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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    An inventory of pig production systems in Europe
    Bonneau, M. ; Dourmad, J.Y. ; Phatsara, C. ; Rydhmer, L. ; Edge, H.L. ; Fabrega, E. ; Greef, K.H. de; Eidnes Sorensen, P. ; Laugé, V. ; Ilari, E. - \ 2009
    Recognition of Cladosporium fulvum Ecp2 elicitor by non-host Nicotiana spp. is mediated by a single dominant gene that is not homologous to known Cf-genes
    Kock, M.J.D. de; Iskandar, H.M. ; Brandwagt, B.F. ; Laugé, R. ; Wit, P.J.G.M. de; Lindhout, W.H. - \ 2004
    Molecular Plant Pathology 5 (2004)5. - ISSN 1464-6722 - p. 397 - 408.
    cultured parsley cells - tobacco mosaic-virus - f-sp lycopersici - disease resistance - confers resistance - short arm - phytophthora-infestans - oligopeptide elicitor - pathogen phytophthora - functional expression
    Cladosporium fulvum is a fungal pathogen of tomato that grows exclusively in the intercellular spaces of leaves. Ecp2 is one of the elicitor proteins that is secreted by C. fulvum and is specifically recognized by tomato plants containing the resistance gene Cf-Ecp2. Recognition is followed by a hypersensitive response (HR) resulting in resistance. HR-associated recognition of Ecp2 has been observed in Nicotiana paniculata, N. sylvestris, N. tabacum and N. undulata that are non-host plants of C. fulvum. Absence of Ecp2-recognition did not lead to growth of C. fulvum on Nicotiana plants. We show that HR-associated recognition of Ecp2 is mediated by a single dominant gene in N. paniculata. However, based on PCR and hybridization analysis this gene is not homologous to known Cf-genes
    Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants
    Laugé, R. ; Goodwin, P.H. ; Wit, P.J.G.M. de; Joosten, M.H.A.J. - \ 2000
    The Plant Journal 23 (2000)6. - ISSN 0960-7412 - p. 735 - 745.
    The resistance of tomato (Lycopersicon esculentum) to the pathogenic fungus Cladosporium fulvum complies with the gene-for-gene concept. Host resistance is based on specific recognition of extracellular fungal proteins, resulting in a hypersensitive response (HR). Five proteins secreted by C. fulvum were purified and the encoding cDNA clone was obtained from two novel ones among them. Various tomato breeding lines and accessions of Lycopersicon pimpinellifolium were tested for their recognitional specificity by injection of the purified proteins or potato virus X-based expression of the cDNA. We found that HR-associated recognition of one or more of these proteins, in addition to recognition of the race-specific elicitors AVR4 and AVR9 of C. fulvum, occurs among Lycopersicon species. Studies on the inheritance of this recognition confirmed that single dominant genes are involved. Furthermore, one of the extracellular proteins of C. fulvum is specifically recognized by Nicotiana paniculata, which is not a host for C. fulvum. These results indicate that plants have a highly effective surveillance system for the presence of 'foreign' proteins, which, together with the high mutation rate of pathogens, can explain the complex gene-for-gene relationships frequently observed in pathosystems.
    Mapping strategy for resistance against Cladosporium fulvum on the short arm of Chromosome 1 of tomato : Cf-ECP5 near the Hcr9 Milky Way cluster
    Haanstra, J.P.W. ; Meijer-Dekens, F. ; Lauge, R. ; Seetanah, D.C. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de; Lindhout, P. - \ 2000
    Theoretical and Applied Genetics 101 (2000). - ISSN 0040-5752 - p. 661 - 668.
    Fungal (A)virulence and host resistance in the Cladosporium fulvum-tomato interaction
    Joosten, M.H.A.J. ; Cai, X. ; Hoorn, R. van der; Jong, C.F. de; Kock, M. de; Laugé, R. ; Luderer, R. ; Roth, R. ; Takken, F. ; Vossen, P. ; Weide, R. ; Westerink, N. ; Wit, P.J.G.M. de - \ 2000
    In: Biology of Plant-Microbe Interactions, volume 2 / de Wit, P.J.G.M., Bisseling, T., Stiekema, W.J., St. Paul, Minnesota, USA : Int. Soc. for Molecular Plant=Microbe Interactions - ISBN 9780965462518 - p. 29 - 34.
    Structure and function of virulence and avirulence genes of Cladosporium fulvum and Cf resistance genes of tomato
    Wit, P.J.G.M. de; Cai, X. ; Hoorn, R. van der; Jong, C. de; Kock, M. de; Kruijt, M. ; Laugé, R. ; Luderer, R. ; Roth, R. ; Takken, F. ; Vossen, P. ; Weide, R. ; Westerink, N. ; Joosten, M.H.A.J. - \ 2000
    In: Book of Abstracts : New Frontiers in Plant Science and Plant Biotechnology, Toulouse-LabOge, France, 5-9 March 2000. - Institute Federatif de Recherche, Toulouse-LabOge, France, 2000 - p. 63 - 63.
    Structure and function of virulence and avirulence genes of Cladosporium fulvum and Cf resistance genes of tomato
    Wit, P.J.G.M. de; Cai, X. ; Hoorn, R. van der; Jong, C. de; Kock, M. de; Kruijt, M. ; Laugé, R. ; Luderer, R. ; Roth, R. ; Takken, F. ; Vossen, P. ; Weide, R. ; Westerink, N. ; Joosten, M.H.A.J. - \ 2000
    In: Abstract Book : Fifth European Conference on Fungal Genetics, Arcachon, France, 25-28 March 2000 Arcachon, France : - p. 8 - 8.
    The surveillance system for Cladosporium fulvum proteins in tomato and its wild relatives
    Wit, P. de; Hoorn, R. van der; Jong, C. de; Laugé, R. ; Luderer, R. ; Roth, R. ; Takken, F. ; Westerink, N. ; Joosten, M. - \ 2000
    In: Book of Abstracts: Self-defense signaling pathways in plants : NIAR-COE/BRAIN/CREST Joint International Symposium, Tsukuba, Japan, 16-17 November 2000. - Tsukuba, Japan : NIAR/BRAIN/CREST, 2000 - p. 5III4 - 5III4.
    Extracellular proteins of the tomato pathogen Cladosporium fulvum; role in pathogenicity and avirulence
    Lauge, R. - \ 1999
    Agricultural University. Promotor(en): P.J.G.M. de Wit; M.H.A.J. Joosten; H.W.J. van den Broek. - S.l. : Lauge - ISBN 9789054859857 - 93
    tomaten - plantenziekteverwekkers - plantenziekteverwekkende schimmels - passalora fulva - cladosporium - pathogeniteit - virulentie - moleculaire genetica - genexpressie - eiwitten - solanum lycopersicum - tomatoes - plant pathogens - plant pathogenic fungi - passalora fulva - cladosporium - pathogenicity - virulence - molecular genetics - gene expression - proteins - solanum lycopersicum

    The interaction between the biotrophic fungus Cladosporium fulvum (Cooke) and its only host, tomato ( Lycopersicon esculentum Miller) complies with the gene-for-gene model. Early genetic studies have shown that many different avirulence ( Avr ) and resistance ( R ) gene pairs exist between strains of the fungus and genotypes of the plant, respectively. Previous studies in our laboratory, as summarized in Chapter 1, led to the isolation and characterization of several proteins of fungal and plant origin that occur in the apoplast during infection. The search for proteinaceous fungal elicitors that could act as avirulence factors on resistant tomato genotypes, led to the isolation of two proteins, AVR4 and AVR9. The development of molecular tools to manipulate C. fulvum provided means to confirm that the two encoding genes, Avr 4 and Avr 9, are the avirulence genes that match the tomato resistance genes Cf-4 and Cf-9 , respectively. The genes encoding two additional fungal e xtra c ellular p roteins (ECPs), Ecp 1 and Ecp 2, have also been cloned. Based on their specific induction in planta , both genes were proposed to be putative pathogenicity genes.

    The object of the research presented in this thesis was to obtain a better understanding of the function of the ECPs in pathogenicity and virulence of C. fulvum on tomato and of their potential role as specific elicitors on particular tomato genotypes, which would possibly fit into additional Avr / R gene-for-gene pairs. Accordingly, most of the work presented in this thesis involves studies on the biological function of the ECP1 and ECP2 proteins and additionally characterized ECPs of C. fulvum .

    In Chapter 2 a review on our current knowledge on fungal avirulence genes is presented. Although only a few fungal Avr genes have been cloned so far, they encode very different proteins and are differently regulated. Their involvement in pathogenicity or virulence, the type of responses that their products trigger on plants carrying the matching resistance genes, and their potential application in molecular resistance breeding are discussed.

    Pathogenicity assays with transgenic strains of C. fulvum in which the Ecp 1 and/or Ecp 2 genes were deleted are presented in Chapter 3. Both genes are virulence factors, as their encoded products, ECP1 and ECP2, are required for full virulence. Nevertheless, when absent, the fungus is still able to cause disease on tomato. The studies also indicate that both genes might function as suppressors of plant defense responses. It is envisaged that pathogenicity of C. fulvum on tomato results from synergism between multiple virulence factors. That is, while each single virulence factor is partly involved in causing disease on tomato, the presence of a complete set of virulence factors ensures maximal parasitic ability.

    Both ECP1 and ECP2 proteins are secreted, have a low molecular weight and are cysteine-rich proteins. They are secreted early and abundantly in the intercellular space, in a similar manner as observed for the two race-specific elicitors, AVR4 and AVR9. In Chapter 4 a search for plant genotypes that could recognize these proteins as specific elicitors of HR is described. One genotype of tomato, which had been preselected for resistance to C. fulvum , showed specific HR upon exposure to ECP2. Significantly, resistance of this genotype was shown to rely solely on ECP2 recognition. The resistance character is conferred by a single dominant gene, designated Cf-ECP2 . Analogous to the Avr 4/ Cf-4 and Avr 9/ Cf-9 gene pairs, Ecp 2/ Cf-ECP2 represents a genuine gene-for-gene pair within the C. fulvum -tomato interaction.

    Since the Cf-ECP2 gene operates through recognition of a crucial virulence factor, it may, therefore, provide durable protection against C. fulvum in tomato crops. Thus, the same protein may have a role in virulence on all tomato plants and a role in avirulence on only particular tomato genotypes.

    In Chapter 5, we subsequently initiated an extensive screen for plants among breeding lines and wild accessions of Lycopersicon species that could respond specifically with HR to any of the five interaction-specific fungal ECPs that we had isolated. Indeed, for each of the five ECPs that were tested, we found at least one individual that responded with HR. This observation indicates that recognition specificities are scattered among populations of plants, suggesting that recognition of proteins of C. fulvum is a generic property of the Lycopersicon genus. To investigate whether this is also true for a non-host species of C. fulvum , wild accessions of Nicotiana spp. were screened for similar specific HR-associated recognition of proteins of C. fulvum . We identified a few N. paniculata plants that exhibited a specific HR towards ECP2. This suggests that generic recognition specificities of proteinaceous elicitors of a fungal pathogen exist in solanaceous plants outside its host range. Consequently, the plant system for recognition of foreign proteins seems to generate new specificities at random, rather than specificities against classes of proteins produced by the pathogens of a given host plant.

    Recently, the cloning of four tomato Cf genes, among which are the Cf-4 and the Cf-9 genes that match the avirulence genes Avr 4 and Avr 9 respectively, was reported. They all belong to the same gene family, which is predicted to encode membrane-anchored leucine-rich-repeat (LRR) proteins. As such, they might participate in the perception of the different fungal avirulence factors. The Cf genes are members of clusters containing several homologues.

    In Chapter 6 we tested whether some of the Cf-9 homologues, referred to as Hcr9-9 genes ( H omologue of C ladosporium fulvumR esistance gene Cf- 9 present at the Cf- 9 locus), could confer additional resistance against C. fulvum . Inoculation of fungal strains in which the Avr 9 gene was deleted onto Cf9 tomato genotypes, showed that additional partial resistance(s) are present on the L.pimpinellifolium genomic segment introgressed into L. esculentum . These additional resistance(s) are independent of the Avr 9/ Cf-9 gene pair and are most probably due to one or more of the Hcr9-9 genes. However, we could not identify any specific proteinaceous elicitor activity in apoplastic fluids of compatible C. fulvum /tomato interactions that could match the identified additional resistance(s). The suggestion that Hcr9-9 genes are responsible for the additional resistance(s) has been proven in an independent study in another research group. Therefore, the Lycopersicon genus is not only rich in recognition specificities for secreted C. fulvum proteins (AVRs and ECPs), also a single plant genotype appears to contain multiple recognition capacities towards a single fungal strain.

    The data obtained in this research are discussed in Chapter 7. They indicate that HR-associated recognition of extracellular, low-molecular weight, cysteine-rich proteins of C. fulvum , some of which are involved in pathogenicity, is a general phenomenon in the Lycopersicon genus. The finding that some of these proteins, that act as avirulence factors, are also important virulence factors of the fungus might help to develop a strategy for identification of putative durable resistance genes, as proposed for the Cf-ECP2 gene. The demonstration of partial resistance(s) conferred by the Cf-9 homologues, without detection of a HR-phenotype, could suggest that recognition capacities of these genes are not limited to proteins, or that gene-for-gene responses other than HR occur in the C. fulvum -tomato interaction. In addition, our data indicate that HR-recognition of C. fulvum proteins is not confined to its host genus, Lycopersicon , but also occurs in the non-host genus Nicotiana .

    In conclusion, it appears that the diversity of the HR-associated recognition of proteins by a variety of Cf genes in a population of tomato relatives, generates plants with a genuine surveillance system against invading pathogens. The importance of the recognized proteins in pathogenicity or virulence of the pathogen is likely to be positively correlated with the durability of the matching resistance gene. The wide occurrence of gene-for-gene systems in crop plants is most probably a result of human plant breeding activities, involving transfer and dissection of gene clusters that originate from wild species.

    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.
    Fungal (a)virulence and host resistance in the Cladosporium fulvum-tomato interaction
    Joosten, M. ; Cai, X. ; Hoorn, R. van der; Jong, C. de; Kock, M. de; Laugé, R. ; Luderer, R. ; Roth, R. ; Takken, F. ; Vossen, P. ; Weide, R. ; Westerink, N. ; Wit, P. de - \ 1999
    In: Book of abstracts : 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam, the Netherlands, 25-30 July 1999. - [S.l.] : [s.n.], 1999 - p. 11 - 11.
    The Cf-ECP2 gene is linked to, but not part of, the Cf-4/Cf-9 cluster on the short arm of chromosome 1 in tomato
    Haanstra, J.P.W. ; Laugé, R. ; Meijer-Dekens, F. ; Bonnema, G. ; Wit, P.J.G.M. de; Lindhout, P. - \ 1999
    Molecular and General Genetics 262 (1999). - ISSN 0026-8925 - p. 839 - 845.
    Perception of elicitors of Cladosporium fulvum by tomato and other solanaceous plants
    Wit, P.J.G.M. de; Joosten, M.H.A.J. ; Laugé, R. - \ 1999
    Biochimie 6 (1999)supplement. - ISSN 0300-9084 - p. s74 - s74.
    Mutation analysis of the ECP2 elicitor of Cladosporium fulvum employing the PVX expression system
    Kock, M.J.D. de; Luderer, R. ; Laugé, R. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de - \ 1999
    In: Book of abstracts : 9th International Congress on Molecular Plant-Microbe Interactions, Amsterdam, the Netherlands, 25-30 July 1999. - [S.l.] : [s.n.], 1999 - p. 119 - 119.
    Alle extracellulaire eiwitten van een pathogene schimmel worden potentieel herkend als avirulentiefactor door waard- en niet waardplanten.
    Lauge, R. ; Luderer, R. ; Vossen, P. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de - \ 1998
    Gewasbescherming 29 (1998). - ISSN 0166-6495 - p. 33 - 33.
    All extracellular proteins of a fungal pathogen are potentially recognised as avirulence factors by host and non-host plants.
    Lauge, R. ; Luderer, R. ; Vossen, P. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de - \ 1998
    In: PhD Summerschool Disease Resistance in Plants: Theory and Application, Wageningen, The Netherlands - p. 47 - 48.
    All extracellular proteins of a fungal pathogen are potentially recognised as avirulence factors by host and non-host plants.
    Lauge, R. ; Luderer, R. ; Vossen, P. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de - \ 1998
    In: 7th International Congress of Plant Pathology, Edinburgh, UK (1998) 1.1.34
    All extracellular proteins of Cladosporium fulvum are potentially recognized as avirulence factors by host and non-host plants: existence of a versatile surveillance system for defence in plants.
    Lauge, R. ; Joosten, M.H.A.J. ; Wit, P.J.G.M. de - \ 1998
    In: 5th International Workshop on Pathogenesis-Related Proteins in Plants: Signalling Pathways and Biological Activities, Aussois, France (1998) L-28
    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.
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