Lipid exchanges drove the evolution of mutualism during plant terrestrialization

Mélanie K. Rich, Nicolas Vigneron, Cyril Libourel, Jean Keller, Li Xue, Mohsen Hajheidari, Guru V. Radhakrishnan, Aurélie Le Ru, Seydina Issa, Diop Giacomo Potente, Elena Conti ,Danny Duijsings, Aurélie Batut, Pauline Le Faouder, Kyoichi Kodama, Junko Kyozuka, Erika Sallet, Guillaume Bécard, Marta Rodriguez-Franco, Thomas Ott, Justine Bertrand-Michel, Giles E. D. Oldroyd, Péter Szövényi, Marcel Bucher, Pierre-Marc Delaux*


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.