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

Jasmonate signalling integrates environmental cues with plant growth and development. Owing to its role in balancing defence 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, which naturally infects Arabis hirsuta but can also colonize Arabidopsis thaliana. In planta, Tue1 hijacks the plant importin-α-dependent nuclear transporter to reach the plant nucleus. We demonstrate that Tue1 interacts with jasmonate ZIM-domain 10 (JAZ10) proteins of both A. thaliana and A. 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 such as MYC3 and COI1. This is further supported by reduced jasmonate concentrations upon tue1 overexpression in A. thaliana and differential regulation of a subset of jasmonate-responsive genes during T. thlaspeos infection of A. hirsuta. Tue1 is part of the Tin2-fold effector family recently described in the corn smut Ustilago maydis. Our study demonstrates that this effector family is expanded across smut fungal species, although further studies are needed to reveal whether targeting JAZ repressors is a conserved mechanism or specifically acquired as an adaptation to the perennial host.