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.

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    Validation of four real-time TaqMan PCRs for the detection of Ralstonia solanacearum and/or Ralstonia pseudosolanacearum and/or Clavibacter michiganensis subsp. sepedonicus in potato tubers using a statistical regression approach
    Vreeburg, R.A.M. ; Zendman, A.J.W. ; Pol, A. ; Verheij, E. ; Nas, M. ; Kooman-Gersmann, M. - \ 2018
    EPPO Bulletin 48 (2018)1. - ISSN 0250-8052 - p. 86 - 96.
    A new DNA extraction method and a new multiplex real-time TaqMan PCR test for detection of Ralstonia solanacearum, Ralstonia pseudosolanacearum and Clavibacter michiganensis subsp. sepedonicus in asymptomatic potato tubers are presented. This new multiplex PCR and three published TaqMan PCRs for detection of R. solanacearum and/or R. pseudosolanacearum and/or R. syzygii spp. and/or C. michiganensis subsp. sepedonicus were validated using linear regression analysis for estimating the Ct values and its variation at 5 × 103 bacteria mL−1. The three published PCRs that have been validated are Massart et al. (2014, detecting R. solanacearum and C. michiganensis subsp. sepedonicus), Weller et al. (1999, detecting R. solanacearum, R. pseudosolanacearum and R. syzygii spp.) and Gudmestad et al. (2009, detecting C. michiganensis subsp. sepedonicus). All tested PCRs were fit for purpose for their target organisms. The PCR tests have different target genes, allowing one of the sets to be used as first screening test and another as second screening test for the detection of R. solanacearum and/or R. pseudosolanacearum and/or C. michiganensis subsp. sepedonicus in asymptomatic potato tubers.
    Virulence of Pectobacterium carotovorum subsp. brasiliense on potato compared with that of other Pectobacterium and Dickeya species under climatic conditions prevailing in the Netherlands
    Wolf, J.M. van der; Haan, E.G. de; Kastelein, P. ; Krijger, M.C. ; Haas, B.H. de; Velvis, H. ; Mendes, O. ; Kooman-Gersmann, M. ; Zouwen, P.S. van der - \ 2017
    Plant Pathology 66 (2017)4. - ISSN 0032-0862 - p. 571 - 583.
    In western Europe, Pectobacterium carotovorum subsp. brasiliense is emerging as a causal agent of blackleg disease. In field experiments in the Netherlands, the virulence of this pathogen was compared with strains of other Dickeya and Pectobacterium species. In 2013 and 2014, seed potato tubers were vacuum infiltrated with high densities of bacteria (106 CFU mL−1) and planted in clay soil. Inoculation with P. carotovorum subsp. brasiliense and P. atrosepticum resulted in high disease incidences (75–95%), inoculation with D. solani and P. wasabiae led to incidences between 5% and 25%, but no significant disease development was observed in treatments with P. carotovorum subsp. carotovorum, D. dianthicola or the water control. Co-inoculations of seed potatoes with P. carotovorum subsp. brasiliense and D. solani gave a similar disease incidence to inoculation with only P. carotovorum subsp. brasiliense. However, co-inoculation of P. carotovorum subsp. brasiliense with P. wasabiae resulted in a decrease in disease incidence compared to inoculation with only P. carotovorum subsp. brasiliense. In 2015, seed potatoes were inoculated with increasing densities of P. carotovorum subsp. brasiliense, D. solani or P. atrosepticum (103–106 CFU mL−1). After vacuum infiltration, even a low inoculum density resulted in high disease incidence. However, immersion without vacuum caused disease only at high bacterial densities. Specific TaqMan assays were evaluated and developed for detection of P. carotovorum subsp. brasiliense, P. wasabiae and P. atrosepticum and confirmed the presence of these pathogens in progeny tubers of plants derived from vacuum-infiltrated seed tubers.
    Herkenning van AVR9 door tomatenplanten met het CF-9 resistentiegen
    Kooman-Gersmann, M. - \ 1999
    Gewasbescherming 30 (1999)1. - ISSN 0166-6495 - p. 23 - 23.
    The fungal gene Avr9 and the oomycete gene inf1 confer avirulence to potato virus X on tobacco
    Kamoun, S. ; Honée, G. ; Weide, R. ; Laugé, R. ; Kooman-Gersmann, M. ; Groot, K. de; Govers, F. ; Wit, P.J.G.M. de - \ 1999
    Molecular Plant-Microbe Interactions 12 (1999)5. - ISSN 0894-0282 - p. 459 - 462.
    The AVR9 peptide of the fungal pathogen Cladosporium fulvum and the INF1 protein of the oomycete pathogen Phytophthora infestans elicit the hypersensitive response (HR) on Cf9 tomato or Cf-9 transgenic tobacco and on all cultivars of tobacco, respectively. Expression of either the functional Avr9 or inf1 genes from engineered potato virus X (PVX) genomes resulted in localized HR lesions on tobacco plants responsive to the elicitors and inhibited spread of the recombinant virus. In contrast, PVX derivatives producing mutant forms of AVR9 and INF1 with reduced elicitor activity caused systemic necrotic and/or mosaic symptoms, and were unable to inhibit PVX spread. These results demonstrate that HR is a highly versatile defense mechanism active against unrelated pathogens irrespective of the HR-inducing agent, and that resistance to recombinant PVX in tobacco is correlated with the strength of the transgene-encoded elicitor.
    Gene-for-gene interactions: the role of avirulence genes in pathogenicity and race-specific resistance.
    Wit, P.J.G.M. de; Joosten, M.H.A.J. ; Lauge, R. ; Roth, R. ; Luderer, R. ; Westerink, N. ; Honee, G. ; Kooman-Gersmann, M. ; Laurent, F. ; Hoorn, R.A.L. van der; Jong, C.F. de - \ 1998
    In: 7th International Congress of Plant Pathology, Edinburgh, UK (1998) 1.1.1
    Avirulence and pathogenicity genes of Cladosporium fulvum.
    Wit, P.J.G.M. de; Lauge, R. ; Goodwin, P.H. ; Joosten, M.H.A.J. ; Vossen, P. ; Kooman-Gersmann, M. ; Weide, R. ; Honee, G. - \ 1998
    In: 15th Eucarpia General Congress, Viterbo, Italy - p. 1 - 2.
    The AVR9 elicitor peptide of the tomato pathogen Cladosporium fulvum : molecular aspects of recognition
    Kooman - Gersmann, M. - \ 1998
    Agricultural University. Promotor(en): P.J.G.M. de Wit; G.J.E.M. Honee. - S.l. : Kooman-Gersmann - ISBN 9789054857938 - 117
    tomaten - passalora fulva - deuteromycotina - solanum lycopersicum - fysiologie - gastheer parasiet relaties - moleculaire biologie - plantenziektekunde - ziekteresistentie - genen - genomen - dematiaceae - tomatoes - passalora fulva - deuteromycotina - solanum lycopersicum - physiology - host parasite relationships - molecular biology - plant pathology - disease resistance - genes - genomes - dematiaceae

    The interaction between the fungal pathogen Cladosporium fulvum and tomato has been used as a model system to study the molecular basis of gene-for-gene relationships. C. fulvum is a specialized, biotrophic pathogen, which causes leaf mold on tomato. Under humid conditions conidia of C. fulvum germinate and form runner hyphae on the lower side of the leaf. If no resistance genes of the plant match any of the avirulence genes of the fungus, the interaction is compatible and infection will proceed. However, when both a resistance gene and its matching avirulence gene are present, the plant recognizes the fungus and the interaction is incompatible. In an incompatible interaction active defense responses, including the hypersensitive response (HR) are initiated, which inhibit fungal growth effectively. Avirulence genes encode lace-specific elicitors, which are present in intercellular washing fluids obtained from compatible interactions of C. fulvum and tomato (De Wit and Spikman, 1982). Injection of these intercellular washing fluids in tomato plants resistant to the C. fulvum strain from which the washing fluids were obtained, results in specific necrosis at the site of injection. The race-specific elicitor AVR9 was isolated and purified (Scholtens-Toma and de Wit, 1988). AVR9 specifically induces necrosis on tomato genotypes carrying the Cf-9 resistance gene. The encoding AVR9 gene was isolated, and it was shown that this gene specifically determines avirulence of C. fulvum on tomato plants carrying the Cf-9 resistance gene (Van den Ackerveken et al., 1992; Marmeisse et al., 1993). The Avr9 gene encodes a 63-amino acid pre-proprotein containing one potential glycosylation site (Van den Ackerveken et al., 1993). Different forms of the AVR9 elicitor were found, of which the mature AVR9 elicitor of 28 amino acids is predominantly present in C. fulvum-infected tomato plants (Van den Ackerveken et al., 1993). The global structure of the AVR9 peptide shows 3 antiparallel β-sheets and 3 disulfide bonds that are arranged in a cystine knot (Vervoort et al., 1997).

    In the research project described in this thesis, we studied AVR9 elicitor perception in tomato plants that carry the Cf-9 resistance gene and compared the results to those obtained with tomato plants lacking this gene. Previously, several research groups had shown that elicitors are recognized through plants receptors, which are localized on the plasma membrane (summarized in chapter 1). To find and characterize the receptor for AVR9, the peptide was labeled with iodine-125 and binding to tomato membranes was studied, as presented in chapter 2. 125 I-AVR9 showed specific, saturable, and reversible
    binding to plasma membranes isolated from leaves of the tomato cultivar Moneymaker without Cf resistance genes (MM-Cf0) and to membranes from a near-isogenic genotype containing the Cf-9 resistance gene (MM-Cf9). Binding of AVR9 is characterized by high affinity and low receptor concentration, and thus fulfills several criteria expected for functional receptors (Hulme and Birdsall, 1992). The dissociation constant was determined at 0.07 nM, and the receptor concentration was determined at 0.8 pmol/mg microsomal membrane protein. Binding is highly influenced by pH and ionic strength of the binding buffer and by temperature, indicating the involvement of both electrostatic and hydrophobic interactions. Surprisingly, binding kinetics and binding capacity were identical for membranes of the MM-Cf0 and MM-Cf9 tomato genotype, indicating that the Cf-9 resistance gene is not required for binding of AVR9. By that time, the Cf-9 resistance gene was isolated (Jones et al., 1994). Cf-9 belongs to a gene family and homologues of the Cf-9 resistance gene are present in both resistant and susceptible tomato genotypes. Two new hypotheses were developed of which the first predicts that not only the Cf-9 resistance gene, but also homologues of the Cf-9 gene, encode the high-affinity binding site for AVR9. Only the protein encoded by Cf-9 itself, designated CF-9, would subsequently initiate the signal transduction cascade resulting in HR. The second hypothesis predicts that the AVR9 binding site is neither CF- 9 nor a homologue of CF-9. The binding site proposed in the second hypothesis would bind AVR9 and subsequently recruit the CF-9 protein to initiate HR.

    As described in chapters 3, 4, and 5, experiments were performed to prove or reject one of these two hypotheses. To determine whether the high-affinity binding site for AVR9 is indeed a functional receptor, we studied the correlation between binding affinity and necrosis-inducing activity of mutant AVR9 peptides. We determined structure-activity relationships of the AVR9 peptide by independently substituting each amino acid of AVR9 by alanine, using a site-directed mutagenesis approach. In addition, surfaceexposed amino acid residues of AVR9 were substituted by other amino acids. Activity of mutant Avr9 constructs was studied by expressing the constructs in MM-Cf9 tomato plants using the potato virus X (PVX) expression system, and assessing the severity of necrosis induced by each PVX::Avr9 construct. This allowed direct identification of amino acid residues of AVR9 that are essential for elicitor activity. We identified amino acid substitutions resulting in AVR9 mutants with higher, similar or lower elicitor activity compared to the wild-type AVR9 peptide. Mutants of the amino acid residues Phe21 and Leu24 had completely lost elicitor activity. Necrosis-inducing activity of isolated AVR9 peptides correlated well with the necrosis induced by the corresponding PVX::Avr9 constructs. It was concluded the PVX expression system is ideally suited to analyze necrosis-inducing activity of AVR9 peptides. We analyzed whether there is a correlation between elicitor activity of the mutant AVR9 peptides and their affinity to the binding site in membranes of tomato. Therefore, Nicotiana clevelandii plants were inoculated with a selection of PVX::Avr9 constructs and mutant AVR9 peptides were purified from these plants. In addition, some AVR9 peptides were chemically synthesized. Characterization by Electrospray Mass Spectrometry, Circular Dichroism-, and 'H-NMR- spectroscopy revealed that both the in planta produced and the synthetic mutant peptides were correctly folded. AVR9 peptides purified from PVX::Avr9-infected N. clevelandii contained one N-acetylglucosamine, although small amounts of non- glycosylated AVR9 peptides were also detected. The glycosylated AVR9 peptides showed lower affinity to the binding site than the non-glycosylated AVR9 peptides, whereas they did not differ significantly in necrosis-inducing activity. For both the non- glycosylated and glycosylated mutant AVR9 peptides, a positive correlation between their affinity to the membranelocalized binding site and their necrosis-inducing activity in MM-Cf9 tomato was found, i.e. peptides with higher affinity to the binding site showed higher necrosis-inducing activity. This correlation suggested that the characterized high-affinity binding site for AVR9 is indeed a functional receptor that initiates the AVR9- CF-9-dependent HR in MM-Cf9 plants.

    In chapter 5, we studied whether the Cf-9 resistance gene or (one of) its homologues code for an AVR9 binding site. We tested binding of AVR9 to microsomal membranes of a variety of solanaceous and non-solanaceous plant species and analyzed these species for the presence of Cf-9-homologues. All solanaceous species tested contain homologues of the Cf-9 resistance gene and membranes of these plants contain a highaffinity binding site for AVR9. However, a high affinity binding site for AVR9 is also present on membranes of the non-solanaceous plant species cucumber, barley and oat, which do not contain homologues of the Cf-9 resistance gene. Membranes of tobacco, transgenic for the Cf-9 resistance gene, showed no change in the number of AVR9 binding sites. Arabidopsis does not have a binding site for AVR9 and membranes of Arabidopsis, transgenic: for the Cf-9 resistance gene, also showed no AVR9 binding. From this we concluded that not only the Cf-9 resistance gene, but also its homologues are not required for high-affinity binding of AVR9. Based on the presented data, we have developed a model, explaining recognition of AVR9 in MM-Cf-9 tomato (chapter 6). This model predicts that the high-affinity binding protein either 'presents' the AVR9 elicitor to the Cf-9-encoded protein or that binding of AVR9 induces a conformational change of the high-affinity binding protein. The latter results in recruitment of Cf-9 into the AVR9- receptor complex. Subsequently, signal cascade(s) resulting in HR will be initiated.

    Correlation between binding affinity and necrosis-inducing activity of mutant AVR9 peptide elicitors.
    Kooman-Gersmann, M. ; Vogelsang, R. ; Vossen, P. ; Hooven, H.W. van den; Mahe, E. ; Honee, G. ; Wit, J.G.M. de - \ 1998
    Plant Physiology 117 (1998). - ISSN 0032-0889 - p. 609 - 618.
    Molecular basis of pathogenicity, avirulence and resistance in the interaction between the fungal pathogen Cladosporium fulvum and tomato.
    Laug, R. ; Goodwin, P.H. ; Joosten, M.H.A.J. ; Vossen, P. ; Kooman-Gersmann, M. ; Weide, R. ; Honée, G. ; Wit, P.J.G.M. de - \ 1997
    In: Human Capital and Mobility workshop, Rome (1997)
    Avirulence genes in plant-fungi interactions.
    Laug, R. ; Joosten, M.H.A.J. ; Honée, G. ; Laurent, G. ; Kooman-Gersmann, M. ; Vossen, P. ; Weide, R. ; Wit, P.J.G.M. de - \ 1997
    In: Journees Jean Chevaugeon. Rencontres de Mycologie-Phytopathologie, Aussois (France) (1997)
    Assignment of amino acid residues of the AVR9 peptide of Cladosporium fulvum that determine elicitor activity.
    Kooman-Gersmann, M. ; Vogelsang, R. ; Hoogendijk, E.C.M. ; Wit, P.J.G.M. de - \ 1997
    Molecular Plant-Microbe Interactions 10 (1997). - ISSN 0894-0282 - p. 821 - 829.
    A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other solanaceous plants.
    Kooman-Gersmann, M. ; Honée, G. ; Bonnema, G. ; Wit, P.J.G.M. de - \ 1996
    The Plant Cell 8 (1996). - ISSN 1040-4651 - p. 929 - 938.
    Host genotype-specific adaptation of the tomato pathogen Cladosporium fulvum.
    Joosten, M.H.A.J. ; Laugé, R. ; Vossen, J.P.M.J. ; Honée, G. ; Weide, R. ; Kooman-Gersmann, M. ; Wit, P.J.G.M. de - \ 1996
    In: Culture collections to improve the quality of life, R.A. Samson et al. (eds.). Proc. 8th Int. Congr. for Culture Collections. Veldhoven, The Netherlands - p. 355 - 359.
    Interplay of fungal avirulence genes with plant resistance genes.
    Wit, P.J.G.M. de; Vossen, J.P.M.J. ; Kooman-Gersmann, K. ; Vogelsang, R. ; Joosten, M.H.A.J. ; Honée, G. ; Vervoort, J.J.M. - \ 1996
    In: Abstracts 3rd European Conf. on Fungal genetics, Münster, Germany - p. 13 - 13.
    Structure-function relation studies on AVR9 and AVR4 elicitors of Cladosporium fulvum.
    Wit, P.J.G.M. de; Vossen, J.P.M.J. ; Laugé, R. ; Kooman-Gersmann, M. ; Vogelsang, R. ; Joosten, M.H.A.J. ; Honée, G. ; Weide, R.L. ; Vervoort, J.J.M. - \ 1996
    In: Abstracts 8th Int. Congr. Molecular-Plant-Microbe Interactions, Knoxville TN, USA (1996) S-52
    Structure and function of avirulence genes and their interactions with plant resistance genes.
    Wit, P.J.G.M. de; Kooman-Gersmann, M. ; Vogelsang, R. ; Joosten, M.H.A.J. ; Vervoort, J.J.M. - \ 1996
    In: Abstracts Federation of the European Biochemical Society (FEBS) Congr., Barcelona, Spain - p. 196 - 196.
    Structure-function relation studies on AVR9 and AVR4 elicitors of Cladosporium fulvum.
    Wit, P.J.G.M. de; Kooman-Gersmann, M. ; Vogelsang, R. ; Joosten, M.H.A.J. ; Vossen, J.P.M.J. ; Weide, R.L. ; Laugé, R. ; Honée, G. ; Vervoort, J.J.M. - \ 1996
    In: Biology of plant-microbe interactions, G. Stacy et al. (eds.). IS-MPMI, Minnesota, USA - p. 253 - 258.
    A high affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of resitant and susceptible tomato genotypes.
    Kooman-Gersmann, M. ; Honée, G. ; Weide, R. ; Wit, P.J.G.M. de - \ 1996
    In: Abstracts 48th Int. Symp. on Crop protection, Ghent, Belgium - p. 20 - 20.
    Molecular basis of pathogenicity, avirulence and resistance in the interaction between the fungal pathogen Cladosporium fulvum and tomato.
    Laugé, R. ; Weide, R. ; Joosten, M.H.A.J. ; Honée, G. ; Vossen, P. ; Kooman-Gersmann, M. ; Vogelsang, R. ; Buitink, J. ; Jabs, T. ; Vervoort, J.M. ; Wit, P.J.G.M. de - \ 1996
    In: Abstracts Human Capital and Mobility Workshop on Molecular genetics of fungal plant pathogens & Signal perception and transduction in plant-fungus interactions, Córdoba, Spain - p. 15 - 21.
    A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is required for the Cf-9 dependent resistance response.
    Kooman-Gersmann, M. ; Vogelsang, R. ; Honée, G. ; Weide, R. ; Wit, P.J.G.M. de - \ 1996
    In: Abstracts 8th Int. Congr. Molecular Plant-Microbe Interactions, Knoxville TN, USA - p. J21 - J21.
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