Plants are the foundation of terrestrial ecosystems and their colonization of land was likely facilitated by mutualistic associations with arbuscular mycorrhizal fungi. Following that founding event, plant diversification has led to the emergence of a tremendous diversity of mutualistic symbioses with microorganisms, ranging from extracellular associations to the most intimate intracellular associations, where fungal or bacterial symbionts are hosted inside plant cells. Through analysis of 271 transcriptomes and 122 plant genomes, we demonstrate that the common symbiosis signalling pathway controlling the association with arbuscular mycorrhizal fungi and with nitrogen-fixing bacteria specifically co-evolved with intracellular endosymbioses, including ericoid and orchid mycorrhizae in angiosperms and ericoid-like associations of bryophytes. In contrast, species forming exclusively extracellular symbioses like ectomycorrhizae or associations with cyanobacteria have lost this signalling pathway. This work unifies intracellular symbioses, revealing conservation in their evolution across 450 million years of plant diversification.
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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