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

Abstract

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- 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.