Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes
Jonathan M. Plett, Yohann Daguerre, Sebastian Wittulsky, Alice Vayssiéres, Aurelie Deveau, Sarah J. Melton, Annegret Kohler, Jennifer L. Morell-Falvey, Annick Brun, Claire Veneault-Fourrey, and Francis Martin
2014 May 20, Proceedings of the National Academy of Sciences, USA 111(22): 8299-8304; doi:10.1073/pnas.1322671111
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.
Jonathan M. Plett, Yohann Daguerre, Sebastian Wittulsky, Alice Vayssières, Aurelie Deveau, Sarah J. Melton, Annegret Kohler, Jennifer L. Morrell-Falvey, Annick Brun, Claire Veneault-Fourrey, and Francis Martin. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes PNAS 2014 ; published ahead of print May 20, 2014, doi:10.1073/pnas.1322671111
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession nos. GSE56865, GSE56863, GSE56864, and GSE53475).