Lipid exchanges drove the evolution of mutualism during plant terrestrialization

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.

A roadmap of plant membrane transporters in arbuscular mycorrhizal and legume–rhizobium symbioses

“…To sum up, it is widely speculated that RAM1, FatM, RAM2, and STR/STR2 form an AM-specific operational unit for lipid biosynthesis and transport in arbusculated cells ( Bravo et al, 2017 ; Jiang et al, 2017 ; Keymer et al, 2017 ; Luginbuehl and Oldroyd, 2017 ; Rich et al, 2017 ). Additionally, AP2-Domain Transcription Factor WRI5 and CBX1 from M. truncatula and L. japonicus , respectively, as well as conserved WRINKLED (WRI) transcription factor from the liverwort Marchantia paleacea , have been shown to be regulators of lipid metabolism during AMS ( Jiang et al, 2018 ; Xue et al, 2018 ; Rich et al, 2021 ). Moreover, it is conceivable that other ABCG proteins, besides STR/STR2, may also be involved in this scenario.…”

Stimulation of Hyphal Ramification and Sporulation in Funneliformis mosseae by Root Extracts Is Host Phosphorous Status-Dependent

“…Although these compounds could promote the asymbiotic growth of AM fungi, there is no evidence that these stimulators could stimulate AM fungal sporulation and help fulfill their life cycles in vitro. Recently, the fatty acid auxotrophy of AM fungi was supported by studies showing that lipids synthesized by host plants are transferred to fungal symbionts and parasites, and that these fungi lack genes encoding cytosolic fatty acid synthases [9][10][11]. Kameoka et al [12] and Sugiura et al [13] assessed the effects of several fatty acids and lipids on the asymbiotic growth of AM fungi, trying to identify the fatty acids that promote AM fungal biomass production.…”

Fungal Metagenome of Chernevaya Taiga Soils: Taxonomic Composition, Differential Abundance and Factors Related to Plant Gigantism

“…Forming intraradical hyphae, the AM increases the uptake of nutrients and facilitates the transfer of phosphorus and nitrogen to the plant under limiting conditions [8,9]. This highly evolved symbiosis was established in the early ancestors of land plants, and likely played a role in land colonization [10,11]. It was shown that the AM fungi and beneficial saprophytic mycoflora are capable of promoting plant growth [12], and there is a relationship between the AM and the synthesis of phytohormones [13].…”