LAUSR

Significance Arbuscular mycorrhizal (AM) fungi promote phosphorus uptake into host plants in exchange for organic carbon. Physiological tracer experiments showed that up to 100% of acquired phosphate can be delivered to plants via the mycorrhizal phosphate uptake pathway (MPU). Previous studies revealed that the CTTC cis-regulatory element (CRE) is required for promoter activation of mycorrhiza-specific phosphate transporter and H+-ATPase genes. However, the precise transcriptional mechanism directly controlling MPU is unknown. Here, we show that CBX1 binds CTTC and AW-box CREs and coregulates mycorrhizal phosphate transporter and H+-ATPase genes. Interestingly, genes involved in lipid biosynthesis are also regulated by CBX1 through binding to AW box, including RAM2. Our work suggests a common regulatory mechanism underlying complex trait control of symbiotic exchange of nutrients. The arbuscular mycorrhizal (AM) symbiosis, a widespread mutualistic association between land plants and fungi, depends on reciprocal exchange of phosphorus driven by proton-coupled phosphate uptake into host plants and carbon supplied to AM fungi by host-dependent sugar and lipid biosynthesis. The molecular mechanisms and cis-regulatory modules underlying the control of phosphate uptake and de novo fatty acid synthesis in AM symbiosis are poorly understood. Here, we show that the AP2 family transcription factor CTTC MOTIF-BINDING TRANSCRIPTION FACTOR1 (CBX1), a WRINKLED1 (WRI1) homolog, directly binds the evolutionary conserved CTTC motif that is enriched in mycorrhiza-regulated genes and activates Lotus japonicus phosphate transporter 4 (LjPT4) in vivo and in vitro. Moreover, the mycorrhiza-inducible gene encoding H+-ATPase (LjHA1), implicated in energizing nutrient uptake at the symbiotic interface across the periarbuscular membrane, is coregulated with LjPT4 by CBX1. Accordingly, CBX1-defective mutants show reduced mycorrhizal colonization. Furthermore, genome-wide–binding profiles, DNA-binding studies, and heterologous expression reveal additional binding of CBX1 to AW box, the consensus DNA-binding motif for WRI1, that is enriched in promoters of glycolysis and fatty acid biosynthesis genes. We show that CBX1 activates expression of lipid metabolic genes including glycerol-3-phosphate acyltransferase RAM2 implicated in acylglycerol biosynthesis. Our finding defines the role of CBX1 as a regulator of host genes involved in phosphate uptake and lipid synthesis through binding to the CTTC/AW molecular module, and supports a model underlying bidirectional exchange of phosphorus and carbon, a fundamental trait in the mutualistic AM symbiosis.