Jasmonic acid signalling is targeted by a smut fungal Tin2-fold effector

In plants, jasmonate signaling is a hub integrating environmental cues with growth and development. Due to its role in balancing defense responses against pathogens, it is a target of effector proteins from various pathogens. Here, we characterized the fungal effector protein Tue1 from the Brassicaceae smut fungus Thecaphora thlaspeos . T. thlaspeos naturally infects Arabis hirsuta but can also colonize the non-host Arabidopsis thaliana . In planta, the fungal protein Tue1 hijacks the plant importin-α dependent nuclear transporter to reach the plant nucleus. It interacts with jasmonate ZIM domain 10 (JAZ10) proteins of both A. thaliana and Ar. hirsuta . Structure-guided analysis of Tue1 suggests that it binds the Jas motif of JAZ10 indicating a role in stabilization or binding competition with proteins like MYC3 and COI1. A subset of jasmonate-responsive genes is differentially regulated during T. thlaspeos infection, proposing a link of the Tue1 function to infection. Tue1 share structural similarity to the Tin2-fold family recently described in the corn smut Ustilago maydis . Our study therefore suggests that this structural effector family is expanded across fungal pathogens, although future studies have to reveal whether targeting JAZ-repressors is a conserved mechanism or specifically acquired as an adaptation to its perennial host.