Mol Plant. 2018 Oct 04. pii: S1674-2052(18)30301-0. [Epub ahead of print]
Most land plants evolve a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi to improve nutrient acquisition from the soil. In return, up to 20% of host plant photosynthate is transferred to the mycorrhizal fungus in the form of lipids and sugar. Nutrient exchange must be regulated by both partners in order to maintain a reliable symbiotic relationship. However, the mechanisms underlying the regulation of lipid transfer from plant to AM fungus remain elusive. Here, we show that Medicago truncatula AP2/EREBP transcription factor WRI5a, and likely its two homologs WRI5b/Erf1 and WRI5c, are master regulators of AM symbiosis by controlling lipid transfer and periarbuscular membrane formation. We found that WRI5a binds the AW-box cis-regulatory elements in the promoters of STR and MtPT4 in M. truncatula, which encodes a periarbuscular membrane-localized ABC transporter required for lipid transfer from the plant to AM fungi-and a phosphate transporter required for phosphate transfer from AM fungi to the plant, respectively. The M. truncatula wri5a mutant and RNAi composite plants hairy roots displayed impaired arbuscule formation, whereas overexpression of WRI5a resulted in enhanced expression of STR and MtPT4, suggesting that WRI5a regulates bidirectional symbiotic nutrient exchange. Moreover, we found that WRI5a and RAM1 (Required for Arbuscular Mycorrhization symbiosis 1) encoding a GRAS-domain transcription factor regulate each other at the transcriptional level, forming a positive feedback loop for regulating AM symbiosis. Our data suggest a role for WRI5a in controlling lipid transfer and periarbuscular membrane formation via the regulation of genes for the biosynthesis and supply of fatty acids and phosphate uptake in arbuscule-containing cells.
Keywords: AW-box; Mycorrhizal symbiosis; lipid transfer; transcription factor