Lipid transfer from plants to arbuscular mycorrhiza fungi

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.

DOI: http://dx.doi.org/10.7554/eLife.29107.001

eLife digest

Most land plants are able to form partnerships with certain fungi – known as arbuscular mycorrhiza fungi – that live in the soil. These fungi supply the plant with mineral nutrients, especially phosphate and nitrogen, in return for receiving carbon-based food from the plant. To exchange nutrients, the fungi grow into the roots of the plant and form highly branched structures known as arbuscules inside plant cells.

Due to the difficulties of studying this partnership, it has long been believed that plants only provide sugars to the fungus. However, it has recently been discovered that these fungi lack important genes required to make molecules known as fatty acids. Fatty acids are needed to make larger fat molecules that, among other things, store energy for the organism and form the membranes that surround each of its cells. Therefore, these results raise the possibility that the plant may provide the fungus with some of the fatty acids the fungus needs to grow.

Keymer, Pimprikar et al. studied how arbuscules form in a plant known as Lotus japonicus, a close relative of peas and beans. The experiments identified a set of mutant L. japonicus plants that had problems forming arbuscules. These plants had mutations in several genes involved in fat production that are only active in plant cells containing arbuscules.

Further experiments revealed that certain fat molecules that are found in fungi, but not plants, were present at much lower levels in samples from mutant plants colonized with the fungus, compared to samples from normal plants colonized with the fungus. This suggests that the fungi colonizing the mutant plants may be starved of fat molecules. Using a technique called stable isotope labelling it was possible to show that fatty acids made in normal plants can move into the colonizing fungus.

The findings of Keymer, Pimprikar et al. provide evidence that the plant feeds the fungus not only with sugars but also with fat molecules. The next challenge will be to find out exactly how the fat molecules are transferred from the plant cell to the fungus. Many crop plants are able to form partnerships with arbuscular mycorrhizal fungi. Therefore, a better understanding of the role of fat molecules in these relationships may help to breed crop plants that, by providing more support to their fungal partner, may grow better in the field.

DOI: http://dx.doi.org/10.7554/eLife.29107.002