Ethylene and jasmonic acid act as negative modulators during mutualistic symbiosis between Laccaria bicolor and Populus roots

Abstract

SummaryThe plant hormones ethylene, jasmonic acid and salicylic acid have interconnecting roles during the response of plant tissues to mutualistic and pathogenic symbionts.We used morphological studies of transgenic-or hormone-treated Populus roots as well as whole-genome oligoarrays to examine how these hormones affect root colonization by the mutualistic ectomycorrhizal fungus Laccaria bicolor S238N.We found that genes regulated by ethylene, jasmonic acid and salicylic acid were regulated in the late stages of the interaction between L. bicolor and poplar. Both ethylene and jasmonic acid treatments were found to impede fungal colonization of roots, and this effect was correlated to an increase in the expression of certain transcription factors (e.g. ETHYLENE RESPONSE FACTOR1) and a decrease in the expression of genes associated with microbial perception and cell wall modification. Further, we found that ethylene and jasmonic acid showed extensive transcriptional cross-talk, cross-talk that was opposed by salicylic acid signaling.We conclude that ethylene and jasmonic acid pathways are induced late in the colonization of root tissues in order to limit fungal growth within roots. This induction is probably an adaptive response by the plant such that its growth and vigor are not compromised by the fungus.

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

“…More recently, we made the observation that mutualistic ECM fungi are distinct from other biotrophic organisms in that JA inhibits their proliferation within root tissues (19). This finding is consistent with the earlier demonstration that colonization by another ECM fungus, Paxillus involutus, results in accumulation of the JA antagonist SA in root tissues and a decrease in JA biosynthesis (31).…”

“…by the hyphae of biotrophic fungi, is inhibited by increased levels of JA (19). How the ECM fungus is able to aggressively colonize plant tissues and not be repulsed by plant defenses controlled by JA and other plant hormones is not well understood.…”

“…Because MiSSP7 is able to reduce JA-induced degradation of PtJAZ6 and partly repress JA-induced gene transcription (Fig. 3), we wished to determine if MiSSP7 application could block the previously described inhibitory effect of JA on L. bicolor Hartig net development (19). The inhibition of Hartig net formation induced by exogenous MeJA is dose-dependent, with lower concentrations of MeJA (10 −14 M) having no significant effect on the establishment of the Hartig net and concentrations higher than 10 −12 M significantly inhibiting Hartig net formation (Fig.…”

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

“…Recently, JA signalling has been shown to be induced in late stages of ectomycorrhiza formation to limit, together with ET, intraradical fungal growth. Moreover, exogenous JA or ET application did not affect the early interaction events (mantle formation), but they affected the later stages, inhibiting the development of the Hartig net (Plett et al 2014a). …”

Ethylene: traffic controller on hormonal crossroads to defense

“…In contrast, activation of ET signaling is essential in the initial stages of colonization of barley (Hordeum vulgare) roots by the mutualistic fungus Piriformospora indica (Khatabi et al, 2012). In the interaction between Populus trichocarpa and the ectomycorrhizal fungus Laccaria bicolor, ET acts together with JA in constraining fungal growth, possibly to maintain an economic balance between costs and benefits in this mutualistic plant-fungus interaction (Plett et al, 2014).…”