Trichoderma swollenin activates AtABCB5-dependent auxin efflux to promote plant development

Abstract

The beneficial fungus Trichoderma enhances plant growth and stress tolerance through poorly understood mechanisms. Here, we show that Trichoderma harzianum swollenin ThSWO contributes to efficient root colonization and plant growth promotion. ThSWO traverses the plant cell wall and localizes to the plasma membrane, where it interacts with ABC transporter AtABCB5, which we establish as a bona fide auxin efflux carrier. ThSWO binding to NBD2 and R-domain faces of AtABCB5 prosmotes phosphorylation at Ser640 and Ser644, enhancing indole-3-acetic acid (IAA) efflux and triggering auxin-associated responses, including cell wall acidification, membrane potential transitions, and accelerated cytoplasmic streaming. Structure-guided substitutions at the AtABCB5-ThSWO interface differentially affected transporter binding and lateral root promotion, supporting the conclusion that host auxin transport is a primary effector target. These findings reveal a molecular mechanism by which a fungal effector co-opts host auxin transport machinery to promote plant development, with implications for microbe-assisted crop improvement.