechanisms operate at a range of scales and different locations which are depicted in nine connected panels: (a) denotes the whole plant and field scale; the numbers in red circles represent normal and low inorganic phosphate conditions (1) phosphorus playing a major role in various plant growth and developmental process including photosynthesis; (2) the highest level of Pi being found in the vegetative parts of the young plant, which upon maturation, moves into (3) fruit and seeds; (4) root development correlating with Pi levels; (5) Pi helping to increase water use efficiency and disease resistance; (6) abnormal leaf discolouration under low Pi conditions; and (7) shallow root system with more root hairs and lateral roots. (b) denotes the whole plant scale with systemic signals Systemic Shoot to Root (SSR) from shoot through the phloem to the root and Systemic Root to Shoot SRS) from the root to the shoot through the xylem; Pi, and water and other nutrients also go up to the shoot by this route. (c) denotes cells from any part of the plant which respond to phosphate deprivation altering the lipid content, releasing phosphate stores from the vacuole where Pi is liberated from esters by Acid Phosphatases (APase). (d) denotes the epigenetic effects (principally chromatin modification) that influence transcription of Phosphate Starvation Response genes. (e) denotes the pyrophosphate-dependent glycolytic bypass enzymes and metabolic Pi recycling system. (f) denotes rhizosphere activities, specifically the exudation of acid phosphatases (P-ases), Strigalactones (SLs) and Low Molecular Weight Organic Acids (LMWOA) which stimulate bacterial activity and attract Arbuscular Mycorrhizal Fungi (AMF) that form arbuscular structures within the root – mycorrhizal delivery of Pi is depicted in red. (g) denotes a close-up view of the rhizosphere boundaries between the root, soil sheath (SS), microbes and soil where exudates and sugars (Glu–glucose, Suc–sucrose and Fru–fructose) are secreted through efflux transporters respectively to solubilise Pi compounds and stimulate bacteria to do the same, l and Pi is imported through transporters of varying affinity; the exudates/sugars, transporters and Pi are respectively depicted by hollow ellipses, lozenges with directional arrows and black circles. (h) denotes the alteration in meristem and elongation zone length and the formation of root hairs. (i) denotes a cross section through a root and the paths taken during Pi uptake: the positions of different tissues within a root, namely, epidermis, exodermis, schlerenchyma plus cortex, endodermis, pericycle, phloem, cambium and xylem are marked respectively by red, blue, green, pink, yellow, orange, pale brown and purple; and transport of shoot-to-root signal molecules, symplastic/inter-organellar Pi and apoplastic Pi are depicted respectively by red, blue and dashed yellow arrows.

Figure 2

Molecular signalling in phosphate starvation responses. The different responses are specified in the grey bands, with hormonal regulation and transcription factor/signal/enzyme regulation delineated respectively below and above; the upstream signal and regulators are denoted in red and blue depending on whether or not they feature one or more times in the network, with some in green and purple boxes respectively to denote shoot-to-root and root-to-shoot systemic signals; the types of edges (interactions) and meaning of the acronyms are shown in the key on the lower left.