A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis

Abstract

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 P i 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 P i 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 P i 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.biotrophic ͉ membrane ͉ mineral nutrition ͉ mutualism ͉ root P lants and their arbuscular mycorrhizal (AM) fungal symbionts have coexisted for Ͼ400 million years (1), and the association is widespread in terrestrial ecosystems. AM symbiosis provides multiple benefits for the plant, not only enhanced phosphorus and nitrogen nutrition but also tolerance to pathogens and abiotic stresses (2, 3). For AM fungi, formation of a symbiosis is an obligate requirement. Their large spores contain reserves sufficient to support growth of a hyphal germ tube, but they must form an association with a plant to acquire additional carbon to complete their life cycle (4). Development of symbiosis, in particular intraradical development of the fungus in the root cortex, is reduced if P i availability is high (5-7). This suggests that the plant has a mechanism of regulating fungal growth, presumably to avoid the unnecessary allocation of carbon resources. The molecular basis is unknown but could occur by the control of carbon allocation (8).In the AM symbiosis, the fungal hyphae grow through the intercellular spaces of the root and subsequently invade the inner cortical cells, developing branched hyphae, called arbuscules, within the cells (9, 10). As each arbuscule forms, the plant cell envelops it in a membrane, the periarbuscular membrane, and the result is an extensive plant-fungal interface specialized for nutrient exchange (11)(12)(13)(14). It is predicted that P i and carbon transfer occur at the arbuscule/cortical cell interface, although direct evidence for carbon transfer at this location is lacking (14). Current data suggest that P i is translocated through the ...

Regulation of plants' phosphate uptake in common mycorrhizal networks: Role of intraradical fungal phosphate transporters

“…6 Remarkably, these mycorrhiza-induced phosphate transporters have been found to be crucial for mycorrhizal Pi acquisition in several studies using mutants with reduced or inhibited mycorrhiza-inducible transporter gene expression. 7,8 In order to study the mycorrhiza-induced Pht1 genes in flax and sorghum, we characterized and analyzed the expression of Pi transporters of the Pht1 family in both plant species, and identified a set of mycorrhiza-inducible Pi transporters in both plants. 4 Although mycorrhizal Pi acquisition was strongly affected by AMF species in our model system, a corresponding change in the expression of mycorrhiza-inducible Pht1 transporters was only marginally detected.…”

Live-Cell Imaging Reveals Periarbuscular Membrane Domains and Organelle Location in Medicago truncatula Roots during Arbuscular Mycorrhizal Symbiosis

“…At a functional level, the AM symbiosis is characterized by nutrient exchange, primarily phosphate and nitrogen, from obligate biotrophic fungi of the phylum Glomeromycota to the plant and reciprocal carbon transfer from the plant to the fungus (Parniske, 2008;Smith and Read, 2008). The ecological importance of the AM symbiosis is illustrated by its ancient origin, estimated at 460 million years ago and coincident with plant colonization of land (Remy et al, 1994;Redeker et al, 2000;Bonfante and Genre, 2008), its evolutionary conservation in approximately 80% of land plant species, and experimental data showing the prominent role of the symbiosis in nutrient uptake and improvement in plant health (Smith et al, 2003;Javot et al, 2007;Liu et al, 2007;Smith and Read, 2008).…”

A Mycorrhizal-Specific Ammonium Transporter from Lotus japonicus Acquires Nitrogen Released by Arbuscular Mycorrhizal Fungi

“…On the other hand, plants are endowed with Pi transporters that are mycorrhizal specific: their role is to acquire the Pi from the interfacial apoplast and to deliver it to the plant cytoplasm. A Medicago truncatula Pi transporter, described as exclusively expressed during AM symbiosis and located in the periarbuscular membrane (Harrison et al, 2002), is not only essential for the acquisition of the Pi delivered by the AM fungus, but also is required to maintain arbuscules and sustain development of the AM fungus (Javot et al, 2007a).…”