Three LysM effectors of<i>Zymoseptoria tritici</i>collectively disarm chitin-triggered plant immunity

Tian, Hui; McKenzie, Craig; Rodríguez‐Moreno, Luis; Berg, Grardy van den; Chen, Hongxin; Rudd, J. J.; Mesters, J.R.; Thomma, Bart P.H.J.

doi:10.1101/2020.06.24.169789

Cited by 7 publications

(13 citation statements)

References 48 publications

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Section: Introductionsupporting

confidence: 78%

“…Furthermore, Mg1LysM homodimers were shown to undergo ligand-induced polymerization in the presence of chitin, leading to a polymeric structure that is able to protect fungal cell walls (Sánchez-Vallet et al, 2019). Similar chitin-induced homopolymer formation was shown for Mgx1LysM (Tian et al, 2021). Suppression of chitin-triggered immunity by secreted fungal effectors that carry no other recognizable domains than LysM domains, collectively referred to as LysM effectors, has been demonstrated for various phytopathogenic fungi.…”

Section: Introductionsupporting

confidence: 56%

“…Zymoseptoria tritici, the causal agent of Septoria tritici blotch (STB) of wheat, secretes the LysM effector Mg3LysM, a close homolog of Ecp6, that similarly suppresses chitin-triggered immunity (Marshall et al, 2011). Additionally, Z. tritici secretes two effectors that comprise a single LysM only, Mg1LysM and Mgx1LysM that were both characterized to protect hyphae against hydrolysis by plant chitinases and to suppress chitin-triggered immunity in plants (Marshall et al, 2011;Tian et al, 2021). An Mg1LysM crystal structure showed that two Mg1LysM monomers form a chitin-independent homodimer via the β-sheet in the N-terminus of Mg1LysM (Sánchez-Vallet et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Fungal dual-domain LysM effectors undergo chitin-induced intermolecular, and not intramolecular, dimerization

Tian¹,

Fiorin²,

Kombrink³

et al. 2020

Preprint

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14Chitin is a polymer of β-(1,4)-linked N-acetyl-D-glucosamine (GlcNAc) and a major 15 structural component of fungal cell walls that acts as a microbe-associated molecular 16 pattern (MAMP) that can be recognized by plant cell surface-localized pattern 17 recognition receptors (PRRs) to activate a wide range of immune responses. In order to 18 deregulate chitin-induced plant immunity and successfully establish their infection, 19 many fungal pathogens secrete effector proteins with LysM domains. We previously 20 determined that two of the three LysM domains of the LysM effector Ecp6 from the 21 tomato leaf mould fungus Cladosporium fulvum cooperate to form a chitin-binding 22 groove that binds chitin with ultra-high affinity, allowing to outcompete host PRRs for 23 chitin binding. In this study, we describe functional and structural analyses aimed to 24 investigate whether LysM effectors that contain two LysM domains bind chitin through 25 intramolecular or intermolecular LysM dimerization. To this end, we focus on MoSlp1 26 from the rice blast fungus Magnaporthe oryzae, Vd2LysM from the broad host range 27 vascular wilt fungus Verticillium dahliae, and ChElp1 and ChElp2 from the Brassicaceae 28 anthracnose fungus Colletotrichum higginsianum. We show that these LysM effectors 29 bind chitin through intermolecular LysM dimerization, allowing the formation of 30 polymeric complexes that may precipitate in order to eliminate the presence of chitin 31 oligomers at infection sites to suppress activation of chitin-induced plant immunity. In 32 this manner, many fungal pathogens are able to subvert chitin-triggered immunity in 33 their plant hosts. 57 enzymes, or prevent the activation of plant immunity by fungal cell wall-derived chitin 58 oligomers (de Jonge et al., 2010; Rovenich et al., 2014; Sanchez-Vallet et al., 2015). A 59 4 well-studied fungus for which several strategies to deal with chitin-triggered immunity 60 have been characterized is Cladosporium fulvum, the fungus that causes leaf mould 61 disease of tomato. C. fulvum secretes the Ecp6 effector protein during host colonization, 62 which contains three LysMs and binds chitin oligosaccharides with ultra-high affinity, to 63 prevent the activation of chitin-induced plant immune responses (Bolton et al., 2008; de 64 Jonge et al., 2010). A crystal structure of Ecp6 revealed that two of its three LysMs 65 cooperate to form a composite chitin-binding groove that binds chitin through 66 intrachain LysM dimerization (Sanchez-Vallet et al., 2013). The genome of another host-67 specific fungus, Zymoseptoria tritici, the causal agent of Septoria tritici blotch (STB) of 68 wheat, encodes a close homolog of Ecp6 known as Mg3LysM that similarly suppresses 69 chitin-triggered immunity (Marshall et al., 2011). Additionally, the Z. tritici genome 70 encodes two secreted effectors that carry a single LysM only. Of these, Mg1LysM was 71 characterized to protect hyphae against hydrolysis by plant chitinases (Marshall et al., 72 2011). An Mg1LysM crystal structure showed tha...

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Section: Introductionsupporting

confidence: 78%

Section: Introductionsupporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Fungal dual-domain LysM effectors undergo chitin-induced intermolecular, and not intramolecular, dimerization

Tian¹,

Fiorin²,

Kombrink³

et al. 2020

Preprint

Self Cite

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“…Until very recently, the general belief was that chitin-binding effectors with a single chitinbinding module were not able to suppress chitin-triggered immunity (van Esse et al 2007;Kohler et al 2016;Sánchez-Vallet et al 2013;. The discovery of Mgx1LysM has challenged this concept by providing evidence that effectors with a single chitin-binding domain were also capable to compete with plant receptors for chitin and suppress immunity (Tian et al 2020). These findings should support further studies into the P. brassicae chitin-binding effectors PbChiB1, which has only one CBM18 module.…”

Section: Discussionmentioning

confidence: 97%

Plasmodiophora brassicaechitin-binding effectors guard and mask spores during infection

Muirhead

Pérez‐López

2020

Preprint

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Plants have a sophisticated and multilayered immune system. However, plant pathogens, helped by effector proteins, have found several strategies to evade plant immunity. For instance, the clubroot pathogen, Plasmodiophora brassicae, is able to turn the roots of the susceptible hosts into nutrient-sink galls surpassing patterns-triggered immunity (PTI) and effector-triggered immunity (ETI). Chitin, the main component of P. brassicae spores cell walls and a well-known pathogens-associated molecular pattern (PAMP), can elicit PTI but is also the target of plant chitinases and chitin deacetylases. The fact that P. brassicae does not trigger PTI during the infection of the susceptible hosts motivated a genome-wide search of genes coding for secreted chitin-related proteins. We found that P. brassicae genome encodes a large repertoire of candidate-secreted effectors containing the chitin-binding domain carbohydrate-binding module family 18 (CBM18), along with chitinases and chitin deacetylases domains. The role of such proteins in the pathogenicity of the clubroot pathogen is unknown. Here, we characterized the function of two effectors, PbChiB2 and PbChiB4, which are transcriptionally activated during the spores transition to uninucleate primary plasmodium and during the spore formation. Through co-precipitation, we found that recombinant PbChiB2 and PbChiB4 bind to the spores and to chitin oligomers in vitro. We also showed that both proteins suppress chitin-triggered activation of the immune MPK3 and MPK6 in the host Brassica napus. These findings suggest a dual role for the P. brassicae CBM18 proteins as effectors for protecting zoospores and resting spores formation and for suppressing chitin-triggered immunity during the infection.

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“…For example, the aggressive fungal pathogen grey mould Botrytis cinerea , can secrete small RNAs to silence host Arabidopsis and tomato plant genes involved in immunity (Weiberg et al ., 2013). Recently the wheat fungal pathogen Zymoseptoria tritici was shown to secrete LysM effector proteins to disarm fungal chitin‐triggered plant immunity (Tian et al ., 2021). Similar mechanisms by which fungi grow undetected in their hosts’ tissues may exist in other fungal lineages; however, just as most research into parasitic plants is focussed on weedy species, most research into fungi has been directed at pathogenic species.…”

Section: Host–parasite Communicationmentioning

confidence: 99%

Endoparasitic plants and fungi show evolutionary convergence across phylogenetic divisions

et al. 2021

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Endoparasitic plants are the most reduced flowering plants, spending most of their lives as a network of filaments within the tissues of their hosts. Despite their extraordinary life form, we know little about their biology. Research into a few species has revealed unexpected insights, such as the total loss of plastome, the reduction of the vegetative phase to a proembryonic stage, and elevated information exchange between host and parasite. To consolidate our understanding, we review life history, anatomy, and molecular genetics across the four independent lineages of endoparasitic plants. We highlight convergence across these clades and a striking trans-kingdom convergence in life history among endoparasitic plants and disparate lineages of fungi at the molecular and physiological levels. We hypothesize that parasitism of woody plants preselected for the endoparasitic life history, providing parasites a stable host environment and the necessary hydraulics to enable floral gigantism and/or high reproductive output. Finally, we propose a broader view of endoparasitic plants that connects research across disciplines, for example pollen-pistil and graft incompatibility interactions and plant associations with various fungi. We shine a light on endoparasitic plants and their hosts as under-explored ecological microcosms ripe for identifying unexpected biological processes, interactions and evolutionary convergence.

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Three LysM effectors ofZymoseptoria triticicollectively disarm chitin-triggered plant immunity

Cited by 7 publications

References 48 publications

Fungal dual-domain LysM effectors undergo chitin-induced intermolecular, and not intramolecular, dimerization

Fungal dual-domain LysM effectors undergo chitin-induced intermolecular, and not intramolecular, dimerization

Plasmodiophora brassicaechitin-binding effectors guard and mask spores during infection

Endoparasitic plants and fungi show evolutionary convergence across phylogenetic divisions

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