Trends in Plant Science
Volume 24, Issue 9, September 2019, Pages 794-801
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Opinion
Phosphorus Transport in Mycorrhiza: How Far Are We?

https://doi.org/10.1016/j.tplants.2019.06.004Get rights and content

Highlights

  • The acquisition of phosphorus by plants is often mediated by soil microbes colonizing the roots, particularly mycorrhizal fungi.

  • Key molecular mechanisms involved in the transport of phosphorus from the soil to mycorrhizal fungi have been revealed recently. However, the release of phosphorus towards colonized roots is still understudied, even if a recent report highlighted the possible involvement of fungal H+:Pi transporters.

  • Based on a survey of fungal transport proteins, others mechanisms possibly ensuring phosphorus efflux in mycorrhizas must coexist besides H+:Pi transporters. These include the putative involvement of Pi :Na+, low-affinity inorganic phosphate, and organic phosphate transporters.

  • Unravelling the fungal phosphorus transportome will allow a better use of plant–fungus symbioses for the improvement of plant nutrition in cropping systems.

Mycorrhizal fungi considerably improve plant nutrition and help them to cope with changing environments. Particularly, these fungi express proteins to transfer inorganic phosphate (Pi) from the soil to colonized roots through symbiotic interfaces. The mechanisms involved in Pi transfer from fungal to plant cells are still largely unknown. Here, we discuss the recent progress made on the description of these mechanisms and we propose the most promising hypotheses and alternative mechanisms for this process. Specifically, we present a phylogenetic survey of candidate Pi transporters of mycorrhizal fungi that might ensure Pi unload into the symbiotic interfaces. Gathering additional knowledge on mycorrhizal Pi transport will improve the Pi-useefficiency in agroecological systems and will guide towards addressing future research challenges.

Section snippets

Phosphate Efflux in Mycorrhizal Roots: The Missing Step

The roots of most land plants fulfill an important part of their need for phosphorus (P) through the association with soil fungi, called mycorrhizal symbiosis 1., 2.. Fungal species belonging to the Mucoromycota, subphylum Glomeromycotina, Ascomycota, and Basidiomycota phyla form different types of mycorrhizas [3]. Arbuscular mycorrhizal (AM) symbiosis (see Glossary), characterized by the formation of fungal arbuscules and/or vesicles within plant cortical cells, is formed by Glomeromycotina

High-Affinity Transporters Mediate Inorganic Phosphate Efflux in Ectomycorrhizas

The simplest hypothesis to explain the fungal P delivery at the symbiotic interface is the release of free orthophosphate ions (Pi) through phosphate transporters (PT). Fungal P transport has been widely studied in baker’s yeast (Saccharomyces cerevisiae), in which two high-affinity Pi symporters have been characterized, one coupled with H+ (Pho84) [15] and one with Na+ (Pho89) [16]. Interestingly, alignment of proteins retrieved from publicly available mycorrhizal species using the sequences

Efflux of Inorganic Phosphate through H+:Pi Symporters Is Tightly Regulated by Undescribed Mechanisms

Determining whether an efflux of Pi is possible through fungal H+:Pi transporters from a thermodynamic point of view is a key question that was addressed recently in AM symbiosis 27., 28.. Indeed, computational modeling was used to simulate in silico the conditions required for Pi exchange through fungal and plant H+:Pi transporters located at the symbiotic interface of AM roots. Briefly, the authors modelized a network based on the activity of fungal and plant membrane ATPases that release

The Intriguing Case of High-Affinity Pi:Na+ Symporters

Based on recent data reporting the role of HcPT2 in ECM symbiosis [26], it is tempting to hypothesize that H+:Pi, and particularly PT2-like transporters, could be the main proteins unloading Pi into the symbiotic interface. Here, we show that all studied mycorrhizal fungi, except Sebacinales, harbor at least one ortholog of H+:Pi PT1-like transporter, whereas most Ascomycota (truffles and parented species) and Glomeromycotina species do not have a PT2-like member (Figure 1). This indicates that

Low-Affinity Transporters Could Also Mediate Inorganic Phosphate Efflux in Mycorrhiza

So far, the most studied mechanisms for Pi efflux in mycorrhizal symbiosis have focused on H+:Pi transporters. In yeast, Pi can also be transported through three low-affinity transporters, described as Na+/dicarboxylate/sulfate/Pi transporter in databases (Pho87, Pho90, Pho91)[41]. When Pho84 and Pho89 are either not expressed in yeast or degraded at high Pi, Pho87 and Pho90 are located at the plasma membrane and ensure Pi acquisition 41., 42., 43.. Pho91 is localized at the vacuolar membrane

Organic Phosphate, an Alternative Phosphorus Source in Mycorrhizas?

We assumed for decades that the form of P released to the symbiotic interface is Pi. However, most mycorrhizal species also harbor at least one ortholog of the yeast organic P transporter, ScGit1p (Figure 1). In yeast, this protein is upregulated at low P and is able to import several phospho-diesters, which are by order of preference: glycerophosphoinositol (GroPIns) ≫ glycerophosphoserine ≫ glycerol-3-phosphate ≫ glycerophosphoethanolamine ≫ glycerophosphocholine [49]. A release of GroPIns

Concluding Remarks and Future Perspectives

Although the improvement of plant P nutrition by mycorrhizal fungi was described for the first time more than 50 years ago 51., 52., critical steps in the transport of P from the soil to colonized roots are still missing. Specifically, only a handful of candidate proteins possibly involved in the release of P from fungal cells into the symbiotic interface have been reported so far in both AM and ECM fungi [53]. With our present survey of fungal P transporters putatively involved in this crucial

Acknowledgments

We would like to thank the anonymous reviewers as well as the editor for their helpful suggestions that helped us improve themanuscript. K.G. acknowledges support of the North Carolina Agriculture Research Service (NCARS) and the North Carolina Soybean Producers Association (2019-1656).

Glossary

Arbuscular mycorrhiza
symbiotic association between roots of most land plants and fungi belonging to the Mucoromycota phylum, Glomeromycotina subphylum.
Arbuscule
highly ramified fungal structure developing within plant cortical cells in arbuscular mycorrhizal symbiosis.
Ectomycorrhiza
symbiotic association between roots from trees and shrubs and fungi belonging to the Ascomycota and Basidiomycota phyla.
Ericoid mycorrhiza
symbiotic association between roots from Ericaceae plants and mycorrhizal fungi.

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