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

Abstract

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.ectomycorrhizal fungus | defense | tree nutrition | host immunity | plant hormone

Defense Related Phytohormones Regulation in Arbuscular Mycorrhizal Symbioses Depends on the Partner Genotypes

“…This finding suggests a lessor control by the plant over R. irregularis colonization that may be related to the fungal ability to suppress or evade the plant defense response, thus achieving a higher root invasion (Campos-Soriano et al 2010). Indeed, it has been reported that R. irregularis can deliver the effector protein SP7, which attenuates the plant immune response that enables the accommodation of the fungus within plant roots (Kloppholz et al 2011), as it occurs in ectomycorrhizas (Plett et al 2014b). How conserved and efficient this mechanism is in other AMF remains to be determined.…”

Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

“…An improved understanding of the ability of ECM fungi to decompose lignocellulose is needed to resolve mechanisms of nutrient cycling in forests. The ECM lifestyle in Laccaria bicolor is associated with the expression of new mycorrhizainduced small secreted proteins (MiSSPs) that are required for establishment of symbiosis 11,12 . Mycorrhizal symbioses have arisen repeatedly during fungal evolution and include not only ECM associations but also those with ERM and ORM mycorrhizae 13 .…”

“…In L. bicolor, symbiosis requires lineage-specific genes encoding small secreted effector proteins that control host-plant development and immunity 4,11,12 . By sequencing RNA from free-living mycelia and mycorrhizal roots, we identified genes regulated by symbiosis development in the ECM A. muscaria, H. cylindrosporum, P. involutus, Piloderma croceum and Suillus luteus, the ERM O. maius and the ORM S. vermifera and T. calospora.…”

“…25 and 26). To assess whether previously uncharacterized but highly induced genes may represent candidates for secreted effector proteins (CSEPs), we assessed which and how many of these genes encode proteins that possess properties (for example, predicted signal peptide, size <300 amino acid residues and no sequence similarity) common to known secreted effectors, such as mycorrhiza-induced small secreted protein of 7 kDa (MiSSP7) 11,12 . Of the induced genes, 8-28% encode proteins with a predicted signal peptide, a significantly higher fraction than the 3-7% of noninduced and non-symbiosis-related genes that encode a protein with a signal peptide (P = 2.04 × 10 −6 to <2.20 × 10 −16 , Fisher's exact test; Fig.…”

Host target modification as a strategy to counter pathogen hijacking of the jasmonate hormone receptor

“…In fact, some strains of the hemibiotrophic bacterial pathogen Pseudomonas syringae have evolved an ability to produce a potent JA-mimicking phytotoxin, coronatine (COR), to activate JA signaling as an effective means of inhibiting SA defense and promote plant susceptibility (4,26,28,29). Furthermore, CORlike compounds are produced by pathogens of other taxa (30,31) and proteinaceous effectors from both bacterial and fungal pathogens have been shown to target the COI1-JAZ coreceptor (32)(33)(34). These recent findings suggest that the COI1-JAZ coreceptor is a common target of manipulation by diverse plant pathogens and represents a prominent vulnerable point of the plant immune network.…”