Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes

Ectomycorrhizal fungi, such as Laccaria bicolor, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secre...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 22; pp. 8299 - 8304
Main Authors: Plett, Jonathan M., Daguerre, Yohann, Wittulsky, Sebastian, Vayssieres, Alice, Deveau, Aurelie, Melton, Sarah J., Kohler, Annegret, Morrell-Falvery, Jennifer L., Brun, Annick, Veneault-Fourrey, Claire, Martin, Francis
Format: Journal Article
Language:English
Published: United States National Academy of Sciences 03-06-2014
National Acad Sciences
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Summary:Ectomycorrhizal fungi, such as Laccaria bicolor, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secreted Protein 7) encoded by L. bicolor is necessary for the establishment of symbiosis with host trees, although the mechanistic reasoning behind this role was unknown. We demonstrate here that MiSSP7 interacts with the host protein PtJAZ6, a negative regulator of jasmonic acid (JA)-induced gene regulation in Populus. As with other characterized JASMONATE ZIM-DOMAIN (JAZ) proteins, PtJAZ6 interacts with PtCOI1 in the presence of the JA mimic coronatine, and PtJAZ6 is degraded in plant tissues after JA treatment. The association between MiSSP7 and PtJAZ6 is able to protect PtJAZ6 from this JA-induced degradation. Furthermore, MiSSP7 is able to block—or mitigate—the impact of JA on L. bicolor colonization of host roots. We show that the loss of MiSSP7 production by L. bicolor can be complemented by transgenically varying the transcription of PtJAZ6 or through inhibition of JA-induced gene regulation. We conclude that L. bicolor, in contrast to arbuscular mycorrhizal fungi and biotrophic pathogens, promotes mutualism by blocking JA action through the interaction of MiSSP7 with PtJAZ6.
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PMCID: PMC4050555
1J.M.P., Y.D., S.W., C.V.-F., and F.M. contributed equally to this work.
Edited by Jeffery L. Dangl, Howard Hughes Medical Institute and The University of North Carolina at Chapel Hill, Chapel Hill, NC, and approved April 8, 2014 (received for review December 8, 2013)
Author contributions: J.M.P., Y.D., S.W., A.V., A.D., J.M.-F., A.B., C.V.-F., and F.M. designed research; J.M.P., Y.D., S.W., A.V., A.D., S.J.M., A.K., J.M.-F., A.B., and C.V.-F. performed research; J.M.-F., A.B., C.V.-F., and F.M. contributed new reagents/analytic tools; J.M.P., Y.D., S.W., A.V., A.D., S.J.M., A.K., J.M.-F., A.B., C.V.-F., and F.M. analyzed data; and J.M.P., Y.D., J.M.-F., C.V.-F., and F.M. wrote the paper.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1322671111