Host-adapted enzymatic deconstruction of acetylated xylan limits immune activation and facilitates mutualistic colonization of monocot roots

Intracellular accommodation of beneficial fungi requires host cell-wall remodeling that avoids excessive immune activation. The root endophyte Serendipita indica, a generalist mutualist capable of colonizing both monocot and dicot plants, employs a monocot-specific enzymatic module to deconstruct acetyl-xylan, the dominant hemicellulose of grasses. Central to this module are the glycoside hydrolase SiGH11, which releases acetylated xylooligosaccharides, and SiAXE, a previously uncharacterized SGNH-like acetyl-xylan esterase that sequentially removes acetyl groups from soluble xylooligosaccharides. Both enzymes are co-expressed within a monocot-enriched transcriptional program that also includes sugar transporters and metabolic regulators. Their coordinated activity, together with co-expressed exo-enzymes, promotes efficient xylan hydrolysis while limiting the prolonged accumulation of immunogenic damage-associated molecular patterns. Functional genetics demonstrated that SiAXE is required for sustained intracellular growth in monocot roots: its deletion impaired colonization, whereas overexpression transiently accelerated entry but provoked immune responses, underscoring the importance of temporal regulation and enzyme coordination for immune-compatible colonization. These findings provide mechanistic insights into an immune-compatible fungal strategy for host cell-wall remodeling and reveal how a broadly colonizing mutualist has repurposed ancestral saprotrophic enzymes into specialized host-adapted modules that balance nutrient acquisition with immune modulation.