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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    The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant-pathogen interactions
    Karimi Jashni, M. ; Mehrabi, R. ; Collemare, J. ; Mesarich, C.H. ; Wit, P.J.G.M. de - \ 2015
    Frontiers in Plant Science 6 (2015). - ISSN 1664-462X - 7 p.
    cf-2-dependent disease resistance - extracellular serine-protease - l. enhances resistance - class iv chitinases - phytophthora-infestans - cladosporium-fulvum - proteolytic-enzymes - antifungal activity - gene-expression - tomato
    Upon host penetration, fungal pathogens secrete a plethora of effectors to promote disease, including proteases that degrade plant antimicrobial proteins, and protease inhibitors (PIs) that inhibit plant proteases with antimicrobial activity. Conversely, plants secrete proteases and PIs to protect themselves against pathogens or to mediate recognition of pathogen proteases and PIs, which leads to induction of defense responses. Many examples of proteases and PIs mediating effector-triggered immunity in host plants have been reported in the literature, but little is known about their role in compromising basal defense responses induced by microbe-associated molecular patterns. Recently, several reports appeared in literature on secreted fungal proteases that modify or degrade pathogenesis-related proteins, including plant chitinases or PIs that compromise their activities. This prompted us to review the recent advances on proteases and PIs involved in fungal virulence and plant defense. Proteases and PIs from plants and their fungal pathogens play an important role in the arms race between plants and pathogens, which has resulted in co-evolutionary diversification and adaptation shaping pathogen lifestyles.
    FPLC and liquid-chromatography mass spectrometry identify candidate necrosis-inducing proteins from culture filtrates of the fungal wheat pathogen Zymoseptoria tritici
    M'Barek, S. Ben; Cordewener, J.H.G. ; Tabib Ghaffary, M.S. ; Lee, T.A.J. van der; Liu, Z. ; Mirzadi Gohari, A. ; Mehrabi, R. ; America, A.H.P. ; Friesen, T.L. ; Hamza, S. ; Stergiopoulos, I. ; Wit, P.J.G.M. de; Kema, G.H.J. - \ 2015
    Fungal Genetics and Biology 79 (2015). - ISSN 1087-1845 - p. 54 - 62.
    host-selective toxins - mycosphaerella-graminicola - stagonospora-nodorum - septoria-tritici - rhynchosporium-secalis - cladosporium-fulvum - ptr toxa - hydrogen-peroxide - barley pathogen - tan spot
    Culture filtrates (CFs) of the fungal wheat pathogen Zymoseptoria tritici were assayed for necrosis-inducing activity after infiltration in leaves of various wheat cultivars. Active fractions were partially purified and characterized. The necrosis-inducing factors in CFs are proteinaceous, heat stable and their necrosis-inducing activity is temperature and light dependent. The in planta activity of CFs was tested by a time series of proteinase K (PK) co-infiltrations, which was unable to affect activity 30min after CF infiltrations. This suggests that the necrosis inducing proteins (NIPs) are either absent from the apoplast and likely actively transported into mesophyll cells or protected from the protease by association with a receptor. Alternatively, plant cell death signaling pathways might be fully engaged during the first 30min and cannot be reversed even after PK treatment. Further fractionation of the CFs with the highest necrosis-inducing activity involved fast performance liquid chromatography, SDS-PAGE and mass spectrometry. This revealed that most of the proteins present in the fractions have not been described before. The two most prominent ZtNIP encoding candidates were heterologously expressed in Pichia pastoris and subsequent infiltration assays showed their differential activity in a range of wheat cultivars.
    Proteome catalog of Zymoseptoria tritici captured during pathogenesis in wheat
    M'Barek, S. Ben; Cordewener, J.H.G. ; Lee, T.A.J. van der; America, A.H.P. ; Mirzadi Gohari, A. ; Mehrabi, R. ; Hamza, S. ; Wit, P.J.G.M. de; Kema, G.H.J. - \ 2015
    Fungal Genetics and Biology 79 (2015)June. - ISSN 1087-1845 - p. 42 - 53.
    wall-degrading enzymes - fungus mycosphaerella-graminicola - programmed cell-death - cladosporium-fulvum - septoria-tritici - plant-pathogen - magnaporthe-grisea - disease resistance - hydrogen-peroxide - blotch pathogen
    Zymoseptoria tritici is an economically important pathogen of wheat. However, the molecular basis of pathogenicity on wheat is still poorly understood. Here, we present a global survey of the proteins secreted by this fungus in the apoplast of resistant (cv. Shafir) and susceptible (cv. Obelisk) wheat cultivars after inoculation with reference Z. tritici strain IPO323. The fungal proteins present in apoplastic fluids were analyzed by gel electrophoresis and by data-independent acquisition liquid chromatography/mass spectrometry (LC/MS(E)) combined with data-dependent acquisition LC-MS/MS. Subsequent mapping mass spectrometry-derived peptide sequence data against the genome sequence of strain IPO323 identified 665 peptides in the MS(E) and 93 in the LC-MS/MS mode that matched to 85 proteins. The identified fungal proteins, including cell-wall degrading enzymes and proteases, might function in pathogenicity, but the functions of many remain unknown. Most fungal proteins accumulated in cv. Obelisk at the onset of necrotrophy. This inventory provides an excellent basis for future detailed studies on the role of these genes and their encoded proteins during pathogenesis in wheat
    Filamentous pathogen effector functions: of pathogens, hosts and microbiomes
    Rövenich, H. ; Boshoven, J.C. ; Thomma, B. - \ 2014
    Current Opinion in Plant Biology 20 (2014). - ISSN 1369-5266 - p. 96 - 103.
    chitin-triggered immunity - secreted fungal effector - potato famine pathogen - cladosporium-fulvum - protease inhibitor - magnaporthe-oryzae - plant-pathogens - genome evolution - tomato - virulence
    Microorganisms play essential roles in almost every environment on earth. For instance, microbes decompose organic material, or establish symbiotic relationships that range from pathogenic to mutualistic. Symbiotic relationships have been particularly well studied for microbial plant pathogens and have emphasized the role of effectors; secreted molecules that support host colonization. Most effectors characterized thus far play roles in deregulation of host immunity. Arguably, however, pathogens not only deal with immune responses during host colonization, but also encounter other microbes including competitors, (myco)parasites and even potential co-operators. Thus, part of the effector catalog may target microbiome co-inhabitants rather than host physiology.
    Functional analysis of the tomato immune receptor Ve1 through domain swaps with Its non-functional homolog Ve2
    Fradin, E.F. ; Zhang, Z. ; Rövenich, H. ; Song, Y. ; Liebrand, T.W.H. ; Masini, L. ; Berg, G.C.M. van den; Joosten, M.H.A.J. ; Thomma, B.P.H.J. - \ 2014
    PLoS ONE 9 (2014)2. - ISSN 1932-6203 - 14 p.
    leucine-rich repeat - disease resistance protein - cladosporium-fulvum - arabidopsis-thaliana - endoplasmic-reticulum - hypersensitive response - verticillium resistance - plasma-membrane - innate immunity - kinase bri1
    Resistance in tomato against race 1 strains of the fungal vascular wilt pathogens Verticillium dahliae and V. albo-atrum is mediated by the Ve locus. This locus comprises two closely linked inversely oriented genes, Ve1 and Ve2, which encode cell surface receptors of the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) type. While Ve1 mediates Verticillium resistance through monitoring the presence of the recently identified V. dahliae Ave1 effector, no functionality for Ve2 has been demonstrated in tomato. Ve1 and Ve2 contain 37 eLRRs and share 84% amino acid identity, facilitating investigation of Ve protein functionality through domain swapping. In this study it is shown that Ve chimeras in which the first thirty eLRRs of Ve1 were replaced by those of Ve2 remain able to induce HR and activate Verticillium resistance, and that deletion of these thirty eLRRs from Ve1 resulted in loss of functionality. Also the region between eLRR30 and eLRR35 is required for Ve1-mediated resistance, and cannot be replaced by the region between eLRR30 and eLRR35 of Ve2. We furthermore show that the cytoplasmic tail of Ve1 is required for functionality, as truncation of this tail results in loss of functionality. Moreover, the C-terminus of Ve2 fails to activate immune signaling as chimeras containing the C-terminus of Ve2 do not provide Verticillium resistance. Furthermore, Ve1 was found to interact through its C-terminus with the eLRR-containing receptor-like kinase (eLRR-RLK) interactor SOBIR1 that was recently identified as an interactor of eLRR-RLP (immune) receptors. Intriguingly, also Ve2 was found to interact with SOBIR1.
    Effector-triggered defence against apoplastic fungal pathogens
    Stotz, H.U. ; Mitrousia, G.K. ; Wit, P.J.G.M. de; Fitt, B.D.L. - \ 2014
    Trends in Plant Science 19 (2014)8. - ISSN 1360-1385 - p. 491 - 500.
    programmed cell-death - plant immune-system - cf-2-dependent disease resistance - leptosphaeria-maculans - cladosporium-fulvum - brassica-napus - mycosphaerella-graminicola - avirulence gene - rhynchosporium-secalis - oilseed rape
    R gene-mediated host resistance against apoplastic fungal pathogens is not adequately explained by the terms pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) or effector-triggered immunity (ETI). Therefore, it is proposed that this type of resistance is termed 'effector-triggered defence' (ETD). Unlike PTI and ETI, ETD is mediated by R genes encoding cell surface-localised receptor-like proteins (RLPs) that engage the receptor-like kinase SOBIR1. In contrast to this extracellular recognition, ETI is initiated by intracellular detection of pathogen effectors. ETI is usually associated with fast, hypersensitive host cell death, whereas ETD often triggers host cell death only after an elapsed period of endophytic pathogen growth. In this opinion, we focus on ETD responses against foliar fungal pathogens of crops.
    Two for all: receptor-associated kinases SOBIR1 and BAK1
    Liebrand, T.W.H. ; Burg, H.A. van den; Joosten, M.H.A.J. - \ 2014
    Trends in Plant Science 19 (2014)2. - ISSN 1360-1385 - p. 123 - 132.
    plant innate immunity - pattern-recognition receptors - ethylene-inducing xylanase - arabidopsis-thaliana - cladosporium-fulvum - defense responses - cell-death - signaling pathways - plasma-membrane - protein-kinase
    Leucine-rich repeat-receptor-like proteins (LRR-RLPs) are ubiquitous cell surface receptors lacking a cytoplasmic signalling domain. For most of these LRR-RLPs, it remained enigmatic how they activate cellular responses upon ligand perception. Recently, the LRR-receptor-like kinase (LRR-RLK) SUPPRESSOR OF BIR1-1 (SOBIR1) was shown to be essential for triggering defence responses by certain LRR-RLPs that act as immune receptors. In addition to SOBIR1, the regulatory LRR-RLK BRI1-ASSOCIATED KINASE-1 (BAK1) is also required for LRR-RLP function. Here, we compare the roles of SOBIR1 and BAK1 as regulatory LRR-RLKs in immunity and development. BAK1 has a general regulatory role in plasma membrane-associated receptor complexes comprising LRR-RLPs and/or LRR-RLKs. By contrast, SOBIR1 appears to be specifically required for the function of receptor complexes containing LRR-RLPs.
    Cloning and functional characterization of the Rvi15 (Vr2) gene for apple scab resistance
    Schouten, H.J. ; Brinkhuis, J. ; Burgh, S. van der; Schaart, J. ; Groenwold, R. ; Broggini, G.A.L. ; Gessler, C. - \ 2014
    Tree Genetics and Genomes 10 (2014)2. - ISSN 1614-2942 - p. 251 - 260.
    malus x domestica - venturia-inaequalis - cladosporium-fulvum - cisgenic plants - plasma-membrane - vf gene - tomato - locus - proteins - pathogen
    Apple scab, caused by Venturia inaequalis, is a serious disease of apple. Previously, the scab resistance Rvi15 (Vr2) from the accession GMAL 2473 was genetically mapped, and three candidate resistance genes were identified. Here, we report the cloning and functional characterization of these three genes, named Vr2-A, Vr2-B, and Vr2-C. Each gene was cloned with its native promoter, terminator and introns, and inserted into the susceptible apple cultivar ‘Gala’. Inoculation of the plants containing Vr2-A and Vr2-B induced no resistance symptoms, but abundant sporulation. However, inoculation of the plants harboring Vr2-C showed a hypersensitive response with clear pinpoint pits, and no or very little sporulation. We conclude that Vr2-C is the Rvi15 (Vr2) gene. This gene belongs to the Toll and mammalian interleukin-1 receptor protein nucleotide-binding site leucine-rich repeat structure resistance gene family. The proteins of this gene family reside in the cytoplasm, whereas V. inaequalis develops in the apoplast, between the epidermis and cuticle, without making haustoria. The spatial separation of the recognizing resistance protein and the pathogen is discussed. This is the second cloned gene for apple scab resistance, and out of these two the only one leading to a symplastic protein.
    Pseudogenization in pathogenic fungi with different host plants and lifestyles might reflect their evolutionary past
    Burgt, I.A. van der; Karimi, M. ; Bahkali, A.H. ; Wit, P.J.G.M. de - \ 2014
    Molecular Plant Pathology 15 (2014)2. - ISSN 1464-6722 - p. 133 - 144.
    cladosporium-fulvum - gene - resistance - prediction - software - proteins - genomics - update - locus
    Pseudogenes are genes with significant homology to functional genes but contain disruptive mutations (DMs) leading to production of non- or partially functional proteins. Little is known about pseudogenization in pathogenic fungi with different lifestyles. Here we report on identification of DMs causing pseudogenes in the genomes of the fungal plant pathogens Botrytis cinerea, Cladosporium fulvum, Dothistroma septosporum, Mycosphaerella fijiensis, Verticillium dahliae and Zymoseptoria tritici. In these fungi we have identified 1740 gene models containing 2795 DMs obtained by an alignment-based gene prediction method. The contribution of sequencing errors to DMs was minimized by analyses of resequenced genomes to obtain a refined data set of 924 gene models containing 1666 true DMs. The frequency of pseudogenes varied from 1 to 5% in the gene catalogues of these fungi, being the highest in the asexually reproducing fungi C. fulvum (4.9%), followed by D. septosporum (2.4%) and V. dahliae (2.1%). The majority of pseudogenes does not represent recent gene duplications, but members of multi-gene families and unitary genes. In general there was no bias for pseudogenization of specific genes in the six fungi. Single exceptions are those encoding secreted proteins including proteases which appeared more frequently pseudogenized in C. fulvum than in D. septosporum. Most pseudogenes present in these two phylogenically closely related fungi are not shared suggesting that they are related to adaptation to a different host (tomato versus pine) and lifestyle (biotroph versus hemi-biotroph)
    System-Wide Hypersensitive Response-Associated Transcriptome and Metabolome Reprogramming in Tomato
    Etalo, D.W. ; Stulemeijer, I.J.E. ; Esse, H.P. van; Vos, R.C.H. de; Bouwmeester, H.J. ; Joosten, M.H.A.J. - \ 2013
    Plant Physiology 162 (2013)3. - ISSN 0032-0889 - p. 1599 - 1617.
    programmed cell-death - pathogen pseudomonas-syringae - campestris pv. vesicatoria - glutathione s-transferases - amino-acid catabolism - leaf rust resistance - higher-plant cells - mass-spectrometry - cladosporium-fulvum - functional-analysis
    The hypersensitive response (HR) is considered to be the hallmark of the resistance response of plants to pathogens. To study HR-associated transcriptome and metabolome reprogramming in tomato (Solanum lycopersicum), we used plants that express both a resistance gene to Cladosporium fulvum and the matching avirulence gene of this pathogen. In these plants, massive reprogramming occurred, and we found that the HR and associated processes are highly energy demanding. Ubiquitin-dependent protein degradation, hydrolysis of sugars, and lipid catabolism are used as alternative sources of amino acids, energy, and carbon skeletons, respectively. We observed strong accumulation of secondary metabolites, such as hydroxycinnamic acid amides. Coregulated expression of WRKY transcription factors and genes known to be involved in the HR, in addition to a strong enrichment of the W-box WRKY-binding motif in the promoter sequences of the coregulated genes, point to WRKYs as the most prominent orchestrators of the HR. Our study has revealed several novel HR-related genes, and reverse genetics tools will allow us to understand the role of each individual component in the HR.
    Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection
    Liebrand, T.W.H. ; Berg, G.C.M. van den; Zhang, Z. ; Smit, P. ; Cordewener, J.H.G. ; America, A.H.P. ; Sklenar, J. ; Jones, A.M.E. ; Tameling, W.I.L. ; Robatzek, S. ; Thomma, B.P.H.J. ; Joosten, M.H.A.J. - \ 2013
    Proceedings of the National Academy of Sciences of the United States of America 110 (2013)24. - ISSN 0027-8424 - p. 10010 - 10015.
    innate immunity - cladosporium-fulvum - verticillium resistance - citrx thioredoxin - plasma-membrane - tomato ve1 - cell-death - arabidopsis - perception - flagellin
    The plant immune system is activated by microbial patterns that are detected as nonself molecules. Such patterns are recognized by immune receptors that are cytoplasmic or localized at the plasma membrane. Cell surface receptors are represented by receptor-like kinases (RLKs) that frequently contain extracellular leucine-rich repeats and an intracellular kinase domain for activation of downstream signaling, as well as receptor-like proteins (RLPs) that lack this signaling domain. It is therefore hypothesized that RLKs are required for RLPs to activate downstream signaling. The RLPs Cf-4 and Ve1 of tomato (Solanum lycopersicum) mediate resistance to the fungal pathogens Cladosporium fulvum and Verticillium dahliae, respectively. Despite their importance, the mechanism by which these immune receptors mediate downstream signaling upon recognition of their matching ligand, Avr4 and Ave1, remained enigmatic. Here we show that the tomato ortholog of the Arabidopsis thaliana RLK Suppressor Of BIR1-1/Evershed (SOBIR1/EVR) and its close homolog S. lycopersicum (Sl)SOBIR1-like interact in planta with both Cf-4 and Ve1 and are required for the Cf-4– and Ve1-mediated hypersensitive response and immunity. Tomato SOBIR1/EVR interacts with most of the tested RLPs, but not with the RLKs FLS2, SERK1, SERK3a, BAK1, and CLV1. SOBIR1/EVR is required for stability of the Cf-4 and Ve1 receptors, supporting our observation that these RLPs are present in a complex with SOBIR1/EVR in planta. We show that SOBIR1/EVR is essential for RLP-mediated immunity and propose that the protein functions as a regulatory RLK of this type of cell-surface receptors.
    Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of cf receptor-like proteins involved in pathogen resistance of tomato
    Liebrand, T.W.H. ; Smit, P. ; Abd-El-Haliem, A. ; Jonge, R. de; Cordewener, J.H.G. ; America, A.H.P. ; Sklenar, J. ; Jones, A.M. ; Robatzek, S. ; Thomma, B.P.H.J. ; Tameling, W.I. ; Joosten, M.H.A.J. - \ 2012
    Plant Physiology 159 (2012)4. - ISSN 0032-0889 - p. 1819 - 1833.
    defective brassinosteroid receptor - pattern-recognition receptors - plant innate immunity - cladosporium-fulvum - disease resistance - hypersensitive response - virulence factor - effector ecp6 - cell-death - gene
    Cf proteins are receptor-like proteins (RLPs) that mediate resistance of tomato (Solanum lycopersicum) to the foliar pathogen Cladosporium fulvum. These transmembrane immune receptors, which carry extracellular leucine-rich repeats that are subjected to posttranslational glycosylation, perceive effectors of the pathogen and trigger a defense response that results in plant resistance. To identify proteins required for the functionality of these RLPs, we performed immunopurification of a functional Cf-4-enhanced green fluorescent protein fusion protein transiently expressed in Nicotiana benthamiana, followed by mass spectrometry. The endoplasmic reticulum (ER) heat shock protein70 binding proteins (BiPs) and lectin-type calreticulins (CRTs), which are chaperones involved in ER-quality control, were copurifying with Cf-4-enhanced green fluorescent protein. The tomato and N. benthamiana genomes encode four BiP homologs and silencing experiments revealed that these BiPs are important for overall plant viability. For the three tomato CRTs, virus-induced gene silencing targeting the plant-specific CRT3a gene resulted in a significantly compromised Cf-4-mediated defense response and loss of full resistance to C. fulvum. We show that upon knockdown of CRT3a the Cf-4 protein accumulated, but the pool of Cf-4 protein carrying complex-type N-linked glycans was largely reduced. Together, our study on proteins required for Cf function reveals an important role for the CRT ER chaperone CRT3a in the biogenesis and functionality of this type of RLP involved in plant defense
    In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins
    Stergiopoulos, I. ; Kourmpetis, Y.A. ; Slot, J.C. ; Bakker, F.T. ; Wit, P.J.G.M. de; Rokas, A. - \ 2012
    Molecular Biology and Evolution 29 (2012)11. - ISSN 0737-4038 - p. 3371 - 3384.
    amino-acid sites - functional divergence - kluyveromyces-lactis - maximum-likelihood - cladosporium-fulvum - multigene families - gene duplication - death process - mixed models - phylogeny
    Most fungal plant pathogens secrete effector proteins during pathogenesis to manipulate their host’s defense and promote disease. These are so highly diverse in sequence and distribution, they are essentially considered as species-specific. However, we have recently shown the presence of homologous effectors in fungal species of the Dothideomycetes class. One such example is Ecp2, an effector originally described in the tomato pathogen Cladosporium fulvum but later detected in the plant pathogenic fungi Mycosphaerella fijiensis and Mycosphaerella graminicola as well. Here, using in silico sequence-similarity searches against a database of 135 fungal genomes and GenBank, we extend our queries for homologs of Ecp2 to the fungal kingdom and beyond, and further study their history of diversification. Our analyses show that Ecp2 homologs are members of an ancient and widely distributed superfamily of putative fungal effectors, which we term Hce2 for Homologs of C. fulvum Ecp2. Molecular evolutionary analyses show that the superfamily originated and diversified within the fungal kingdom, experiencing multiple lineage-specific expansions and losses that are consistent with the birth-and- death model of gene family evolution. Newly formed paralogs appear to be subject to diversification early after gene duplication events, whereas at later stages purifying selection acts to preserve diversity and the newly evolved putative functions. Some members of the Hce2 superfamily are fused to fungal Glycoside Hydrolase family 18 chitinases that show high similarity to the Zymocin killer toxin from the dairy yeast Kluyveromyces lactis, suggesting an analogous role in antagonistic interactions. The observed high rates of gene duplication and loss in the Hce2 superfamily, combined with diversification in both sequence and possibly functions within and between species suggest that Hce2s are involved in adaptation to stresses and new ecological niches. Such findings address the need to rationalize effector biology and evolution beyond the perspective of solely host-microbe interactions
    Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease
    Mentlak, T.A. ; Kombrink, A. ; Shinya, T. ; Ryder, L.S. ; Otomo, I. ; Saitoh, H. ; Terauchi, R. ; Nishizawa, Y. ; Shibuya, N. ; Thomma, B.P.H.J. ; Talbot, N.J. - \ 2012
    The Plant Cell 24 (2012)1. - ISSN 1040-4651 - p. 322 - 335.
    cladosporium-fulvum - plant infection - defense responses - virulence factor - plasma-membrane - tomato cells - receptor - fungus - elicitor - protein
    Plants use pattern recognition receptors to defend themselves from microbial pathogens. These receptors recognize pathogen-associated molecular patterns (PAMPs) and activate signaling pathways that lead to immunity. In rice (Oryza sativa), the chitin elicitor binding protein (CEBiP) recognizes chitin oligosaccharides released from the cell walls of fungal pathogens. Here, we show that the rice blast fungus Magnaporthe oryzae overcomes this first line of plant defense by secreting an effector protein, Secreted LysM Protein1 (Slp1), during invasion of new rice cells. We demonstrate that Slp1 accumulates at the interface between the fungal cell wall and the rice plasma membrane, can bind to chitin, and is able to suppress chitin-induced plant immune responses, including generation of reactive oxygen species and plant defense gene expression. Furthermore, we show that Slp1 competes with CEBiP for binding of chitin oligosaccharides. Slp1 is required by M. oryzae for full virulence and exerts a significant effect on tissue invasion and disease lesion expansion. By contrast, gene silencing of CEBiP in rice allows M. oryzae to cause rice blast disease in the absence of Slp1. We propose that Slp1 sequesters chitin oligosaccharides to prevent PAMP-triggered immunity in rice, thereby facilitating rapid spread of the fungus within host tissue
    Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens
    Klosterman, S.J. ; Subbarao, K.V. ; Kang, S. ; Veronese, P. ; Gold, S.E. ; Thomma, B.P.H.J. ; Chen, Z.J. ; Henrissat, B. ; Lee, Y.H. ; Park, J. ; Garcia-Pedrajas, M.D. ; Barbara, D.J. ; Anchieta, A. ; Jonge, R. de; Santhanam, P. ; Maruthachalam, K. ; Atallah, Z. ; Amyotte, S.G. ; Paz, Z. ; Inderbitzin, P. ; Hayes, R.J. ; Heiman, D.I. ; Young, S. ; Zeng, Q. ; Engels, R. ; Galagan, J. ; Cuomo, C. ; Dobinson, K.F. ; Ma, L.J. - \ 2011
    PLoS Pathogens 7 (2011)7. - ISSN 1553-7366 - 19 p.
    induced point mutation - cladosporium-fulvum - verticillium wilt - fusarium-oxysporum - nep1-like proteins - maximum-likelihood - transcription factor - neurospora-crassa - virulence factor - effector ecp6
    The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases.
    The role of chitin detection in plant-pathogen interactions
    Kombrink, A. ; Sánchez-Vallet, A. ; Thomma, B.P.H.J. - \ 2011
    Microbes and Infection 13 (2011)14-15. - ISSN 1286-4579 - p. 1168 - 1176.
    cultured rice cells - receptor-like kinases - n-acetylchitooligosaccharide elicitor - fungus magnaporthe-oryzae - cladosporium-fulvum - high-affinity - binding-site - lysm domains - arbuscular mycorrhiza - medicago-truncatula
    Despite the deployment of antifungal defence strategies, fungal diseases occur in all types of multicellular organisms. In plants, the role of fungal chitin as pathogen-associated molecular pattern that activates host defence is well established. Interestingly, plants employ homologs of the chitin immune receptors to initiate microbial symbiosis. Accumulating evidence shows that fungal pathogens developed secreted effectors to disarm chitin-triggered host immunity.
    Interfamily Transfer of Tomato Ve1 Mediates Verticillium Resistance in Arabidopsis
    Fradin, E.F. ; Abd-El-Haliem, A. ; Masini, L. ; Berg, G.C.M. van den; Joosten, M.H.A.J. ; Thomma, B.P.H.J. - \ 2011
    Plant Physiology 156 (2011)4. - ISSN 0032-0889 - p. 2255 - 2265.
    receptor-like proteins - leucine-rich repeat - disease resistance - cladosporium-fulvum - cell-death - recognitional specificity - scab resistance - innate immunity - plant-pathogen - gene family
    Vascular wilts caused by soil-borne fungal species of the Verticillium genus are devastating plant diseases. The most common species, Verticillium dahliae and Verticillium albo-atrum, have broad host ranges and are notoriously difficult to control. Therefore, genetic resistance is the preferred method for disease control. Only from tomato (Solanum lycopersicum) has a Verticillium resistance locus been cloned, comprising the Ve1 gene that encodes a receptor-like protein-type cell surface receptor. Due to lack of a suitable model for receptor-like protein (RLP)-mediated resistance signaling in Arabidopsis (Arabidopsis thaliana), so far relatively little is known about RLP signaling in pathogen resistance. Here, we show that Ve1 remains fully functional after interfamily transfer to Arabidopsis and that Ve1-transgenic Arabidopsis is resistant to race 1 but not to race 2 strains of V. dahliae and V. albo-atrum, nor to the Brassicaceae-specific pathogen Verticillium longisporum. Furthermore, we show that signaling components utilized by Ve1 in Arabidopsis to establish Verticillium resistance overlap with those required in tomato and include SERK3/BAK1, EDS1, and NDR1, which strongly suggests that critical components for resistance signaling are conserved. We subsequently investigated the requirement of SERK family members for Ve1 resistance in Arabidopsis, revealing that SERK1 is required in addition to SERK3/BAK1. Using virus-induced gene silencing, the requirement of SERK1 for Ve1-mediated resistance was confirmed in tomato. Moreover, we show the requirement of SERK1 for resistance against the foliar fungal pathogen Cladosporium fulvum mediated by the RLP Cf-4. Our results demonstrate that Arabidopsis can be used as model to unravel the genetics of Ve1-mediated resistance.
    Analysis of Two in Planta Expressed LysM Effector Homologs from the Fungus Mycosphaerella graminicola Reveals Novel Functional Properties and Varying Contributions to Virulence on Wheat
    Marshall, R. ; Kombrink, A. ; Motteram, J. ; Loza-Reyes, E. ; Lucas, J. ; Hammond-Kosack, K.E. ; Thomma, B.P.H.J. ; Rudd, J.J. - \ 2011
    Plant Physiology 156 (2011)2. - ISSN 0032-0889 - p. 756 - 769.
    cladosporium-fulvum - septoria-tritici - maximum-likelihood - blotch pathogen - innate immunity - protein - resistance - host - tomato - recognition
    Secreted effector proteins enable plant pathogenic fungi to manipulate host defenses for successful infection. Mycosphaerella graminicola causes Septoria tritici blotch disease of wheat (Triticum aestivum) leaves. Leaf infection involves a long (approximately 7 d) period of symptomless intercellular colonization prior to the appearance of necrotic disease lesions. Therefore, M. graminicola is considered as a hemibiotrophic (or necrotrophic) pathogen. Here, we describe the molecular and functional characterization of M. graminicola homologs of Ecp6 (for extracellular protein 6), the Lysin (LysM) domain-containing effector from the biotrophic tomato (Solanum lycopersicum) leaf mold fungus Cladosporium fulvum, which interferes with chitin-triggered immunity in plants. Three LysM effector homologs are present in the M. graminicola genome, referred to as Mg3LysM, Mg1LysM, and MgxLysM. Mg3LysM and Mg1LysM genes were strongly transcriptionally up-regulated specifically during symptomless leaf infection. Both proteins bind chitin; however, only Mg3LysM blocked the elicitation of chitin-induced plant defenses. In contrast to C. fulvum Ecp6, both Mg1LysM and Mg3LysM also protected fungal hyphae against plant-derived hydrolytic enzymes, and both genes show significantly more nucleotide polymorphism giving rise to nonsynonymous amino acid changes. While Mg1LysM deletion mutant strains of M. graminicola were fully pathogenic toward wheat leaves, Mg3LysM mutant strains were severely impaired in leaf colonization, did not trigger lesion formation, and were unable to undergo asexual sporulation. This virulence defect correlated with more rapid and pronounced expression of wheat defense genes during the symptomless phase of leaf colonization. These data highlight different functions for MgLysM effector homologs during plant infection, including novel activities that distinguish these proteins from C. fulvum Ecp6.
    The Diverse Roles of Extracellular Leucine-rich Repeat-containing Receptor-like Proteins in Plants
    Wang, G. ; Fiers, M.A. ; Ellendorff, U. ; Wang, Z. ; Wit, P.J.G.M. de; Angenent, G.C. ; Thomma, B.P.H.J. - \ 2010
    Critical Reviews in Plant Sciences 29 (2010). - ISSN 0735-2689 - p. 285 - 299.
    stem-cell fate - cf-2-dependent disease resistance - arabidopsis shoot meristems - ligand-induced endocytosis - of-function phenotypes - apple scab disease - cladosporium-fulvum - organ development - hypersensitive response - root-meristem
    Plant cells use various types of cell surface receptor molecules to sense extracellular signals and modulate cell-to-cell communication in many biological processes. Extracellular leucine-rich repeat (eLRR) receptor-like proteins (RLPs) represent an important class of such cell surface receptors. RLPs differ from receptor-like kinases (RLKs), which compose the largest class of cell surface receptors in many plant species, because they lack a cytoplasmic kinase domain. RLPs play roles in both developmental processes and disease resistance. A total of 57 RLP encoding genes has been identified in Arabidopsis. Two of them, CLAVATA2 (CLV2) and Too Many Mouths (TMM) have a function in meristem maintenance and stomatal distribution, respectively, whereas few others act in basal defense against pathogens. Although the function of most RLPs in Arabidopsis remains unclear, considerable progress has been made in understanding RLP functioning and signaling over the years. This review focuses on the function of RLPs in plants. Furthermore, the function of distinct RLP domains and the role of conserved residues important for perception and ligand specificity are discussed. The role of RLP proteins in multimeric complexes to sense biotic and abiotic extracellular signals is also addressed.
    Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants
    Jonge, R. de; Esse, H.P. van; Kombrink, A. ; Shinya, T. ; Desaki, Y. ; Bours, R.M.E.H. ; Krol, A.R. van der; Shibuya, N. ; Joosten, M.H.A.J. ; Thomma, B.P.H.J. - \ 2010
    Science 329 (2010). - ISSN 0036-8075 - p. 953 - 955.
    receptor-like kinase - cladosporium-fulvum - virulence factor - binding - defense - tomato - cells - avr4 - recognition - arabidopsis
    Multicellular organisms activate immunity upon recognition of pathogen-associated molecular patterns (PAMPs). Chitin is the major component of fungal cell walls, and chitin oligosaccharides act as PAMPs in plant and mammalian cells. Microbial pathogens deliver effector proteins to suppress PAMP-triggered host immunity and to establish infection. Here, we show that the LysM domain–containing effector protein Ecp6 of the fungal plant pathogen Cladosporium fulvum mediates virulence through perturbation of chitin-triggered host immunity. During infection, Ecp6 sequesters chitin oligosaccharides that are released from the cell walls of invading hyphae to prevent elicitation of host immunity. This may represent a common strategy of host immune suppression by fungal pathogens, because LysM effectors are widely conserved in the fungal kingdom
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