Summary During arbuscular mycorrhizal symbiosis (AMS), considerable amounts of lipids are generated, modified and moved within the cell to accommodate the fungus in the root, and it has also been suggested that lipids are delivered to the fungus. To determine the mechanisms by which root cells redirect lipid biosynthesis during AMS we analyzed the roles of two lipid biosynthetic enzymes (FatM and RAM2) and an ABC transporter (STR) that are required for symbiosis and conserved uniquely in plants that engage in AMS. Complementation analyses indicated that the biochemical function of FatM overlaps with that of other Fat thioesterases, in particular FatB. The essential role of FatM in AMS was a consequence of timing and magnitude of its expression. Lipid profiles of fatm and ram2 suggested that FatM increases the outflow of 16:0 fatty acids from the plastid, for subsequent use by RAM2 to produce 16:0 β‐monoacylglycerol. Thus, during AMS, high‐level, specific expression of key lipid biosynthetic enzymes located in the plastid and the endoplasmic reticulum enables the root cell to fine‐tune lipid biosynthesis to increase the production of β‐monoacylglycerols. We propose a model in which β‐monoacylglycerols, or a derivative thereof, are exported out of the root cell across the periarbuscular membrane for ultimate use by the fungus.

SUMMARYArbuscular mycorrhiza formation with fungi of the Glomeromycota represents a widespread symbiotic interaction of vascular plants. Different signaling events and metabolic adaptations are required for the close interaction between the two partners. Membrane lipid synthesis is a prerequisite for symbiosis, and membrane properties depend on lipid composition. Lipid profiling was performed by liquid chromatography mass spectrometry to study the role of triacylglycerol, diacylglycerol, phospholipids, galactolipids, sterols and sphingolipids during the colonization of Lotus japonicus roots with Rhizophagus irregularis (syn. Glomus intraradices). Mycorrhization leads to an increased phosphate supply and suppresses the increase in galactolipids commonly observed in phosphate-deprived plants. In addition to free sterols and sterol esters, R. irregularis contains sterol glucosides and acylated sterol glucosides. Glycosylated sphingolipids (glucosylceramide, dihexosylceramide) and inositolphosphorylceramide were detected in the fungus. Lysophosphatidylcholine, a lipid previously implicated in mycorrhiza signaling, is present in low amounts in mock-infected and mycorrhized roots. The composition of fungal phospholipids changes after mycorrhization because molecular species with palmitvaccenic (di-16:1) or tetracosenoic (24:1) acyl groups decrease in intraradical mycelium. This adaptation of lipid metabolism during intraradical growth is likely a prerequisite for symbiosis, achieving functional compatibility between the fungal and the periarbuscular membrane. Data mining in genomic and transcript databases revealed the presence of genes encoding enzymes of lipid biosynthesis in R. irregularis. However, no gene encoding multidomain fatty acid de novo synthase was detected in the genome sequence of this obligate biotrophic fungus.

Arbuscular mycorrhiza (AM) symbioses contribute to global carbon cycles as plant hosts divert up to 20% of photosynthate to the obligate biotrophic fungi. Previous studies suggested carbohydrates as the only form of carbon transferred to the fungi. However, de novo fatty acid (FA) synthesis has not been observed in AM fungi in absence of the plant. In a forward genetic approach, we identified two Lotus japonicus mutants defective in AM-specific paralogs of lipid biosynthesis genes (KASI and GPAT6). These mutants perturb fungal development and accumulation of emblematic fungal 16:1ω5 FAs. Using isotopolog profiling we demonstrate that 13C patterns of fungal FAs recapitulate those of wild-type hosts, indicating cross-kingdom lipid transfer from plants to fungi. This transfer of labelled FAs was not observed for the AM-specific lipid biosynthesis mutants. Thus, growth and development of beneficial AM fungi is not only fueled by sugars but depends on lipid transfer from plant hosts.DOI: http://dx.doi.org/10.7554/eLife.29107.001

Arbuscular mycorrhiza (AM) symbioses contribute to global carbon cycles as plant hosts divert up to 20% of photosynthate to the obligate biotrophic fungi. Previous studies suggested carbohydrates as the only form of carbon transferred to the fungi.However, de novo fatty acid (FA) synthesis has not been observed in AM fungi in absence of the plant. In a forward genetic approach, we identified two Lotus japonicus mutants defective in AM-specific paralogs of lipid biosynthesis genes (KASI and GPAT6). These mutants perturb fungal development and accumulation of emblematic fungal 16:1ω5 FAs. Using isotopolog profiling we demonstrate that 13 C patterns of fungal FAs recapitulate those of wild-type hosts, indicating cross-kingdom lipid transfer from plants to fungi. This transfer of labelled FAs was not observed for the AM-specific lipid biosynthesis mutants. Thus, growth and development of beneficial AM fungi is not only fueled by sugars but depends on lipid transfer from plant hosts.

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