Medicago AP2-Domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer during Mycorrhizal Symbiosis

Abstract Most land plants have evolved a mutualistic symbiosis with arbuscular mycorrhiza (AM) fungi that 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 the plant to the AM fungus remain elusive. Here, we show that the Medicago truncatula AP2/EREBP transcription factor WRI5a, and likely its two homologs WRI5b/Erf1 and WRI5c, are master regulators of AM symbiosis controlling lipid transfer and periarbuscular membrane formation. We found that WRI5a binds AW-box cis -regulatory elements in the promoters of M . truncatula STR , which encodes a periarbuscular membrane-localized ABC transporter required for lipid transfer from the plant to the AM fungus, and MtPT4 , which encodes a phosphate transporter required for phosphate transfer from the AM fungus to the plant. The hairy roots of the M . truncatula wri5a mutant and RNAi composite plants 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 ), which encodes a GRAS-domain transcription factor, regulate each other at the transcriptional level, forming a positive feedback loop for regulating AM symbiosis. Collectively, our data suggest a role for WRI5a in controlling bidirectional nutrient exchange and periarbuscular membrane formation via the regulation of genes involved in the biosynthesis of fatty acids and phosphate uptake in arbuscule-containing cells.