An ectomycorrhizal fungus alters sensitivity to jasmonate, salicylate, gibberellin, and ethylene in host roots

Abstract

The phytohormones jasmonate, gibberellin, salicylate, and ethylene regulate an interconnected reprogramming network integrating root development with plant responses against microbes. The establishment of mutualistic ectomycorrhizal symbiosis requires the suppression of plant defense responses against fungi as well as the modification of root architecture and cortical cell wall properties. Here, we investigated the contribution of phytohormones and their crosstalk to the ontogenesis of ectomycorrhizae (ECM) between grey poplar (Populus tremula x alba) roots and the fungus Laccaria bicolor. To obtain the hormonal blueprint of developing ECM, we quantified the concentrations of jasmonates, gibberellins, and salicylate via liquid chromatography–tandem mass spectrometry. Subsequently, we assessed root architecture, mycorrhizal morphology, and gene expression levels (RNA sequencing) in phytohormone‐treated poplar lateral roots in the presence or absence of L. bicolor. Salicylic acid accumulated in mid‐stage ECM. Exogenous phytohormone treatment affected the fungal colonization rate and/or frequency of Hartig net formation. Colonized lateral roots displayed diminished responsiveness to jasmonate but regulated some genes, implicated in defense and cell wall remodelling, that were specifically differentially expressed after jasmonate treatment. Responses to salicylate, gibberellin, and ethylene were enhanced in ECM. The dynamics of phytohormone accumulation and response suggest that jasmonate, gibberellin, salicylate, and ethylene signalling play multifaceted roles in poplar L. bicolor ectomycorrhizal development.

Alterations in the phenylpropanoid pathway affect poplar ability for ectomycorrhizal colonisation and susceptibility to root-knot nematodes

“…Since the increase in GA signalling suggested by our transcriptomic dataset is correlated with the deficient mycorrhizal colonisation of the modified line, we may speculate that GA signalling is also negatively associated with ectomycorrhizal colonisation. This is consistent with a recent study showing that exogenous GA treatment of poplar roots impedes the ectomycorrhizal colonisation process (Basso et al 2020). DELLA proteins suppress GA signalling, as demonstrated in Medicago truncatula double della mutant (Gutjahr 2014).…”

Function and Mechanism of Jasmonic Acid in Plant Responses to Abiotic and Biotic Stresses

“…This negative crosstalk has been reported in tomato plants after an attack from mealybugs, wherein the deficiency of SA leads to activation of JA and enhancement of the plant defense response [81]. Recently, a study investigated the contributions of JA and SA to ectomycorrhizae between the roots of grey poplar and the fungus Laccaria bicolor, and reported the regulation of gene clusters by their crosstalk [82].…”

Abscisic acid supports colonization of Eucalyptus grandis roots by the mutualistic ectomycorrhizal fungus Pisolithus microcarpus

“…During this stage of the interaction, plant transcriptomic changes linked to pathways involved with immune and stress responses have been reported, as have increases in gene expression of signal receptors (Sebastiana et al ., 2009; Balestrini & Bonfante, 2014; Larsen et al ., 2015; Plett et al ., 2015b; Liao et al ., 2016). In the final stage of the interaction, during which the fungus becomes fully established within the host as determined by the presence of a Hartig net, plant nutrient transporter genes are induced and nutrient fluxes between the partner organisms can be measured (Duplessis et al ., 2005; Willmann et al ., 2014; Garcia et al ., 2015; Hortal et al ., 2017; Basso et al ., 2019; Plett et al ., 2020; Plett et al ., 2021b).…”

“…Many phytohormones are important to the development of EcM interactions, with previous research highlighting how the sensitivity to, and regulation of, plant hormones such as jasmonic acid, ethylene, and auxin affect colonization (Plett et al ., 2014; Basso et al ., 2019). In addition to these classic phytohormones, only a few studies in EcM fungi have explored the role of abscisic acid (ABA) in host interactions (Luo et al ., 2009; Calvo‐Polanco et al ., 2019; Lorente et al ., 2021) despite the finding of its crucial role in the establishment of AM fungal symbioses (Herrera‐Medina et al ., 2007; Charpentier et al ., 2014; Lou et al ., 2021).…”