The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins

Ma, Lay-Sun; Wang, Lei; Trippel, Christine; Mendoza‐Mendoza, Artemio; Ullmann, Steffen; Moretti, Marino; Carsten, Alexander; Kahnt, Joerg; Reißmann, Stefanie; Zechmann, Bernd; Bange, Gert; Kahmann, Regine

doi:10.1038/s41467-018-04149-0

Cited by 113 publications

(162 citation statements)

References 62 publications

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“…The physiological ligands of ddCRRSP, CRKs and PDLPs remain to be discovered and our work suggests that different tandem DUF26 domains likely recognize diverse sets of ligands. Similar to plant malectin receptors 62 , DUF26 domains may have evolved novel or additional functions which might include mediation of protein-protein interactions at the cell surface 20,35 . The strong structural similarity between DUF26 domains and fungal lectins suggests a common origin, and DUF26 proteins represent novel carbohydrate-binding domains in plants.…”

Section: Discussionmentioning

confidence: 99%

“…The best characterized CRRSP is Gnk2, a protein from Gingko biloba with single DUF26 which exhibits antifungal activity and acts as mannose-binding lectin in vitro 18,19 . Two maize CRRSPs have been shown to also bind mannose and participate in defence against a fungal pathogen 20 . The second class, CYSTEINE-RICH RECEPTOR-LIKE PROTEIN KINASES (CRKs), has a typical configuration of two DUF26 in the extracellular region and forms a large subgroup of RLKs in plants with 44 members encoded in the Arabidopsis thaliana genome.…”

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confidence: 99%

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Mechanistic insights into the evolution of DUF26-containing proteins in land plants

Vaattovaara

Brandt

Rajaraman

et al. 2018

Preprint

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Large protein families are a prominent feature of plant genomes and their size variation is a key element for adaptation in plants. Here we infer the evolutionary history of a representative protein family, the DOMAIN OF UNKNOWN FUNCTION (DUF) 26-containing proteins. The DUF26 first appeared in secreted proteins. Domain duplications and rearrangements led to the emergence of CYSTEINE-RICH RECEPTOR-LIKE PROTEIN KINASES (CRKs) and PLASMODESMATA-LOCALIZED PROTEINS (PDLPs). While the DUF26 itself is specific to land plants, structural analyses of Arabidopsis PDLP5 and PDLP8 ectodomains revealed strong similarity to fungal lectins. Therefore, we propose that DUF26-containing proteins constitute a novel group of plant carbohydrate-binding proteins. Following their appearance, CRKs expanded both through tandem duplications and preferential retention of duplicates in whole genome duplication events, whereas PDLPs evolved according to the dosage balance hypothesis. Based on our findings, we suggest that the main mechanism of expansion in new gene families is small-scale duplication, whereas genome fractionation and genetic drift after whole genome multiplications drive families towards dosage balance.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Mechanistic insights into the evolution of DUF26-containing proteins in land plants

Vaattovaara

Brandt

Rajaraman

et al. 2018

Preprint

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“…Alternatively, it is possible it is only cleaved in planta and not in axenic culture. While the function of SspN is not known it does have a repeat domain structure which is a common feature of several effectors characterized to date including Ecp6 from C. fulvum [107], which contains multiple LysM domain containing repeats, Sp7 from the mutualist Glomus intraradices [18], Colletotrichium graminicola EP1[108] and the recently identified effector Rsp3 from U. maydis [6]. However, unlike all these proteins, which have been shown by genetic analysis to be very important for the interaction with the host, deletion of sspN had no obvious plant interaction phenotype.…”

Section: Discussionmentioning

confidence: 99%

“…More specifically, Avr4 binds to chitin molecules present in the cell wall of invading hyphae to prevent hydrolysis by host chitinases [2, 7], while Ecp6 sequesters chitin oligosaccharides released from the cell wall of invading hyphae to prevent detection by host chitin immune receptors [4, 8]. Rsp3 binds to the cell wall of invading hyphae to protect them against two antimicrobial mannose-binding host proteins [6], while both Pit2 and Avr2 inhibit host cysteine proteases to prevent degradation of fungal proteins [3, 9-11]. A well-characterized example of an intracellular fungal effector protein is Cmu1 from U. maydis , which functions as a chorismate mutase to redirect the metabolism of chorismate away from the production of the defense signaling hormone salicylic acid [12].…”

Section: Introductionmentioning

confidence: 99%

Analysis of Epichloë festucae small secreted proteins in the interaction with Lolium perenne

Scott

Hassing

Winter

et al. 2018

Preprint

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19Epichloë festucae is an endophyte of the agriculturally important perennial 20 ryegrass. This species systemically colonises the aerial tissues of this host 21 where its growth is tightly regulated thereby maintaining a mutualistic symbiotic 42 proteins are either not required for the interaction at the observed life stages or 43 that there is redundancy between effectors expressed by E. festucae. 44 45 53 Cladosporium fulvum [2-4], as well as Pit2 and Rsp3 from the corn smut 54 pathogen Ustilago maydis [5, 6]. More specifically, Avr4 binds to chitin 55 molecules present in the cell wall of invading hyphae to prevent hydrolysis by 56 host chitinases [2, 7], while Ecp6 sequesters chitin oligosaccharides released 57 from the cell wall of invading hyphae to prevent detection by host chitin immune 58 receptors [4, 8]. Rsp3 binds to the cell wall of invading hyphae to protect them 59 against two antimicrobial mannose-binding host proteins [6], while both Pit2 60 and Avr2 inhibit host cysteine proteases to prevent degradation of fungal 61 proteins [3, 9-11]. A well-characterized example of an intracellular fungal 62 effector protein is Cmu1 from U. maydis, which functions as a chorismate 63 mutase to redirect the metabolism of chorismate away from the production of 64 the defense signaling hormone salicylic acid [12]. 4 65 Like plant-pathogenic fungi, plant-beneficial fungi must also deploy 66 effector proteins to promote host colonization [13, 14]. However, to date only a 67 small number of effectors from this group of fungi have been identified and 68 functionally characterized. Furthermore, of those that have been functionally 69 characterized all are from mycorrhizal fungi. One such example is MiSSP7 from 70 Laccaria bicolor, an ectomycorrhizal fungus of poplar roots. In plants (including 71 poplar), JAZ proteins repress the expression of jasmonic acid (JA)-related 72 defense genes, with the degradation of these proteins leading to the activation 73 of JA-related defense genes [15]. During infection of poplar, MiSSP7 is 74 transported into the plant nucleus where it interacts with and stabilizes the JAZ 75 protein PtJAZ6 to prevent its degradation, and thus prevent the expression of 76 JA defence-related genes [16, 17]. A second example is SP7, which is 77 produced by the arbuscular mycorrhizal fungus, Glomus intraradices. SP7, 78 which like PtJAZ6 is also transported into the plant nucleus, influences defense 79 gene signaling by interacting with the pathogenicity-related transcription factor 80 ERF12 [18]. A third example is Fgb1 has been characterized from the 81 endophytic root-colonizing fungus, Piriformospora indica. Fgb1 is a β-glucan-82 binding lectin that modulates the fungal cell composition and prevents β-glucan-83 triggered immunity in plants, presumably through a similar mechanism to that 84 shown for as Ecp6 and other LysM domain-containing effectors from plant-85 pathogenic fungi [19]. 86 There is little amino acid sequence conservation between effector 87 proteins of plant-associated fungi, and mo...

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“…Only a few have been characterized as effector proteins, with diverse functions during the biotrophic phase. Three apoplastic effectors, Pep1, Pit2, and Rsp3, interfere with host peroxidases, cysteine proteases, and mannose binding proteins, respectively, thereby inhibiting early immune responses of the host plant (Ma et al, 2018, Mueller et al, 2013, Hemetsberger et al, 2012. Three translocated effectors, Tin2, Cmu1, and See1, have also been characterized.…”

Section: Introductionmentioning

confidence: 99%

Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

Darino

Marques

Chia

et al. 2019

Preprint

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Ustilago maydis (U. maydis) is the causal agent of maize smut disease. During the colonization process, the fungus secretes effector proteins which suppress immune responses and redirect the hostmetabolism in favor of the pathogen. Here we describe a novel strategy by which U. maydis induces plant jasmonate/ethylene (JA/ET) hormone signaling and thereby biotrophic susceptibility. The U. maydis effector Jasmonate/Ethylene signaling inducer 1 (Jsi1) possesses an ethylene-responsive element binding factor-associated amphiphilic repression (EAR) motif, DLNxxP, which interacts with the second WD40 domain of the conserved plant co-repressor family Topless/Topless related (TPL/TPR). Jsi1 interaction with TPL/TPRs leads to derepression of the ethylene response factor (ERF) branch of the JA/ET signaling pathway, supporting biotrophic susceptibility. Jsi1 likely activates the ERF branch by interfering with the binding of endogenous DLNxxP motif-containing ERF transcription factors to TPL/TPR proteins. The identification of effector proteins possessing a DLNxxP motif in different fungal species with biotrophic and hemibiotrophic lifestyles together with the validation of the interaction between such effectors from Magnaporthe oryzae (M. oryzae), Sporisorium scitamineum (S. scitamineum), and S. reilianum with TPL proteins indicates the convergent evolution of effectors for modulating the TPL/TPR co-repressor hub.

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The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins

Cited by 113 publications

References 62 publications

Mechanistic insights into the evolution of DUF26-containing proteins in land plants

Mechanistic insights into the evolution of DUF26-containing proteins in land plants

Analysis of Epichloë festucae small secreted proteins in the interaction with Lolium perenne

Fungal effector Jsi1 hijacks plant JA/ET signaling through Topless

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