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 GRASdomain 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.

The Potassium Transporter SlHAK10 Is Involved in Mycorrhizal Potassium Uptake

“…The asterisks indicate significant differences (P , 0.05). (Bravo et al, 2017;Jiang et al, 2017Jiang et al, , 2018Keymer et al, 2017;Luginbuehl et al, 2017). The assay of fatty acid contents in the mycorrhizal roots of wild-type and slhak10 mutant plants showed no significant difference under both the K + supply conditions (Supplemental Fig.…”

To trade in the field: the molecular determinants of arbuscular mycorrhiza nutrient exchange

“…The RAM1 transcription factor has been identified as an early regulator of the mycorrhiza-specific reprogramming, activating on the one hand genes involved in the transfer of FAs to the fungus [121] and the AM-specific phosphate transporter PT4 on the other [122]. Following different strategies to screen for transcription factors that could bind the promoters of mycorrhiza-inducible genes, two very recent researches identified elements acting downstream RAM1, namely LjCBX1 in Lotus japonicus [123] and MtWRI5a in Medicago truncatula [124]. LjCBX1 binds the conserved cis-regulatory motif "CTTC" enriched in mycorrhiza-regulated genes as well as an AW-box motif present in the promoters of glycolysis and fatty acid biosynthesis genes.…”

“…Accordingly, the authors showed that LjCBX1 can activate the transcription of FA metabolic genes as well as of the L. japonicus PT4 [123]. The M. truncatula MtWRI5a transcription factor has also been shown to bind the AW-box motif present in the promoter of the fatty acid ABC transporter STR, as well as the phosphate transporter MtPT4, enhancing their expression [124]. On the contrary, hairy roots of M. truncatula wri5a mutants showed an impaired arbuscule formation [124].…”

Dysfunction in the arbuscular mycorrhizal symbiosis has consistent but small effects on the establishment of the fungal microbiota in Lotus japonicus

“…The RAM2 gene encodes a glycero‐3‐phosphate acyl transferase (Wang et al ., ) required for the synthesis of 16:0 β‐monoacylglycerols (β‐MAG) (Bravo et al ., ; Jiang et al ., ; Keymer et al ., ; Luginbuehl et al ., ). AP2 transcription factors CBX1 and WRI5a co‐regulate a divergent set of genes underlying mycorrhizal phosphate uptake and lipid biosynthesis (Jiang et al ., ; Xue et al ., ). β‐MAGs are subsequently exported to the fungus probably via half‐ABC transporters STR to maintain the symbiotic relationship (Bravo et al ., ; Jiang et al ., ; Keymer et al ., ; Luginbuehl et al ., ).…”