Adenylate cyclase Mac1 functions as a cutin monomer receptor to drive appressorium development and infection in Magnaporthe oryzae

The rice blast fungus Magnaporthe oryzae senses plant surface cues, such as cutin monomers, to initiate appressorium formation. Although cutin monomers are known to trigger the cAMP–protein kinase A signaling pathway, their fungal receptor has remained unknown. Here, we identify the adenylate cyclase Mac1 as a direct receptor for cutin monomers in M. oryzae . A 32-amino acid segment (residues 424 to 455) in Mac1’s N terminus is specifically required for its binding to and activation by cutin monomers. Strikingly, Mac1’s subcellular localization dictates its functional response to cutin monomers: when anchored to late endosomes, Mac1 promotes appressorium maturation in a cutin monomer–dependent manner; in contrast, cytosolic Mac1 is inhibited by the same ligand, leading to reduced cAMP accumulation and failed appressorium maturation. We show that both the appressorium-specific membrane protein Pams1 and high intracellular turgor are required for stable Mac1 anchoring to late endosomes. Our findings reveal a spatial regulatory mechanism whereby a single chemical signal elicits opposing cellular responses depending on receptor localization during appressorium development in M. oryzae . This work resolves a long-standing question in M. oryzae –plant interactions, establishes a molecular framework for how this pathogen decodes host-derived chemical signals, and advances our mechanistic understanding of fungal pathogenesis.