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 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.
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;Hawkesbury Institute for the Environment, University of Western Sydney, Richmond 2753, NSW, Australia; and.
Jonathan M
JM
Plett
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Yohann
Y
Daguerre
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Sebastian
S
Wittulsky
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Alice
A
Vayssières
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Aurelie
A
Deveau
Biological and Nanoscale Systems, BioSciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6445.
Sarah J
SJ
Melton
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Annegret
A
Kohler
Biological and Nanoscale Systems, BioSciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831-6445.
Jennifer L
JL
Morrell-Falvey
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Annick
A
Brun
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France;
Claire
C
Veneault-Fourrey
Laboratoire d'Excellence Advanced Research on the Biology of Tree and Forest Ecosystems, Unité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Lorraine "Interactions Arbres/Micro-organismes," Champenoux 54180, France; fmartin@nancy.inra.fr.
Francis
F
Martin
D029681:Arabidopsis Proteins / Q000235:genetics; D003517:Cyclopentanes / Q000378:metabolism*; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D018506:Gene Expression Regulation, Plant; D055399:Laccaria / Q000235:genetics / Q000378:metabolism*; D038821:Mycorrhizae / Q000378:metabolism*; D054883:Oxylipins / Q000378:metabolism*; D010802:Phylogeny; D010937:Plant Growth Regulators / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D018517:Plant Roots / Q000378:metabolism* / Q000382:microbiology; D032107:Populus / Q000235:genetics* / Q000276:immunology / Q000378:metabolism; D012097:Repressor Proteins / Q000235:genetics / Q000378:metabolism; D013559:Symbiosis / Q000502:physiology
D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D005656:Fungal Proteins; C554742:JAZ6 protein, Arabidopsis; D054883:Oxylipins; D010937:Plant Growth Regulators; D010940:Plant Proteins; D012097:Repressor Proteins; C011006:jasmonic acid
defense; ectomycorrhizal fungus; host immunity; plant hormone; tree nutrition