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. We demonstrate that Tue1 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. This is further supported by reduced jasmonate levels 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 that was recently described in the corn smut Ustilago maydis. Our study further demonstrates that this structural effector family is expanded across smut fungal species, although future studies have to reveal whether targeting JAZ-repressors is a conserved mechanism or specifically acquired as an adaptation to its perennial host.
Gul et al. (Wed,) studied this question.