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.