A lysin motif effector subverts chitin‐triggered immunity to facilitate arbuscular mycorrhizal symbiosis

Abstract

Summary Arbuscular mycorrhizal (AM) fungi greatly improve mineral uptake by host plants in nutrient‐depleted soil and can intracellularly colonize root cortex cells in the vast majority of higher plants. However, AM fungi possess common fungal cell wall components such as chitin that can be recognized by plant chitin receptors to trigger immune responses, raising the question as to how AM fungi effectively evade chitin‐triggered immune responses during symbiosis.In this study, we characterize a secreted lysin motif (LysM) effector identified from the model AM fungal species Rhizophagus irregularis, called RiSLM.RiSLM is one of the highest expressed effector proteins in intraradical mycelium during the symbiosis. In vitro binding assays show that RiSLM binds chitin‐oligosaccharides and can protect fungal cell walls from chitinases. Moreover, RiSLM efficiently interferes with chitin‐triggered immune responses, such as defence gene induction and reactive oxygen species production in Medicago truncatula. Although RiSLM also binds to symbiotic (lipo)chitooligosaccharides it does not interfere significantly with symbiotic signalling in Medicago. Host‐induced gene silencing of RiSLM greatly reduces fungal colonization levels.Taken together, our results reveal a key role for AM fungal LysM effectors to subvert chitin‐triggered immunity in symbiosis, pointing to a common role for LysM effectors in both symbiotic and pathogenic fungi.

A secreted LysM effector protects fungal hyphae through chitin-dependent homodimer polymerization

“…Recently, it was demonstrated that the arbuscular mycorrhizal (AM) fungus Rhizophagus irregularis secretes the LysM effector RiSLM to facilitate its mutualistic symbiosis [39]. Interestingly, like Mg1LysM, RiSLM was shown to be composed of a single LysM only, and furthermore to protect hyphae against hydrolysis by chitinases.…”

“…Also this phenomenon was not observed for Ecp6. Intriguingly, the recently characterized LysM effector RiSLM from the mutualistic fungus Rhizophagus irregularis [39] that, like Mg1LysM, is composed of a single LysM only and protects hyphae against chitinases also showed the ability to polymerize in a chitin-dependent manner, suggesting that polymerization of into oligomeric super-complexes in the fungal cell wall is a common phenomenon among LysM effectors that protect fungal hyphae. Possibly, it is such contiguous structure that provides steric hindrance that renders fungal cell wall chitin inaccessible to chitinase enzymes.…”

“…Native proteins were finally dialysed against 50 mM NaH 2 PO 4 , 300 mM NaCl at pH 8.0, concentrated to 0.6 mg/mL over Amicon ultracentrifugal filter units (Sigma-Aldrich, St. Louis, MO, USA) and used for subsequent assays. RiSLM was produced as described previously [39].…”

Exogenous Melatonin Application Enhances Rhizophagus irregularis Symbiosis and Induces the Antioxidant Response of Medicago truncatula Under Lead Stress

“…Gene-specific primers for four melatonin synthesis genes, MtPT4, and MtP5CS were designed as described in Supplementary Table S1. The M. truncatula elongation factor 1-alpha gene (MtEF-1α, DQ282611.1) was used as an internal control (Jiang et al, 2018;Zeng et al, 2020). qRT-PCR was performed based on SYBR Green PCR and MIQE guidelines.…”

Functional and structural characterization of LysM proteins in interactions between fungi and plants

“…Interestingly, homologs of the LysM effector Ecp6 from various fungal pathogens were found to similarly suppress chitin-triggered immunity in their hosts, including LysM effectors of the wheat pathogen Zymoseptoria tritici (Marshall et al, 2011), the rice blast fungus Magnaporthe oryzae (Mentlak et al, 2012), the Brassicaceae antracnose fungus Colletotrichum higginsianum , and the broad host range vascular wilt fungus Verticillium dahliae (Kombrink et al, 2017). However, not only fungal pathogens employ LysM effectors to suppress host immunity, as the mutualistic fungus Rhizophagus irregularis was shown to secrete the LysM effector RiSLM to facilitate the establishment of arbuscular mycorrhizal symbiosis (Zeng et al, 2020).…”