Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Divergent evolution of pcf/scr74 effectors in oomycetes is associated with distinct recognition patterns in solanaceous plants
    Lin, Xiao ; Wang, Shumei ; Rond, Laura de; Bertolin, Nicoletta ; Wouters, Roland H.M. ; Wouters, Doret ; Domazakis, Emmanouil ; Bitew, Mulusew Kassa ; Win, Joe ; Dong, Suomeng ; Visser, Richard G.F. ; Birch, Paul ; Kamoun, Sophien ; Vleeshouwers, Vivianne G.A.A. - \ 2020
    mBio 11 (2020)3. - ISSN 2161-2129 - p. 1 - 12.
    Apoplastic effector - MAMP - Phytophthora infestans - Potato late blight - Surface immune receptor

    Plants deploy cell surface receptors known as pattern-recognition re ceptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen Phytophthora infestans. A subclass that includes the conserved effector PcF from Phytophthora cactorum activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to P. infestans and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (GLecRK) locus in the wild potato Solanum microdontum subsp. gigantophyllum. The G-LecRK locus displays a high diversity in Solanum host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in P. infestans is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants. IMPORTANCE Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of Phytophthora small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen Phytophthora infestans and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized Phytophthora proteins are expected to contribute to disease resistance breeding in potato.

    Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition
    Gao, Chuyun ; Xu, Huawei ; Huang, Jie ; Sun, Biying ; Zhang, Fan ; Savage, Zachary ; Duggan, Cian ; Yan, Tingxiu ; Wu, Chih Hang ; Wang, Yuanchao ; Vleeshouwers, Vivianne G.A.A. ; Kamoun, Sophien ; Bozkurt, Tolga O. ; Dong, Suomeng - \ 2020
    Proceedings of the National Academy of Sciences of the United States of America 117 (2020)17. - ISSN 0027-8424 - p. 9613 - 9620.
    Chloroplast - Disease resistance - Light - NLR - Potato blight

    In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1-mediated resistance is compromised because plants produce a shorter GLYK-lacking the intact chloroplast transit peptide-that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.

    Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen
    Pais, Marina ; Yoshida, Kentaro ; Giannakopoulou, Artemis ; Pel, M. ; Cano, Liliana M. ; Oliva, Ricardo F. ; Witek, Kamil ; Lindqvist-Kreuze, Hannele ; Vleeshouwers, V.G.A.A. ; Kamoun, Sophien - \ 2018
    The Sainsbury Laboratory
    asexual reproduction - clonal lineage - Phytophthora infestans - emergent pathogen - evolution - immunity - phenotypic plasticity - expression polymorphism - structural variation - copy number variation - loss of heterozygosity
    Background Outbreaks caused by asexual lineages of fungal and oomycete pathogens are a continuing threat to crops, wild animals and natural ecosystems (Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ, Nature 484:186–194, 2012; Kupferschmidt K, Science 337:636–638, 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl MF, Thomma BP, BioEssays 36:335–345, 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Goodwin SB, Cohen BA, Fry WE, Proc Natl Acad Sci USA 91:11591–11595, 1994; Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10:e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, et al. PLoS Pathog 8:e1002940, 2012). However, the dynamics of genome evolution within these clonal lineages have not been determined. The objective of this study was to use a comparative genomics and transcriptomics approach to determine the molecular mechanisms that underpin phenotypic variation within a clonal lineage of P. infestans. Results Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by comparing strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Delgado RA, Monteros-Altamirano AR, Li Y, Visser RGF, van der Lee TAJ, Vosman B, Plant Pathol 62:1081–1088, 2013; Forbes GA, Escobar XC, Ayala CC, Revelo J, Ordonez ME, Fry BA, Doucett K, Fry WE, Phytopathology 87:375–380, 1997; Oyarzun PJ, Pozo A, Ordonez ME, Doucett K, Forbes GA, Phytopathology 88:265–271, 1998). We detected numerous examples of structural variation, nucleotide polymorphisms and loss of heterozygosity within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor. Conclusions Our findings highlight the molecular changes underpinning the exceptional genetic and phenotypic plasticity associated with host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen. We observed that the asexual P. infestans lineage EC-1 can exhibit phenotypic plasticity in the absence of apparent genetic mutations resulting in virulence on a potato carrying the Rpi-vnt1.1 gene. Such variant alleles may be epialleles that arose through epigenetic changes in the underlying genes.
    The ELR-SOBIR1 complex functions as a two-component receptor-like Kinase to mount defense against phytophthora infestans
    Domazakis, Emmanouil ; Wouters, Doret ; Visser, Richard G.F. ; Kamoun, Sophien ; Joosten, Matthieu H.A.J. ; Vleeshouwers, Vivianne G.A.A. - \ 2018
    Molecular Plant-Microbe Interactions 31 (2018)8. - ISSN 0894-0282 - p. 795 - 802.

    The ELICITIN RESPONSE protein (ELR) from Solanum microdontum can recognize INF1 elicitin of Phytophthora infestans and trigger defense responses. ELR is a receptor-like protein (RLP) that lacks a cytoplasmic signaling domain and is anticipated to require interaction with a signaling-competent receptor-like kinase. SUPPRESSOR OF BIR1-1 (SOBIR1) has been proposed as a general interactor for RLPs involved in immunity and, as such, is a potential interactor for ELR. Here, we investigate whether SOBIR1 is required for response to INF1 and resistance to P. infestans and whether it associates with ELR. Our results show that virus-induced gene silencing of SOBIR1 in Nicotiana benthamiana leads to loss of INF1-triggered cell death and increased susceptibility to P. infestans. Using genetic complementation, we found that the kinase activity of SOBIR1 is required for INF1-triggered cell death. Coimmunoprecipitation experiments showed that ELR constitutively associates with potato SOBIR1 in planta, forming a bipartite receptor complex. Upon INF1 elicitation, this ELR-SOBIR1 complex recruits SERK3 (SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3) leading to downstream signaling activation. Overall, our study shows that SOBIR1 is required for basal resistance to P. infestans and for INF1-triggered cell death and functions as an adaptor kinase for ELR.

    Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen
    Pais, Marina ; Yoshida, Kentaro ; Giannakopoulou, Artemis ; Pel, Mathieu A. ; Cano, Liliana M. ; Oliva, Ricardo F. ; Witek, Kamil ; Lindqvist-Kreuze, Hannele ; Vleeshouwers, Vivianne G.A.A. ; Kamoun, Sophien - \ 2018
    BMC Evolutionary Biology 18 (2018)1. - ISSN 1471-2148
    Asexual reproduction - Clonal lineage - Copy number variation - Emergent pathogen - Evolution - Expression polymorphism - Immunity - Loss of heterozygosity - Phenotypic plasticity - Phytophthora infestans - Structural variation

    Background: Outbreaks caused by asexual lineages of fungal and oomycete pathogens are a continuing threat to crops, wild animals and natural ecosystems (Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ, Nature 484:186-194, 2012; Kupferschmidt K, Science 337:636-638, 2012). However, the mechanisms underlying genome evolution and phenotypic plasticity in asexual eukaryotic microbes remain poorly understood (Seidl MF, Thomma BP, BioEssays 36:335-345, 2014). Ever since the 19th century Irish famine, the oomycete Phytophthora infestans has caused recurrent outbreaks on potato and tomato crops that have been primarily caused by the successive rise and migration of pandemic asexual lineages (Goodwin SB, Cohen BA, Fry WE, Proc Natl Acad Sci USA 91:11591-11595, 1994; Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10:e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, et al. PLoS Pathog 8:e1002940, 2012). However, the dynamics of genome evolution within these clonal lineages have not been determined. The objective of this study was to use a comparative genomics and transcriptomics approach to determine the molecular mechanisms that underpin phenotypic variation within a clonal lineage of P. infestans. Results: Here, we reveal patterns of genomic and gene expression variation within a P. infestans asexual lineage by comparing strains belonging to the South American EC-1 clone that has dominated Andean populations since the 1990s (Yoshida K, Burbano HA, Krause J, Thines M, Weigel D, Kamoun S, PLoS Pathog 10e1004028, 2014; Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, Lanz C, Martin FN, Kamoun S, Krause J, et al. eLife 2:e00731, 2013; Delgado RA, Monteros-Altamirano AR, Li Y, Visser RGF, van der Lee TAJ, Vosman B, Plant Pathol 62:1081-1088, 2013; Forbes GA, Escobar XC, Ayala CC, Revelo J, Ordonez ME, Fry BA, Doucett K, Fry WE, Phytopathology 87:375-380, 1997; Oyarzun PJ, Pozo A, Ordonez ME, Doucett K, Forbes GA, Phytopathology 88:265-271, 1998). We detected numerous examples of structural variation, nucleotide polymorphisms and loss of heterozygosity within the EC-1 clone. Remarkably, 17 genes are not expressed in one of the two EC-1 isolates despite apparent absence of sequence polymorphisms. Among these, silencing of an effector gene was associated with evasion of disease resistance conferred by a potato immune receptor. Conclusions: Our findings highlight the molecular changes underpinning the exceptional genetic and phenotypic plasticity associated with host adaptation in a pandemic clonal lineage of a eukaryotic plant pathogen. We observed that the asexual P. infestans lineage EC-1 can exhibit phenotypic plasticity in the absence of apparent genetic mutations resulting in virulence on a potato carrying the Rpi-vnt1.1 gene. Such variant alleles may be epialleles that arose through epigenetic changes in the underlying genes.

    NLR network mediates immunity to diverse plant pathogens
    Wu, Chih Hang ; Abd-El-Haliem, Ahmed ; Bozkurt, Tolga O. ; Belhaj, Khaoula ; Terauchi, Ryohei ; Vossen, Jack H. ; Kamoun, Sophien - \ 2017
    Proceedings of the National Academy of Sciences of the United States of America 114 (2017)30. - ISSN 0027-8424 - p. 8113 - 8118.
    Evolution - Host–microbe interactions - Immunity
    Both plants and animals rely on nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins to respond to invading pathogens and activate immune responses. An emerging concept of NLR function is that “sensor” NLR proteins are paired with “helper” NLRs to mediate immune signaling. However, our fundamental knowledge of sensor/helper NLRs in plants remains limited. In this study, we discovered a complex NLR immune network in which helper NLRs in the NRC (NLR required for cell death) family are functionally redundant but display distinct specificities toward different sensor NLRs that confer immunity to oomycetes, bacteria, viruses, nematodes, and insects. The helper NLR NRC4 is required for the function of several sensor NLRs, including Rpi-blb2, Mi-1.2, and R1, whereas NRC2 and NRC3 are required for the function of the sensor NLR Prf. Interestingly, NRC2, NRC3, and NRC4 redundantly contribute to the immunity mediated by other sensor NLRs, including Rx, Bs2, R8, and Sw5. NRC family and NRC-dependent NLRs are phylogenetically related and cluster into a well-supported superclade. Using extensive phylogenetic analysis, we discovered that the NRC superclade probably emerged over 100 Mya from an NLR pair that diversified to constitute up to one-half of the NLRs of asterids. These findings reveal a complex genetic network of NLRs and point to a link between evolutionary history and the mechanism of immune signaling. We propose that this NLR network increases the robustness of immune signaling to counteract rapidly evolving plant pathogens.
    ELR interacts with sobir1 to mount defense responses against phytophthora infestans in potato
    Domazakis, E. ; Joosten, M.H.A.J. ; Wouters, T.C.A.E. ; Kamoun, Sophien ; Visser, R.G.F. ; Vleeshouwers, V.G.A.A. - \ 2016
    - p. 165 - 165.
    Late blight, caused by the oomycete Phytophthora infestans, is the most threatening disease of potato. So far, plant breeding for late blight resistance has been focused on the introduction of cytoplasmic NLR resistance (R) genes. However, any introduced R-gene has been defeated by the pathogen rather quickly, indicating that alternative resistance mechanisms should be studied. Recently, the receptor-like protein ELR was identified in a wild potato species, Solanum microdontum (Sm). ELR confers response to elicitins, a highly conserved family of secreted effectors of Phytophthora and Pythium. It has been shown that upon INF1 elicitation, ELR forms an inducible complex with the receptor-like kinase (RLK) SERK3. In order to study whether ELR associates with potato SOBIR1, another RLK involved in immunity, co-immunoprecipitation studies were performed. We found that ELR is indeed forming a constitutive complex with SmSOBIR1. Moreover, SmSOBIR1 seems to have a stabilizing effect on ELR, leading to a higher accumulation of the receptor. Virus-induced gene silencing (VIGS) studies of SOBIR1 homologues in Nicotiana benthamiana resulted in a compromised response to INF1 of P. infestans. This response could be complemented by expressing a synthetic version of SmSOBIR1 that is not targeted by VIGS. Additionally, the same NbSOBIR1-silenced plants were more susceptible to a number of P. infestans isolates. This indicates that SOBIR1 plays an important role in plant defense against P. infestans, as shown for other pathogens. Further studies aim to demonstrate whether ELR physically associates with INF1 in a direct or indirect fashion.
    Nine things to know about elicitins
    Derevnina, Lida ; Dagdas, Yasin F. ; Concepcion, Juan Carlos De la; Bialas, Aleksandra ; Kellner, Ronny ; Petre, Benjamin ; Domazakis, Emmanouil ; Du, Juan ; Wu, Chih Hang ; Lin, Xiao ; Aguilera-Galvez, Carolina ; Cruz-Mireles, Neftaly ; Vleeshouwers, Vivianne G.A.A. ; Kamoun, Sophien - \ 2016
    New Phytologist 212 (2016)4. - ISSN 0028-646X - p. 888 - 895.
    Cell death - Elicitin response (ELR) - Elicitor - Hypersensitive response (HR) - INF1 - Microbe-associated molecular patterns (MAMPs) - Oomycetes

    Elicitins are structurally conserved extracellular proteins in Phytophthora and Pythium oomycete pathogen species. They were first described in the late 1980s as abundant proteins in Phytophthora culture filtrates that have the capacity to elicit hypersensitive (HR) cell death and disease resistance in tobacco. Later, they became well-established as having features of microbe-associated molecular patterns (MAMPs) and to elicit defences in a variety of plant species. Research on elicitins culminated in the recent cloning of the elicitin response (ELR) cell surface receptor-like protein, from the wild potato Solanum microdontum, which mediates response to a broad range of elicitins. In this review, we provide an overview on elicitins and the plant responses they elicit. We summarize the state of the art by describing what we consider to be the nine most important features of elicitin biology.

    Plant immunity switched from bacteria to virus
    Giannakopoulou, Artemis ; Bialas, Aleksandra ; Kamoun, Sophien ; Vleeshouwers, Vivianne G.A.A. - \ 2016
    Nature Biotechnology 34 (2016)4. - ISSN 1087-0156 - p. 391 - 392.
    A plant immune receptor is engineered to recognize viruses rather than bacteria.
    Meeting Report: Fungal Genomics Meets Social Media: Highlights of the 28th Fungal Genetics Conference at Asilomar
    Momany, M. ; Pietro, A. Di; Alexander, W.G. ; Barker, B.M. ; Harb, O.S. ; Kamoun, S. ; Martin, F. ; Pires, J.C. ; Stajich, J.E. ; Thomma, B.P.H.J. ; Unruh, S. - \ 2015
    G3 : Genes Genomes Genetics 5 (2015)12. - ISSN 2160-1836 - p. 2523 - 2525.
    Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora
    Sharma, R. ; Xia, X. ; Cano, L.M. ; Evangelisti, E. ; Kemen, E. ; Judelson, H. ; Oome, S. ; Sambles, C. ; Hoogen, D.J. van den; Kitner, M. ; Klein, J. ; Meijer, H.J.G. ; Spring, O. ; Win, J. ; Zipper, R. ; Bode, H.B. ; Govers, F. ; Kamoun, S. ; Schornack, S. ; Studholme, D.J. ; Ackerveken, G. van den; Thines, M. - \ 2015
    BMC Genomics 16 (2015). - ISSN 1471-2164 - 23 p.
    Background Downy mildews are the most speciose group of oomycetes and affect crops of great economic importance. So far, there is only a single deeply-sequenced downy mildew genome available, from Hyaloperonospora arabidopsidis. Further genomic resources for downy mildews are required to study their evolution, including pathogenicity effector proteins, such as RxLR effectors. Plasmopara halstedii is a devastating pathogen of sunflower and a potential pathosystem model to study downy mildews, as several Avr-genes and R-genes have been predicted and unlike Arabidopsis downy mildew, large quantities of almost contamination-free material can be obtained easily. Results Here a high-quality draft genome of Plasmopara halstedii is reported and analysed with respect to various aspects, including genome organisation, secondary metabolism, effector proteins and comparative genomics with other sequenced oomycetes. Interestingly, the present analyses revealed further variation of the RxLR motif, suggesting an important role of the conservation of the dEER-motif. Orthology analyses revealed the conservation of 28 RxLR-like core effectors among Phytophthora species. Only six putative RxLR-like effectors were shared by the two sequenced downy mildews, highlighting the fast and largely independent evolution of two of the three major downy mildew lineages. This is seemingly supported by phylogenomic results, in which downy mildews did not appear to be monophyletic. Conclusions The genome resource will be useful for developing markers for monitoring the pathogen population and might provide the basis for new approaches to fight Phytophthora and downy mildew pathogens by targeting core pathogenicity effectors.
    Functional Divergence of Two Secreted Immune Proteases of Tomato
    Ilyas, M. ; Hörger, A.C. ; Bozkurt, T.O. ; Burg, H.A. van den; Kaschani, F. ; Kaiser, M. ; Belhaj, K. ; Smoker, M. ; Joosten, M. ; Kamoun, S. ; Hoorn, R.A.L. van der - \ 2015
    Current Biology 25 (2015)17. - ISSN 0960-9822 - p. 2300 - 2306.
    cf-2-dependent disease resistance - pathogen effectors - transcription factors - provides insights - genome sequence - plant-pathogens - gene - defense - target - specialization
    Rcr3 and Pip1 are paralogous secreted papain-like proteases of tomato. Both proteases are inhibited by Avr2 from the fungal pathogen Cladosporium fulvum, but only Rcr3 acts as a co-receptor for Avr2 recognition by the tomato Cf-2 immune receptor [ 1, 2, 3 and 4]. Here, we show that Pip1-depleted tomato plants are hyper-susceptible to fungal, bacterial, and oomycete plant pathogens, demonstrating that Pip1 is an important broad-range immune protease. By contrast, in the absence of Cf-2, Rcr3 depletion does not affect fungal and bacterial infection levels but causes increased susceptibility only to the oomycete pathogen Phytophthora infestans. Rcr3 and Pip1 reside on a genetic locus that evolved over 36 million years ago. These proteins differ in surface-exposed residues outside the substrate-binding groove, and Pip1 is 5- to 10-fold more abundant than Rcr3. We propose a model in which Rcr3 and Pip1 diverged functionally upon gene duplication, possibly driven by an arms race with pathogen-derived inhibitors or by coevolution with the Cf-2 immune receptor detecting inhibitors of Rcr3, but not of Pip1.
    Evolution of Hyaloperonospora effectors: ATR1 effector homologs from sister species of the downy mildew pathogen H. arabidopsidis are not recognised by RPP1WsB
    Solovyeva, I. ; Schmuker, A. ; Cano, L.M. ; Damme, M. van; Ploch, S. ; Kamoun, S. ; Thines, M. - \ 2015
    Mycological Progress 14 (2015). - ISSN 1617-416X - 9 p.
    plant immune-system - phylogenetic-relationships - peronospora-parasitica - oomycete effector - resistance gene - proteins - sequences - thaliana - reveals - plasmopara
    Like other plant-pathogenic oomycetes, downy mildew species of the genus Hyaloperonospora manipulate their hosts by secreting effector proteins. Despite intense research efforts devoted to deciphering the virulence and avirulence activities of effectors in the H. arabidopsidis/Arabidopsis thaliana pathosystem, there is only a single study in this pathosystem on the variation of effectors and resistance genes in natural populations, and the evolution of these effectors in the context of pathogen evolution is studied even less. In this work, the identification of A rabidopsis t haliana recognised (ATR)1-homologs is reported in two sister species of H. arabidopsidis, H. thlaspeos-perfoliati, and H. crispula, which are specialized on the host plants Microthlaspi perfoliatum and Reseda lutea, respectively. ATR1-diversity within these sister species of H. arabidopsidis was evaluated, and the ATR1-homologs from different isolates of H. thlaspeos-perfoliati and H. crispula were tested to see if they would be recognised by the previously characterised RPP1-WsB protein from A. thaliana. None of the effectors from the sister species was recognised, suggesting that due to the adaptation to altered or new targets after a host jump, features of variable effectors might vary to a degree that recognition of orthologous Avr-causing effectors is no longer effective and probably does not contribute to non-host immunity.
    Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato
    Du, J. ; Verzaux, E.C. ; Chaparro-Garcia, A. ; Bijsterbosch, G. ; Keizer, L.C.P. ; Zhou, J. ; Liebrand, T.W.H. ; Xie, C. ; Govers, F. ; Robatzek, S. ; Vossen, E.A.G. van der; Jacobsen, E. ; Visser, R.G.F. ; Kamoun, S. ; Vleeshouwers, V.G.A.A. - \ 2015
    Nature Plants 1 (2015). - ISSN 2055-026X - 5 p.
    Potato late blight, caused by the destructive Irish famine pathogen Phytophthora infestans, is a major threat to global food security1,2. All late blight resistance genes identified to date belong to the coiled-coil, nucleotide-binding, leucine-rich repeat class of intracellular immune receptors3. However, virulent races of the pathogen quickly evolved to evade recognition by these cytoplasmic immune receptors4. Here we demonstrate that the receptor-like protein ELR (elicitin response) from the wild potato Solanum microdontum mediates extracellular recognition of the elicitin domain, a molecular pattern that is conserved in Phytophthora species. ELR associates with the immune co-receptor BAK1/SERK3 and mediates broad-spectrum recognition of elicitin proteins from several Phytophthora species, including four diverse elicitins from P. infestans. Transfer of ELR into cultivated potato resulted in enhanced resistance to P. infestans. Pyramiding cell surface pattern recognition receptors with intracellular immune receptors could maximize the potential of generating a broader and potentially more durable resistance to this devastating plant pathogen.

    Potato (Solanum tuberosum L.) is the most important non-grain food crop and a major source of calories for the world's poor5. Increasing potato production is critical to prevent global malnutrition and hunger in an era of expanding world population. Unfortunately, potato suffers from the devastating late blight disease, which is caused by the notorious oomycete pathogen Phytophthora infestans. To limit losses to late blight, potato breeders rely on fungicide treatment and breeding of disease resistance (R) genes, all of which identified thus far belong to the coiled-coil, nucleotide-binding, leucine-rich repeat (CC-NB-LRR) class of immune receptors. These intracellular proteins recognize pathogen avirulence (Avr) proteins of the RxLR class of effectors to mount defence responses. However, RxLR effectors display high evolutionary rates4, and as a result, P. infestans can rapidly circumvent recognition by intracellular R immune receptors, thereby limiting the development of sustainable and durable genetic resistance. Therefore, novel types of immune receptors that recognize a broader spectrum of pathogen molecules are needed.

    To fend off pathogens, plants rely on two classes of immune receptors that either reside inside the plant cell (NB-LRRs) or on the cell surface. The first line of defence is initiated by surface receptors, also called pattern recognition receptors (PRRs). PRRs are characteristically receptor-like proteins (RLPs), such as Ve1/Ve26, Cfs7,8 and LeEIX19, or receptor-like kinases (RLKs), such as FLS2, EFR and XA2110. PRRs typically recognize conserved pathogen-associated molecular patterns (PAMPs)11. So far, only a relatively few cell surface receptors against agronomically important pathogens have been identified.

    Elicitins are structurally conserved extracellular proteins in Phytophthora and Pythium pathogen species (Pfam PF00964)12,​13,​14. P. infestans contains six elicitin genes that are conserved among different strains13,15. Elicitins are recognized as oomycete PAMPs but their intrinsic function in oomycetes is to bind lipids. Some elicitins sequester sterols from plants, thereby fulfilling an important biological function in Phytophthora and Pythium species that cannot synthesize sterols12. Targeting such conserved ‘Achilles heel’ proteins of pathogens is expected to lead to a more broad-spectrum resistance.

    To identify novel types of potential immune receptors against the potato late blight pathogen, we initiated the cloning of ELR, a gene that determines response to elicitins16. We screened a collection of wild Solanum germplasm by Potato virus X (PVX) agroinfection for responses to INF1, a secreted elicitin of P. infestans (Fig. 1a). Solanum microdontum genotype mcd360-1 consistently responded to INF1 with a cell death response (Fig. 1b). We crossed mcd360-1 with S. microdontum ssp. gigantophyllum gig714-1 that does not respond to INF1. The F1 population segregated for response to INF1 in a 1:1 ratio, which suggests that ELR is a single dominant gene.
    The Top 10 oomycete pathogens in molecular plant pathology
    Kamoun, S. ; Furzer, O. ; Jones, J.D.G. ; Judelson, H.S. ; Ali, G.S. ; Dalio, R.J.D. ; Roy, S.G. ; Schena, L. ; Zambounis, A. ; Panabières, F. ; Cahill, D. ; Ruocco, M. ; Figueiredo, A. ; Chen, X.R. ; Hulvey, J. ; Stam, R. ; Lamour, K. ; Gijzen, M. ; Tyler, B.M. ; Grünwald, N.J. ; Mukhtar, M.S. ; Tomé, D.F.A. ; Tör, M. ; Ackerveken, G. van den; McDowell, J. ; Daayf, F. ; Fry, W.E. ; Lindqvist-Kreuze, H. ; Meijer, H.J.G. ; Petre, B. ; Ristaino, J. ; Yoshida, K. ; Birch, P.R.J. ; Govers, F. - \ 2015
    Molecular Plant Pathology 16 (2015)4. - ISSN 1464-6722 - p. 413 - 434.
    grapevine downy mildew - irish potato famine - sudden oak death - blister rusts albuginaceae - eastern united-states - 3 clonal lineages - nb-lrr gene - phytophthora-infestans - plasmopara-viticola - arabidopsis-thaliana
    Oomycetes form a deep lineage of eukaryotic organisms that includes a large number of plant pathogens that threaten natural and managed ecosystems. We undertook a survey to query the community for their ranking of plant pathogenic oomycete species based on scientific and economic importance. In total, we received 263 votes from 62 scientists in 15 countries for a total of 33 species. The Top 10 species and their ranking are: (1) Phytophthora infestans; (2, tied) Hyaloperonospora arabidopsidis; (2, tied) Phytophthora ramorum; (4) Phytophthora sojae; (5) Phytophthora capsici; (6) Plasmopara viticola; (7) Phytophthora cinnamomi; (8, tied) Phytophthora parasitica; (8, tied) Pythium ultimum; and (10) Albugo candida. The article provides an introduction to these 10 taxa and a snapshot of current research. We hope that the list will serve as a benchmark for future trends in oomycete research.
    Potato SOBIR1 and SOBIR1-like interact with the elicitin-response receptor (ELR) of potato and are involved in the response to INF1 elicitin of Phytophthora infestans
    Domazakis, E. ; Du, J. ; Liebrand, T.W.H. ; Chaparro-Garcia, A. ; Visser, R.G.F. ; Kamoun, S. ; Joosten, M.H.A.J. ; Vleeshouwers, V.G.A.A. - \ 2014
    In: Book of Abstracts XVI International Congress on Molecular Plant-Microbe Interactions. - - p. 117 - 117.
    P715 - Late blight, caused by the oomycete Phytophthora infestans, is the most threatening disease of potato ( Solanum tuberosum, St). So far, plant breeding for late blight resistance was focused on the introduction of resistance (R) genes, which encode cytoplasmic receptors of the NB-LRR family. However, these introduced resistances have been defeated by the pathogen rather quickly. Currently, we are investigating whether immunity that is triggered upon perception of apoplastic pathogen elicitors can enhance late blight resistance. Previous work in our group led to the identification of ELR, a pattern recognition receptor (PRR) that recognizes several elicitins, a highly conserved family of secreted effectors of Phytophthora and Pythium spp. ELR encodes a receptor-like protein (RLP) and providesbroad spectrum recognition of various elicitins in potato. Since RLPs do not have a kinase domain, they were anticipated to require a co-regulatory receptor-like kinase (RLK) that does carry a kinase domain to initiate cytoplasmic signaling. Indeed, it was recently described that several RLPs form a constitutive complex with the RLK SOBIR1. Tostudy whether ELR associates withSOBIR1, we cloned several StSOBIR1 and StSOBIR1-like homologues from wild potato accessions. We found that these genes are highly conserved in Solanum spp. and co-immunoprecipitation experiments showed that all StSOBIR1 variants physically interact with ELR. Virus-induced gene silencing (VIGS) studies of the Nicotiana benthamiana SOBIR1 homologues resulted in a compromised response to INF1 of P. infestans in N. benthamiana. Together, our results suggest that StSOBIR1 and StSOBIR1-like are involved in the INF1 response by associating with ELR.
    Effector-driven breeding for broad-spectrum disease
    Vleeshouwers, V.G.A.A. ; Du, J. ; Domazakis, E. ; Chaparro-Garcia, A. ; Lin, X. ; Dong, S. ; Wouters, D. ; Joosten, M.H.A.J. ; Kamoun, S. ; Visser, R.G.F. - \ 2014
    In: Book of Abstracts XVI International Congress on Molecular Plant-Microbe Interactions. - - p. 38 - 38.
    CS-23.6 - Potato late blight, caused by the destructive Irish famine pathogen Phytophthora infestans, is a major threat to global food security. All known late blig ht resistance genes that are identified to date belong to the NB-LRR class of immune receptors. However, virulent races of the pathogen quickly evolved to evade recognition by these intracellular cytoplasmic immune receptors. Another, yet unexploited, layer of immunity occurs at the surface of plant cells. This apoplastic immunity generally has a broader spectrum and is based on recognition of conserved proteins of pathogens. Recently we demonstrated that the receptor-like protein ELR from the wild potato Solanum microdontum mediates extracellular recognition of the elicitin domain, a molecular pat tern that is conserved in Phytophthora species. ELR mediates broad-spectrum recognition of elicitin pro teins from several Phytophthora species, including four diverse elicitins from P. infestans. Transfer of ELR to cultivated potato resulted in enhanced resistance to P. infestans. Co-immunoprecipitation studies revealed that ELR associates with the immune co-receptor BAK1/SERK3, as well as with SOBIR1/EVR. Currently we are expanding the repertoire of receptors that recognize apoplastic effectors of Phytophthora. One of our targets is the receptor of SCR74, a highly polymorphic apoplastic effector that is under diversifying selection in P. infestans. We have identified wild Solanum species that recognize SCR74, and the identification of the receptor is underway. We postulate that pyramiding diverse types of apoplastic and cytoplasmic receptors maximizes the potential of generating a broader and potentially more durable resistance to this devastating plant pathogen. infestans . We have identified wild Solanum species that recognize SCR74, and the identificati on
    Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus
    Lin, K. ; Limpens, E.H.M. ; Zhang, Z. ; Ivanov, S. ; Saunders, D.G.O. ; Mu, D. ; Pang, E. ; Cao, H. ; Cha, H. ; Lin, T. ; Zhou, Q. ; Shang, Y. ; Li, Y. ; Sharma, T.C. ; Velzen, R. van; Ruijter, N.C.A. de; Aanen, D.K. ; Win, J. ; Kamoun, S. ; Bisseling, T. ; Geurts, R. ; Huang, S.W. - \ 2014
    Plos Genetics 10 (2014)1. - ISSN 1553-7404 - 13 p.
    arbuscular mycorrhizal fungi - pathogen phytophthora-infestans - glomus-intraradices - sexual reproduction - protein families - cdna sequences - kingdom fungi - gene - identification - efficient
    Nuclei of arbuscular endomycorrhizal fungi have been described as highly diverse due to their asexual nature and absence of a single cell stage with only one nucleus. This has raised fundamental questions concerning speciation, selection and transmission of the genetic make-up to next generations. Although this concept has become textbook knowledge, it is only based on studying a few loci, including 45S rDNA. To provide a more comprehensive insight into the genetic makeup of arbuscular endomycorrhizal fungi, we applied de novo genome sequencing of individual nuclei of Rhizophagus irregularis. This revealed a surprisingly low level of polymorphism between nuclei. In contrast, within a nucleus, the 45S rDNA repeat unit turned out to be highly diverged. This finding demystifies a long-lasting hypothesis on the complex genetic makeup of arbuscular endomycorrhizal fungi. Subsequent genome assembly resulted in the first draft reference genome sequence of an arbuscular endomycorrhizal fungus. Its length is 141 Mbps, representing over 27,000 protein-coding gene models. We used the genomic sequence to reinvestigate the phylogenetic relationships of Rhizophagus irregularis with other fungal phyla. This unambiguously demonstrated that Glomeromycota are more closely related to Mucoromycotina than to its postulated sister Dikarya.
    The receptor-like protein ELR is providing a novel layer of resistance to Phytophthora infestans in potato
    Du, J. ; Verzaux, E.C. ; Bijsterbosch, G. ; Chaparro-Garcia, A. ; Jacobsen, E. ; Visser, R.G.F. ; Kamoun, S. ; Vleeshouwers, V.G.A.A. - \ 2012
    The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells
    Damme, M. van; Bozkurt, T.O. ; Cakir, C. ; Schornack, S. ; Sklenar, J. ; Jones, A.M.E. ; Kamoun, S. - \ 2012
    PLoS Pathogens 8 (2012)8. - ISSN 1553-7366
    toxoplasma-gondii - protein-kinase - iii effectors - tyrosine-phosphatase - oomycete effectors - molecular-cloning - virulence factor - rhoptry protein - innate immunity - rxlr effectors
    Phytopathogenic oomycetes, such as Phytophthora infestans, secrete an arsenal of effector proteins that modulate plant innate immunity to enable infection. We describe CRN8, a host-translocated effector of P. infestans that has kinase activity in planta. CRN8 is a modular protein of the CRN effector family. The C-terminus of CRN8 localizes to the host nucleus and triggers cell death when the protein is expressed in planta. Cell death induction by CRN8 is dependent on its localization to the plant nucleus, which requires a functional nuclear localization signal (NLS). The C-terminal sequence of CRN8 has similarity to a serine/threonine RD kinase domain. We demonstrated that CRN8 is a functional RD kinase and that its autophosphorylation is dependent on an intact catalytic site. Co-immunoprecipitation experiments revealed that CRN8 forms a dimer or multimer. Heterologous expression of CRN8 in planta resulted in enhanced virulence by P. infestans. In contrast, in planta expression of the dominant-negative CRN8 R469A; D470A resulted in reduced P. infestans infection, further implicating CRN8 in virulence. Overall, our results indicate that similar to animal parasites, plant pathogens also translocate biochemically active kinase effectors inside host cells.
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