Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter?

Abstract

Most plants entertain mutualistic interactions known as arbuscular mycorrhiza (AM) with soil fungi (Glomeromycota) which provide them with mineral nutrients in exchange for reduced carbon from the plant. Mycorrhizal roots represent strong carbon sinks in which hexoses are transferred from the plant host to the fungus. However, most of the carbon in AM fungi is stored in the form of lipids. The absence of the type I fatty acid synthase (FAS-I) complex from the AM fungal model species Rhizophagus irregularis suggests that lipids may also have a role in nutrition of the fungal partner. This hypothesis is supported by the concerted induction of host genes involved in lipid metabolism. We explore the possible roles of lipids in the light of recent literature on AM symbiosis. Carbohydrates in AM Fungal NutritionAM fungi are strictly biotrophic, in other words they depend on their host to complete their life cycle. Although the basis of biotrophy is poorly understood, it has been suggested that it is due to the dependency of AM fungi on some essential nutritional factor(s) from the host [1]. Direct uptake measurements revealed that intraradical mycelium (IRM) can take up carbohydrates, whereas extraradical mycelium (ERM) did not acquire significant amounts of carbohydrates [2,3]. Perhaps this is because AM fungal genes involved in nutrient uptake are expressed only in the host, which would explain their biotrophy. Tracer studies on mycorrhizal roots, and respirometric analysis on isolated intraradical hyphae have established glucose as a central substrate for AM fungi [3][4][5], and indeed a monosaccharide transporter has been identified in the fungal partner [6]. Mycorrhizal roots represent strong carbon sinks [2,4,7], suggesting that they attract sucrose from photosynthetic source tissues. Sucrose is thought to be cleaved in the vicinity of the fungus by invertases and sucrose synthase [8], resulting in monosaccharides (glucose and fructose) that are released to the fungus and taken up by its IRM [5,6]. However, in the fungal storage compartments -the spores and the vesicles -carbon is stored primarily in the form of lipids, with minor amounts of the glucose polymer glycogen. We discuss here salient issues relating to carbohydrate and lipid metabolism in AM fungi and their significance for fungal nutrition during symbiosis. Lipid Metabolism in AM Fungi -Open Questions and SurprisesAlthough the aforementioned carbon fluxes in AM fungi have been firmly established, several questions remain open. AM fungi store and transport most of their carbon in the form of lipids [9][10][11][12]. However, AM fungi cannot produce the basic fatty acid (FA) palmitate (C16) in the absence of their host (as shown in two distantly related species, Rhizophagus irregularis and Gigaspora rosea), while FA elongation and desaturation can occur independently of the plant [13]. This and similar results suggested that AM fungi can only synthesize C16 in the IRM [3,13]. Taken together, the available evidence suggests that AM fungi take up sugars (...

Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis

“…We expect to see progress in the description and characterization of plant receptors for AMF signalling molecules as well as in the identification of substrates of receptors and transporters such as D14L/KAI2 and NOPE1 (Gutjahr et al, 2015;Nadal et al, 2017). Physiological and molecular investigation is needed to resolve mechanisms and regulation of nutrient transfer between the symbionts and, in particular, the flux of carbohydrates and lipids towards the fungus (Rich et al, 2017). It is becoming increasingly clear that despite their large host range, the efficiency of AMF in promoting plant performance differs strongly among fungal species and isolates, and the ability of the plant to respond to the symbiosis depends on the plant genotype.…”

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

“…The development in arbusculated cells of stromulated plastids that can connect to the PM, however, supports a close association of FA-related proteins with the plasmalemma (Fester et al 2001;Ivanov and Harrison 2014;Kumar et al 2014;Pérez-Sancho et al 2016). This development is believed to facilitate the diffusion/uptake of plant FAs by the AM fungus (Rich et al 2017). The mycorrhiza-specific enzyme FatM is localized consistently in stromulated plastids in cells containing arbuscules (Bravo et al 2017).…”

“…AM fungi notably assist the plant with the acquisition of mineral nutrients, mainly inorganic phosphate (Pi) and nitrogen (N) that are absorbed from the soil solution by the extra-radical mycelium. In turn, AM fungi are supplied with organic carbon forms essential for them to achieve their full life cycle (Gutjahr and Parniske 2013;Rich et al 2017;Luginbuehl et al 2017). As a result, AM fungi are obligate plant biotrophic microorganisms that have a global impact on plant mineral nutrition and on the carbon cycle.…”

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

“…Recently it has been shown that fatty acids are transported from the host to the fungus, likely serving as a major nutritive carbon source (Jiang et al ., ; Keymer et al ., ; Luginbuehl et al ., ). However, previously it has been shown that the host also provides sugars as carbon source, although the mechanism by which sugars are transported to the fungus is unclear (Rich et al ., ; Roth & Paszkowski, ; Wang et al ., ). Therefore, in this study we investigated the role of SWEET sugar transporters.…”