Lipid exchanges drove the evolution of mutualism during plant terrestrialization

Symbiosis with arbuscular mycorrhizal fungi (AMF) improves plant nutrition in most land plants, and its contribution to the colonization of land by plants has been hypothesized. Here, we identify a conserved transcriptomic response to AMF among land plants, including the activation of lipid metabolism. Using gain of function, we show the transfer of lipids from the liverwort Marchantia paleacea to AMF and its direct regulation by the transcription factor WRINKLED (WRI). Arbuscules, the nutrient-exchange structures, were not formed in loss-of-function wri mutants in M. paleacea, leading to aborted mutualism. Our results show the orthology of the symbiotic transfer of lipids across land plants and demonstrate that mutualism with arbuscular mycorrhizal fungi was present in the most recent ancestor of land plants 450 million years ago.

Automated summary

Symbiosis with arbuscular mycorrhizal fungi benefits plant nutrition and elicits a conserved transcriptomic response among land plants, including activation of lipid metabolism. Transfer of lipids from liverwort to AMF is regulated by the transcription factor WRINKLED, and the formation of arbuscules is essential for mutualism. The symbiotic transfer of lipids is orthologous across land plants, indicating the presence of mutualism with AMF in the most recent ancestor of land plants 450 million years ago.