Transcriptomics reveal a mechanism of niche defense: two beneficial root endophytes deploy an antimicrobial GH18-CBM5 chitinase to protect their hosts

Eichfeld, Ruben; Mahdi, Lisa K.; De Quattro, Concetta; Armbruster, Laura; Endeshaw, Asmamaw B.; Miyauchi, Shingo; Hellmann, Margareta J.; Cord‐Landwehr, Stefan; Peterson, Daniel; Singan, Vasanth; Lail, Kathleen; Savage, Emily; Ng, Vivian; Grigoriev, Igor V.; Langen, Gregor; Moerschbacher, Bruno M.; Zuccaro, Alga

Abstract

Effector secretion is crucial for root endophytes to establish and protect their ecological niche. We used time-resolved transcriptomics to monitor effector gene expression dynamics in two closely related Sebacinales, Serendipita indica and Serendipita vermifera, during symbiosis with three plant species, competition with the phytopathogenic fungus Bipolaris sorokiniana, and cooperation with root-associated bacteria. We observed increased effector gene expression in response to biotic interactions, particularly with plants, indicating their importance in host colonization. Some effectors responded to both plants and microbes, suggesting dual roles in intermicrobial competition and plant– microbe interactions. A subset of putative antimicrobial effectors, including a GH18-CBM5 chitinase, was induced exclusively by microbes. Functional analyses of this chitinase revealed its antimicrobial and plant-protective properties. We conclude that dynamic effector gene expression underpins the ability of Sebacinales to thrive in diverse ecological niches with a single fungal chitinase contributing substantially to niche defense.