From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association

Abstract

Phosphorus (P) is essential for plant growth and productivity. It is one of the most limiting macronutrients in soil because it is mainly present as unavailable, bound P whereas plants can only use unbound, inorganic phosphate (Pi), which is found in very low concentrations in soil solution. Some ectomycorrhizal fungi are able to release organic compounds (organic anions or phosphatases) to mobilize unavailable P. Recent studies suggest that bacteria play a major role in the mineralization of nutrients such as P through trophic relationships as they can produce specific phosphatases such as phytases to degrade phytate, the main form of soil organic P. Bacteria are also more effective than other microorganisms or plants at immobilizing free Pi. Therefore, bacterial grazing by grazers, such as nematodes, could release Pi locked in bacterial biomass. Free Pi may be taken up by ectomycorrhizal fungus by specific phosphate transporters and transferred to the plant by mechanisms that have not yet been identified. This mini-review aims to follow the phosphate pathway to understand the ecological and molecular mechanisms responsible for transfer of phosphate from the soil to the plant, to improve plant P nutrition.

Keywords: bacterial grazers; ectomycorrhizal association; phosphate; phosphate transport systems; tree P nutrition.

FIGURE 1

Role of plants and their mycorrhizal symbionts together with rhizosphere bacterial populations on the use of soil phytate. Phytate is the main pool of organic phosphorus (Po) in soil ( Turner et al., 2002) that is filled by phytate from ungerminated seeds. To be used by plants, phytate must be hydrolyzed by specialized enzymes called phytases. (A) The capacity of roots and ECM fungi to release phytases in the rhizosphere is very low (Richardson et al., 2007) whereas some bacteria have a great ability to produce phytase and to mineralize phytate (Jorquera et al., 2008a,b) for their own. This will result in bacterial P immobilization at the expense of plants and ECM fungi. (B) To improve P nutrition of plants alone or with ECM fungi, P from phytate locked in bacteria has to be released through the grazing activity of microfauna, such as bacterial grazer nematodes (Irshad et al., 2012). Black arrows: P fluxes, blue arrows: biological controls, (a) release of phytase, (b) grazing activity.

FIGURE 2

Current knowledge about phosphate transporters in ectomycorrhizal roots. In ectomycorrhizal (ECM) roots, the fungus forms extraradical hyphae and a fungal sheath outside the root (A) and the Hartig net surrounding root cells (B) hiding epidermal cells and cortical (cc) cells (C). (A) In fungal cells, the uptake of Pi occurs mostly through Pht1 phosphate transporters. To date, only HcPT1.1, HcPT2 ( Tatry et al., 2009), and BePT ( Wang et al., 2014) genes have been characterized by heterologous expression in yeasts. Genomics and transcriptomic data suggest that other transporters may play a role in phosphate uptake (e.g., HcPT1.2, LbPTs, AmPTs, TvPTs, TmPT3 (Pht2; Casieri et al., 2013). (B) In the Hartig net, fungal and plant cells have a common apoplastic space with no direct symplastic communication. It is hypothesized that the hydrolysis (a) of polyphosphate (PolyP) increases Pi concentration in the cytosol of the fungus. Up to now, the molecular mechanisms sustaining P efflux from the fungus (b) to the apoplast and P influx (c) from the apoplast to the plant cell have not been identified. It is also hypothesized that fungal P transporters may not be functioning (d). (C) In plant cells, phosphate ions enter through plant P transporters. Little is known about plant transporters responsible for Pi acquisition in ECM roots. Only phosphate transporters from Populus trichocarpa (PtPTs; Loth-Pereda et al., 2011) and Eucalyptus marginata (EmPhts; Kariman et al., 2014) have so far been identified. Transcriptomic data for Pinus pinaster (Canales et al., 2013) showed putative encoding sequences for phosphate transporters (PpPTs). Full lines indicate transport systems whose capability in phosphate transport has been verified by heterologous expression in yeast. Dotted lines indicate transport systems whose involvement in phosphate transport during mycorrhizal symbioses is suggested by genomic or transcriptomic data. ed: endodermal cells. Hc: Hebeloma cylindrosporum, Be: Boletus edulis, Tm: Tuber melanosporum, Am: Amanita muscaria, Lb: Laccaria bicolor, Tv: Tricholoma vaccinum, Pt: Populus trichocarpa, Em: Eucalyptus marginata, Pp: Pinus pinaster.