The beneficial effects of mycorrhizae on plant growth have often been related to the increase in the uptake of immobile nutrients, especially phosphorus (P). In this review the mechanisms for the increase in the uptake of P by mycorrhizae and the sources of soil P for mycorrhizal and non-mycorrhizal plants are examined. Various mechanisms have been suggested for the increase in the uptake of P by mycorrhizal plants. These include: exploration of larger soil volume; faster movement of P into mycorrhizal hyphae; and solubilization of soil phosphorus. Exploration of larger soil volume by mycorrhizal plants is achieved by decreasing the distance that P ions must diffuse to plant roots and by increasing the surface area for absorption. Faster movement of P into mycorrhizal hyphae is achieved by increasing the affinity for P ions and by decreasing the threshold concentration required for absorption of P. Solubilization of soil P is achieved by the release of organic acids and phosphatase enzymes. Mycorrhizal plants have been shown to increase the uptake of poorly soluble P sources, such as iron and aluminium phosphate and rock phosphates. However, studies in which the soil P has been labelled with radioactive 32P indicated that both mycorrhizal and non-mycorrhizal plants utilized the similarly labelled P sources in soil.

A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants

Many plants have the capacity to obtain phosphate via a symbiotic association with arbuscular mycorrhizal (AM) fungi. In AM associations, the fungi release phosphate from differentiated hyphae called arbuscules, that develop within the cortical cells, and the plant transports the phosphate across a symbiotic membrane, called the periarbuscular membrane, into the cortical cell. In Medicago truncatula, a model legume used widely for studies of root symbioses, it is apparent that the phosphate transporters known to operate at the root–soil interface do not participate in symbiotic phosphate transport. EST database searches with short sequence motifs shared by known phosphate transporters enabled the identification of a novel phosphate transporter from M. truncatula, MtPT4. MtPT4 is significantly different from the plant root phosphate transporters cloned to date. Complementation of yeast phosphate transport mutants indicated that MtPT4 functions as a phosphate transporter, and estimates of the Km suggest a relatively low affinity for phosphate. MtPT4 is expressed only in mycorrhizal roots, and the MtPT4 promoter directs expression exclusively in cells containing arbuscules. MtPT4 is located in the membrane fraction of mycorrhizal roots, and immunolocalization revealed that MtPT4 colocalizes with the arbuscules, consistent with a location on the periarbuscular membrane. The transport properties and spatial expression patterns of MtPT4 are consistent with a role in the acquisition of phosphate released by the fungus in the AM symbiosis.

A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi

The arbuscular mycorrhizal (AM) symbiosis is a mutualistic endosymbiosis formed by plant roots and AM fungi. Most vascular flowering plants have the ability to form these associations, which have a significant impact on plant health and consequently on ecosystem function. Nutrient exchange is a central feature of the AM symbiosis, and AM fungi obtain carbon from their plant host while assisting the plant with the acquisition of phosphorus (as phosphate) from the soil. In the AM symbiosis, the fungus delivers Pi to the root through specialized hyphae called arbuscules. The molecular mechanisms of Pi and carbon transfer in the symbiosis are largely unknown, as are the mechanisms by which the plant regulates the symbiosis in response to its nutrient status. Plants possess many classes of Pi transport proteins, including a unique clade (Pht1, subfamily I), members of which are expressed only in the AM symbiosis. Here, we show that MtPT4, a Medicago truncatula member of subfamily I, is essential for the acquisition of Pi delivered by the AM fungus. However, more significantly, MtPT4 function is critical for AM symbiosis. Loss of MtPT4 function leads to premature death of the arbuscules; the fungus is unable to proliferate within the root, and symbiosis is terminated. Thus, Pi transport is not only a benefit for the plant but is also a requirement for the AM symbiosis.

https://www.pnas.org/content/pnas/104/5/1720.full.pdf

A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis.

Summary
In this review we compare the structure and function of the interfaces between symbionts in biotrophic associations. The emphasis is on biotrophic fungal parasites and on mycorrhizas, although necrotrophic parasitic associations and the Rhizobium/legume symbiosis are mentioned briefly. We take as a starting point the observations that in the parasitic associations nutrient transport is polarized towards the parasite, whereas in mutualistic associations it is bidirectional. The structure and function of the interfaces are then compared. An important common feature is that in nearly all cases the heterotrophic symbiont (whether mutualistic or parasitic) is located topologically outside the cytoplasm of the host cells, in an apoplastic compartment. This means that nutrient movements across the interface must involve transport into and out of this apoplastic region through membranes of both organisms.

Basic principles of membrane transport in uninfected cells are briefly reviewed to set the scene for a discussion of transport mechanisms which may operate in parasitic and mycorrhizal symbioses. The presence and possible roles of ATPases associated with membranes at the interfaces are discussed. We conclude that cytochemical techniques (used to demonstrate the activity of these enzymes) need to he extended and complemented by biochemical and biophysical studies in order to confirm that the activity is due to transport ATPases. Nevertheless, the distribution of activity appears to he in accord with polarized transport mechanisms in some pathogens and with bidirectional transport in mycorrhizas. The absence of ATPases on many fungal membranes needs re-examination.

We emphasize that transport mechanisms between mycorrhizal symbionts cannot be viewed simply as the exchange of carbon for phosphate. Additional features include provision for transport of carbon and nitrogen as amino acids or amides and for ions such as K+ and H+ involved in the maintenance of charge balance and pH regulation, processes which also occur in parasitic associations. Interplant transport of nutrients via mycorrhizal hyphae is discussed in the context of these complexities. Some suggestions for the directions of future work are made.

Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport.

Publisher Summary This chapter discusses the role of mycorrhizas in the growth and nutrition of nitrogen-fixing nodulated plants. It reviews some general, well-established principles on mycorrhizal types, morphology, physiology, and function. The interactions between nodular and mycorrhizal endophytes related to the formation and effects of these dual symbioses that greatly enhance the development of the common host plant are discussed. It presents the ecological significance of plants bearing the two types of symbioses, with emphasis on the possibilities of harnessing them to increase crop yield. Mycorrhizal associations play an important role in the growth and nutrition of higher plants. It is recognized that this symbiosis can be harnessed to improve nutrient cycling and crop productivity by reducing industrial fertilizer inputs, thereby conserving and reducing environmental costs. Mycorrhizal infection can help plants to become reestablished in eroded or degraded habitats, to thrive in arid conditions, to deter pathogens, and to cope with various stress situations. The common mycorrhizal types, the vesicular-arbuscular mycorrhizas (VAM), are nearly omnipresent and are studied intensively throughout the world. VAM enhance growth, nodulation, and nitrogen fixation in grain and forage legumes, crops of the greatest interest for food production in the biosphere.

Mycorrhizas and their Significance in Nodulating Nitrogen-Fixing Plants

Summary
X-ray microanalysis has confirmed, and measured, the phosphorus content (0·03 g cm-3) of cytochemically-demonstrated polyphosphate granules in onion mycorrhizas. The volume occupied by the granules measured from stereoscopic high-voltage electron micrographs of thick sections was 0·8 % of the fungal volume, and cytoplasmic streaming rates of the extra-matrical mycelium in soil measured in the light microscope were around 12·6 cm h-1. From these data a flux rate of about 2·7 × 10-8 mol P cm-2 s-1 has been calculated, which fulfils the hypothesis that phosphorus is translocated in the fungus by means of the transport of polyphosphate granules by cytoplasmic streaming.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8137.1980.tb04778.x

Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. III. Polyphosphate granules and phosphorus translocation

SUMMARY X-ray microanalysis has confirmed, and measured, the phosphorus content (003 g cm-3) of cytochemically-demonstrated polyphosphate granules in onion mycoirhizas. The volume occupied by the granules measured from stereoscopic high-voltage electron micrographs of thick sections was 0-8 % of the fungal volume, and cytoplasmic streaming rates of the extramatrical mycelium in soil measured in the light microscope were around 12-6 cm h-1. From these data a flux rate of about 2-7 x 10-8 mol P cm-2 s-1 has been calculated, which fulfils the hypothesis that phosphorus is translocated in the fungus by means of the transport of polyphosphate granules by cytoplasmic streaming.

https://www.jstor.org/stable/info/2431918

K. J. Moran

Papers

Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. III. Polyphosphate granules and phosphorus translocation

Translocation and transfer of nutrients in vesicular-arbuscular