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

Tian Zeng, Luis Rodriguez-Moreno, Artem Mansurkhodzaev, Peng Wang, Willy van den Berg, Virginie Gasciolli, Sylvain Cottaz, Sébastien Fort, Bart P.H.J. Thomma, Jean Jacques Bono, Ton Bisseling, Erik Limpens*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

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.

Original languageEnglish
Pages (from-to)448-460
JournalNew Phytologist
Volume225
Issue number1
DOIs
Publication statusPublished - Jan 2020

Fingerprint

Chitin
Symbiosis
chitin
symbiosis
Immunity
immunity
Fungi
mycorrhizal fungi
immune response
Cell Wall
Medicago truncatula
chitooligosaccharides
Medicago
Chitinases
gene induction
Mycelium
Gene Silencing
cell wall components
gene silencing
Cellular Structures

Keywords

  • arbuscular mycorrhiza
  • chitin
  • effector
  • LysM
  • plant immunity
  • symbiosis

Cite this

Zeng, Tian ; Rodriguez-Moreno, Luis ; Mansurkhodzaev, Artem ; Wang, Peng ; van den Berg, Willy ; Gasciolli, Virginie ; Cottaz, Sylvain ; Fort, Sébastien ; Thomma, Bart P.H.J. ; Bono, Jean Jacques ; Bisseling, Ton ; Limpens, Erik. / A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. In: New Phytologist. 2020 ; Vol. 225, No. 1. pp. 448-460.
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abstract = "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.",
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A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. / Zeng, Tian; Rodriguez-Moreno, Luis; Mansurkhodzaev, Artem; Wang, Peng; van den Berg, Willy; Gasciolli, Virginie; Cottaz, Sylvain; Fort, Sébastien; Thomma, Bart P.H.J.; Bono, Jean Jacques; Bisseling, Ton; Limpens, Erik.

In: New Phytologist, Vol. 225, No. 1, 01.2020, p. 448-460.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Zeng, Tian

AU - Rodriguez-Moreno, Luis

AU - Mansurkhodzaev, Artem

AU - Wang, Peng

AU - van den Berg, Willy

AU - Gasciolli, Virginie

AU - Cottaz, Sylvain

AU - Fort, Sébastien

AU - Thomma, Bart P.H.J.

AU - Bono, Jean Jacques

AU - Bisseling, Ton

AU - Limpens, Erik

PY - 2020/1

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N2 - 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.

AB - 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.

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