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Lipid exchanges drove the evolution of mutualism during plant terrestrialization

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Science  21 May 2021:
Vol. 372, Issue 6544, pp. 864-868
DOI: 10.1126/science.abg0929

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Fungal symbiosis with early land plants

Hundreds of millions of years ago, evolved descendants of aquatic plants began showing up on dry land. These newly terrestrialized species had to deal with increased ultraviolet light exposure, desiccation, and less accessible nutrients. Rich et al. show how mutualist fungi may have helped these nascent plant lineages with adaptation to their newly challenging environment (see the Perspective by Bouwmeester). Genetic and metabolic analysis of a liverwort as a representative of such plants suggests that the mutually beneficial exchange of nutrients with arbuscular mycorrhizal fungi may have been a feature of these most early land plants.

Science, abg0929, this issue p. 864; see also abi8016, p. 789

Abstract

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.

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