Lipid transfer from plants to arbuscular mycorrhiza fungi.

Andreas Keymer,Caroline Gutjahr,Peter Dörmann,Martin Parniske,Claudia Huber,Simone L Bucerius,Pierre-Marc Delaux,Edda Von Röpenack-Lahaye,Vera Wewer,Mathias Brands,Trevor L Wang,Wolfgang Eisenreich,Priya Pimprikar,Verena Klingl

doi:10.7554/elife.29107

Abstract

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.

Highlights

Arbuscular mycorrhiza (AM) is a widespread symbiosis between most land plants and fungi of the Glomeromycota (Smith and Read, 2008)
During AM symbiosis, an array of lipid biosynthesis genes is induced in arbuscocytes (Gaude et al, 2012a, 2012b), indicating a large demand for lipids in these cells
Two genes encoding lipid biosynthesis enzymes, the thioesterase FatM and the GPAT6 REDUCED ARBUSCULAR MYCORRHIZA2 (RAM2), have previously been shown to be required for arbuscule branching in M. truncatula (Wang et al, 2012; Bravo et al, 2017; Jiang et al, 2017). Both enzymes have a substrate preference for 16:0 fatty acid (FA) (Salas and Ohlrogge, 2002; Yang et al, 2012; Bravo et al, 2017) and, consistent with this, we and others observed that colonized ram2 mutant roots over-accumulate 16:0 FA containing phospholipids and TAGs (Figure 7, [Bravo et al, 2017]), indicating re-channeling of superfluous 16:0 FAs in the absence of RAM2 function and placing RAM2 downstream of FatM (Figure 9)

Summary

Introduction

Arbuscular mycorrhiza (AM) is a widespread symbiosis between most land plants and fungi of the Glomeromycota (Smith and Read, 2008). The fungi provide mineral nutrients to the plant These nutrients are taken up from the soil and released inside root cortex cells at highly branched hyphal structures, the arbuscules (Javot et al, 2007). Arbuscular mycorrhiza fungi (AMF) develop extended extraradical hyphal networks. Their growth requires a large amount of energy and carbon building blocks, which are transported mostly as lipid droplets and glycogen to the growing hyphal tips (Bago et al, 2002, 2003). A fungal hexose transporter, with high transport activity for glucose is required for arbuscule development and quantitative root colonization as shown by host induced gene silencing (Helber et al, 2011), indicating the importance of hexose transfer for intra-radical fungal development

Methods

Results

Conclusion