Staff Publications

Staff Publications

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

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    Population structure and pathotype diversity of the wheat blast pathogen Magnaporthe oryzae 25 years after its emergence in Brazil
    Nunes Maciel, J.L. ; Ceresini, P. ; Castroagudin, V.L. ; Zala, M. ; Kema, G.H.J. - \ 2014
    Phytopathology 104 (2014)1. - ISSN 0031-949X - p. 95 - 107.
    mating-type distribution - pyricularia-grisea - mycosphaerella-graminicola - genotypic diversity - fertility status - growth-stages - rice - resistance - gene - recombination
    Since its first report in Brazil in 1985, wheat blast, caused by Magnaporthe oryzae (anamorph: Pyricularia oryzae), has become increasingly important in South America, where the disease is still spreading. We used 11 microsatellite loci to elucidate the population structure of the wheat blast pathogen in wheat fields in central-western, southeastern, and southern Brazil. No subdivision was found among the wheat-infecting populations, consistent with high levels of gene flow across a large spatial scale. Although the clonal fraction was relatively high and the two mating type idiomorphs (MAT1-1 and MAT1-2) were not at similar frequencies, the clone-corrected populations from Distrito Federal and Goiás, Minas Triangle, and São Paulo were in gametic equilibrium. Based on these findings, we propose that populations of the wheat blast pathogen exhibit a mixed reproductive system in which sexual reproduction is followed by the local dispersal of clones. Seedling virulence assays with local wheat cultivars differentiated 14 pathotypes in the current population. Detached head virulence assays differentiated eight virulence groups on the same wheat cultivars. There was no correlation between seedling and head reaction
    Increased difficulties to control late blight in Tunisia are caused by a genetically diverse Phytophthora infestans population next to the clonal lineage NA-01
    Harbaoui, K. ; Hamada, W. ; Li, Y. ; Vleeshouwers, V.G.A.A. ; Lee, T.A.J. van der - \ 2014
    Plant Disease 98 (2014)7. - ISSN 0191-2917 - p. 898 - 908.
    genotypic diversity - durable resistance - potato - tomato - plant - netherlands - virulence
    In Tunisia, late blight caused by Phytophthora infestans is a serious threat to potato and tomato. The Mediterranean weather conditions can be conducive to infection in all seasons and the host crops, tomato and potato, are grown year round. Potato is planted and harvested in two to four overlapping intervals from August to June and tomato is grown both in open fields and in greenhouses. The consequences of these agricultural practices and the massive import of seed potato on the genetic variation of P. infestans are largely unknown. We conducted a survey in which 165 P. infestans isolates, collected from five subregions in Tunisia between 2006 and 2008, on which we studied genotypic diversity through nuclear (simple-sequence repeat [SSR]) markers and combined this with a previous study on their mitochondrial haplotypes (mtDNA). The phylogenetic analysis revealed the presence of a major clonal lineage (NA-01, A1 mating type, mitochondrial haplotype Ia). Isolates belonging to this clonal lineage were found in all regions and showed a relatively simple virulence pattern on a potato differential set carrying different Solanum demissum resistance genes. Apart from isolates belonging to this NA-01 clonal lineage, a group of isolates was found that showed a high genetic diversity, comprising both mating types and a more complex race structure that was found in the regions where late blight on potato was more difficult to control. The population on potato and tomato seems to be under different selection pressures. Isolates collected from tomato showed a low genetic diversity even though potato isolates collected simultaneously from the same location showed a high genetic diversity. Based on the SSR profile comparison, we could demonstrate that the four major clonal lineages found in the Netherlands and also in other European countries could not be found in Tunisia. Despite the massive import of potato seed from Europe, the P. infestans population in Tunisia was found to be clearly distinct
    Characterisation of Phytophthora infestans Isolates Collected from Potato and Tomato Crops in Tunisia During 2006–2008
    Harbaoui, K. ; Lee, T.A.J. van der; Vleeshouwers, V.G.A.A. ; Khammassy, N. ; Harrabi, M. ; Hamada, W. - \ 2013
    Potato Research 56 (2013)1. - ISSN 0014-3065 - p. 11 - 29.
    genotypic diversity - united-states - mating-type - northwestern washington - genetic-structure - populations - resistance - metalaxyl - migration - canada
    Severe late blight epidemics in Tunisia in recent years prompted population studies on the pathogen responsible for this disease, Phythophthora infestans. Characterisation of 165 Tunisian P. infestans isolates collected from 2006 to 2008 was performed for the mating type and mt haplotype, while subsets were analysed for metalaxyl sensitivity (n¿=¿65), virulence on differential set of 11 R genes of Solanum demissum (n¿=¿31), aggressiveness on cv. Bintje (n¿=¿36) and measurement of the radial growth on agar medium at three temperatures (n¿=¿38). Most isolates from potato and all isolates from tomato had the A1 mating type. The A2 mating type was detected in the north-east and northern areas, but not in the north-west. All the A2 mating type isolates were metalaxyl resistant and seem to be part of a new generation of the P. infestans isolates which are more aggressive, with more complex races, and tolerant to higher temperatures. The increased severity of epidemics during 2006 to 2008 can be attributed to favourable weather conditions during growing seasons, adaptation of new genotypes, widespread phenylamide resistance in potato production regions and most probably incorrect spray programmes. In contrast to the presence of complex pathotypes in two major potato crop regions (north-east and northern areas), the P. infestans population detected in the other regions and in tomato crops was still relatively simple. Compared with the situation in Europe and the American continent, or even compared with neighbouring countries such as Algeria, the genetic changes in Tunisia are still comforting and require strict management decision on late blight control to avoid the spread of new P. infestans populations from Europe or neighbouring countries
    Population dynamics of Phytophthora infestans in the Netherlands reveals expansion and spread of dominant clonal lineages and virulence in sexual offspring
    Li, Y. ; Lee, T.A.J. van der; Evenhuis, A. ; Bosch, G.B.M. van den; Bekkum, P.J. van; Förch, M.G. ; Gent-Pelzer, M.P.E. van; Raaij, H.M.G. van; Jacobsen, E. ; Huang, S.W. ; Govers, F. ; Vleeshouwers, V.G.A.A. ; Kessel, G.J.T. - \ 2012
    G3 : Genes Genomes Genetics 2 (2012). - ISSN 2160-1836 - p. 1529 - 1540.
    broad-spectrum resistance - genetics data-analysis - microsatellite markers - genotypic diversity - mating-type - late blight - potato - reproduction - migration - progeny
    For a comprehensive survey of the structure and dynamics of the Dutch Phytophthora infestans population, 652 P. infestans isolates were collected from commercial potato fields in the Netherlands during the 10-year period 2000–2009. Genotyping was performed using 12 highly informative microsatellite markers and mitochondrial haplotypes. In addition, for each isolate, the mating type was determined. STRUCTURE analysis grouped the 322 identified genotypes in three clusters. Cluster 1 consists of a single clonal lineage NL-001, known as “Blue_13”; all isolates in this cluster have the A2 mating type and the Ia mitochondrial haplotype. Clusters 2 and 3 display a more elaborate substructure containing many unique genotypes. In Cluster 3, several distinct clonal lineages were also identified. This survey witnesses that the Dutch population underwent dramatic changes in the 10 years under study. The most notable change was the emergence and spread of A2 mating type strain NL-001 (or “Blue_13”). The results emphasize the importance of the sexual cycle in generating genetic diversity and the importance of the asexual cycle as the propagation and dispersal mechanism for successful genotypes. Isolates were also screened for absence of the Avrblb1/ipiO class I gene, which is indicative for virulence on Rpi-blb1. This is also the first report of Rpi-blb1 breakers in the Netherlands. Superimposing the virulence screening on the SSR genetic backbone indicates that lack the Avrblb1/ipiO class I gene only occurred in sexual progeny. So far, the asexual spread of the virulent isolates identified has been limited.
    Genome Analyses of an Aggressive and Invasive Lineage of the Irish Potato Famine Pathogen
    Cooke, D.E.L. ; Cano, L.M. ; Raffaele, S. ; Bain, R.A. ; Cooke, L.R. ; Etherington, G.J. ; Deahl, K.L. ; Farrer, R.A. ; Gilroy, E.M. ; Goss, E.M. ; Grünwald, N.J. ; Hein, I. ; Maclean, D. ; McNicol, J.W. ; Randall, E. ; Oliva, R.F. ; Pel, M. ; Shaw, D.S. ; Squires, J.N. ; Taylor, M.C. ; Vleeshouwers, V.G.A.A. ; Birch, P.R.J. ; Lees, A.K. ; Kamoun, S. - \ 2012
    PLoS Pathogens 8 (2012)10. - ISSN 1553-7366
    phytophthora-infestans populations - late blight - microsatellite markers - genotypic diversity - clonal lineages - rxlr effectors - plant - resistance - expression - virulence
    Pest and pathogen losses jeopardise global food security and ever since the 19th century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics
    Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea
    Kos, M. ; Broekgaarden, C. ; Kabouw, P. ; Oude Lenferink, K. ; Poelman, E.H. ; Vet, L.E.M. ; Dicke, M. ; Loon, J.J.A. van - \ 2011
    Functional Ecology 25 (2011)5. - ISSN 0269-8463 - p. 1113 - 1124.
    glucosinolate profiles - brevicoryne-brassicae - genotypic diversity - chemical diversity - trophic cascades - communities - performance - cultivars - quality - wild
    1. Arthropod communities are structured by complex interactions between bottom-up (resource-based) and top-down (natural enemy-based) forces. Their relative importance in shaping arthropod communities, however, continues to be under debate. Bottom-up and top-down forces can be affected by intraspecific plant variation, for example by differences in concentrations of secondary metabolites that affect herbivore abundance through plant quality (bottom-up) or attract natural enemies of these herbivores (top-down). 2. Our objective was to investigate whether herbivore abundance is more strongly affected by plant-mediated bottom-up or top-down forces. 3. We used a model system of four cultivars of Brassica oleracea that show a high degree of variation in several plant traits, resistance to herbivores and attraction of natural enemies. During two field seasons, we recorded the abundance of several herbivorous and carnivorous insect species. To assess the relative importance of bottom-up and top-down forces, we quantified chemical and morphological traits of the cultivars (bottom-up) and assessed parasitization of herbivores and predator oviposition on plants inoculated with a controlled number of herbivores (top-down). 4. We show that intraspecific variation in plant chemistry and morphology consistently affects the abundance of insect herbivores and their natural enemies, resulting in cascading effects on tritrophic interactions in the associated insect community. Foliar profiles of glucosinolates and leaf toughness appeared most important for these effects. Brassica oleracea cultivars that harboured the largest numbers of herbivores also harboured the largest numbers of natural enemies. Differences in the fraction of herbivores parasitized and in predator oviposition on plants inoculated with a controlled number of herbivores could not explain the differences in natural abundance of herbivores. 5. Although abundance of herbivores is most likely influenced by a combination of bottom-up and top-down forces, it appears that in the tritrophic system investigated, bottom-up forces (plant chemistry and morphology) were more important for herbivore abundance than plant-mediated top-down forces (attraction and arrestment of natural enemies).
    Epidemiology and integrated control of Potato Late Blight in Europe
    Cooke, R.J. ; Schepers, H.T.A.M. ; Hermansen, A. ; Bain, R. ; Bradshaw, N. ; Ritchie, F. ; Shaw, D.S. ; Evenhuis, A. ; Kessel, G.J.T. ; Wander, J.G.N. ; Andersson, B. ; Hansen, J.G. ; Hannukkala, A. ; Naerstad, R. ; Nielsen, B. - \ 2011
    Potato Research 54 (2011)2. - ISSN 0014-3065 - p. 183 - 222.
    phytophthora-infestans population - a2 mating-type - genotypic diversity - northern-ireland - foliar aggressiveness - metalaxyl resistance - great-britain - r-genes - netherlands - cultivars
    Phytophthora infestans, the causal agent of late blight, is a major threat to potato production in northwestern Europe. Before 1980, the worldwide population of P. infestans outside Mexico appeared to be asexual and to consist of a single clonal lineage of A1 mating type characterized by a single genotype. It is widely believed that new strains migrated into Europe in 1976 and that this led to subsequent population changes including the introduction of the A2 mating type. The population characteristics of recently collected isolates in NW Europe show a diverse population including both mating types, sexual reproduction and oospores, although differences are observed between regions. Although it is difficult to find direct evidence that new strains are more aggressive, there are several indications from experiments and field epidemics that the aggressiveness of P. infestans has increased in the past 20 years. The relative importance of the different primary inoculum sources and specific measures for reducing their role, such as covering dumps with plastic and preventing seed tubers from becoming infected, is described for the different regions. In NW Europe, varieties with greater resistance tend not to be grown on a large scale. From the grower’s perspective, the savings in fungicide input that can be achieved with these varieties are not compensated by the higher (perceived) risk of blight. Fungicides play a crucial role in the integrated control of late blight. The spray strategies in NW Europe and a table of the specific attributes of the most important fungicides in Europe are presented. The development and use of decision support systems (DSSs) in NW Europe are described. In The Netherlands, it is estimated that almost 40% of potato growers use recommendations based on commercially available DSS. In the Nordic countries, a new DSS concept with a fixed 7-day spray interval and a variable dose rate is being tested. In the UK, commercially available DSSs are used for c. 8% of the area. The validity of Smith Periods for the new population of P. infestans in the UK is currently being evaluated.
    Clonal expansion of the Belgian Phytophthora ramorum populations based on new microsatellite markers
    Vercauteren, A. ; Dobbelaere, I. de; Grünwald, N. ; Bonants, P.J.M. ; Bockstaele, E. van; Maes, M. ; Heungens, K. - \ 2010
    Molecular Ecology 19 (2010)1. - ISSN 0962-1083 - p. 92 - 107.
    sudden oak death - fungicide resistance - genotypic diversity - 1st report - metalaxyl resistance - practical experience - ornamental plants - mating-type - infestans - pathogen
    Co-existence of both mating types A1 and A2 within the EU1 lineage of Phytophthora ramorum has only been observed in Belgium, which begs the question whether sexual reproduction is occurring. A collection of 411 Belgian P. ramorum isolates was established during a 7-year survey. Our main objectives were genetic characterization of this population to test for sexual reproduction, determination of population structure, evolution and spread, and evaluation of the effectiveness and impact of control measures. Novel, polymorphic simple sequence repeat (SSR) markers were developed after screening 149 candidate loci. Eighty isolates of P. ramorum, broadly representing the Belgian population, were analyzed using four previously described and three newly identified polymorphic microsatellite loci as well as amplified fragment length polymorphisms. SSR analysis was most informative and was used to screen the entire Belgian population. Thirty multilocus genotypes were identified, but 68% of the isolates belonged to the main genotype EU1MG1. Although accumulated mutation events were detected, the overall level of genetic diversity within the Belgian isolates of P. ramorum appears to be limited, indicating a relatively recent clonal expansion. Based on our SSR analysis there is no evidence of sexual recombination in the Belgian population of P. ramorum. Metalaxyl use decreased the genetic diversity of P. ramorum until 2005, when the majority of the isolates had become resistant. Most genotypes were site-specific and despite systematic removal of symptomatic and neighbouring plants, some genotypes were detected over a period of several years at a single site, sometimes discontinuously, indicating (latent) survival of the pathogen at those sites
    Letter to the Editor : Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum
    Grünwald, N.J. ; Goss, E.M. ; Ivors, K. ; Garbelotto, M. ; Martin, F.N. ; Prospero, S. ; Hansen, E. ; Bonants, P.J.M. ; Hamelin, R.C. ; Chastagner, M. ; Werres, S. ; Rizzo, D.M. ; Abad, G. ; Beales, P. ; Bilodeau, G.J. ; Blomquist, C.L. ; Brasier, C. ; Brière, S.C. ; Chandelier, A. ; Davidson, J.M. ; Denman, S. ; Elliott, M. ; Frankel, S.J. ; Goheen, E.M. ; Gruyter, H. de; Heungens, K. ; James, D. ; Kanaskie, A. ; McWilliams, M.G. ; Man in't Veld, W. ; Moralejo, E. ; Osterbauer, N.K. ; Palm, M.E. ; Parke, J.L. ; Perez Sierra, A.M. ; Shamoun, S.F. ; Shishkoff, N. ; Tooley, P.W. ; Vettraino, A.M. ; Webber, J. ; Widmer, T.L. - \ 2009
    Phytopathology 99 (2009)7. - ISSN 0031-949X - p. 792 - 795.
    in-vitro - north-american - european populations - genotypic diversity - dna polymorphisms - central mexico - toluca valley - united-states - infestans - california
    Phytophthora ramorum, the causal agent of sudden oak death and ramorum blight, is known to exist as three distinct clonal lineages which can only be distinguished by performing molecular marker-based analyses. However, in the recent literature there exists no consensus on naming of these lineages. Here we propose a system for naming clonal lineages of P. ramorum based on a consensus established by the P. ramorum research community. Clonal lineages are named with a two letter identifier for the continent on which they were first found (e.g., NA = North America; EU = Europe) followed by a number indicating order of appearance. Clonal lineages known to date are designated NA1 (mating type: A2; distribution: North America; environment: forest and nurseries), NA2 (A2; North America; nurseries), and EU1 (predominantly A1, rarely A2; Europe and North America; nurseries and gardens). It is expected that novel lineages or new variants within the existing three clonal lineages could in time emerge.
    Population studies on Phytophthora infestans on potatoes and tomatoes in southern Germany
    Moller, K. ; Dilger, M. ; Habermeyer, J. ; Zinkernagel, V. ; Flier, W.G. ; Hausladen, H. - \ 2009
    European Journal of Plant Pathology 124 (2009)4. - ISSN 0929-1873 - p. 659 - 672.
    genotypic diversity - mating-type - late blight - france - aggressiveness - pathogenicity - switzerland - netherlands - migrations - resistance
    Fifty-seven isolates of Phytophthora infestans from blighted potato foliage were collected in 1995 in southern Germany and analysed for mating type and sensitivity to metalaxyl. Fifty-six of them were characterised as A1 and one as A2 mating types. Resistance to metalaxyl was observed frequently: 53 isolates were resistant, three were partially sensitive, and one was sensitive. In a subsequent field study in 1999, 84 isolates collected from blighted potato and tomato foliage were analysed for mating type. Seventy-two were characterised as A1 and twelve as A2 mating types. The response of 76 isolates to metalaxyl and to propamocarb was tested. The majority (42) of the 76 isolates was classified as resistant to metalaxyl; 31 were partially sensitive and only three isolates were sensitive. The results with propamocarb were less discrete; 10 isolates were classified as resistant and three were clearly sensitive. AFLP fingerprinting was used to examine the genetic structure of the southern German P. infestans population collected in 1999 and indicated that the tested population can be sub-divided into a tomato group, a potato group and a mixed group containing isolates collected from both crops. The presence of Ia and IIa mitochondrial DNA haplotypes indicates that the German P. infestans isolates belong to the new pathogen population that has also been reported in neighbouring regions of Europe. The present study indicates that at the beginning of the season only a few genotypes were present, and the population became genetically more variable at the end of the growing season.
    Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt
    Mazurier, S. ; Corberand, T. ; Lemanceau, P. ; Raaijmakers, J.M. - \ 2009
    ISME Journal 3 (2009). - ISSN 1751-7362 - p. 977 - 991.
    black root-rot - dose-response relationships - graminis var tritici - nonpathogenic fusarium - biological-control - oxysporum fo47 - 2,4-diacetylphloroglucinol-producing pseudomonas - genotypic diversity - genetic diversity - chlororaphis pcl1391
    Natural disease-suppressive soils provide an untapped resource for the discovery of novel beneficial microorganisms and traits. For most suppressive soils, however, the consortia of microorganisms and mechanisms involved in pathogen control are unknown. To date, soil suppressiveness to Fusarium wilt disease has been ascribed to carbon and iron competition between pathogenic Fusarium oxysporum and resident non-pathogenic F. oxysporum and fluorescent pseudomonads. In this study, the role of bacterial antibiosis in Fusarium wilt suppressiveness was assessed by comparing the densities, diversity and activity of fluorescent Pseudomonas species producing 2,4-diacetylphloroglucinol (DAPG) (phlD+) or phenazine (phzC+) antibiotics. The frequencies of phlD+ populations were similar in the suppressive and conducive soils but their genotypic diversity differed significantly. However, phlD genotypes from the two soils were equally effective in suppressing Fusarium wilt, either alone or in combination with non-pathogenic F. oxysporum strain Fo47. A mutant deficient in DAPG production provided a similar level of control as its parental strain, suggesting that this antibiotic does not play a major role. In contrast, phzC+ pseudomonads were only detected in the suppressive soil. Representative phzC+ isolates of five distinct genotypes did not suppress Fusarium wilt on their own, but acted synergistically in combination with strain Fo47. This increased level of disease suppression was ascribed to phenazine production as the phenazine-deficient mutant was not effective. These results suggest, for the first time, that redox-active phenazines produced by fluorescent pseudomonads contribute to the natural soil suppressiveness to Fusarium wilt disease and may act in synergy with carbon competition by resident non-pathogenic F. oxysporum.
    Genetic structure and pathogenicity of populations of Phytophthora infestans from organic potato crops in France, Norway, Switzerland and the United Kingdom
    Flier, W.G. ; Kroon, L.P.N.M. ; Hermansen, A. ; Raaij, H.M.G. van; Speiser, B. ; Tamm, L. ; Fuchs, J.G. ; Lambion, J. ; Razzaghian, J. ; Andrivon, D. ; Wilcockson, S. ; Leifert, C. - \ 2007
    Plant Pathology 56 (2007)4. - ISSN 0032-0862 - p. 562 - 572.
    late blight - genotypic diversity - foliar aggressiveness - toluca valley - mating-type - resistance - cultivars - netherlands - inoculum - finland
    Genetic variation and pathogenicity of Pbytophthora infestans isolates collected from organic potato crops of the susceptible cv. Bintje and the moderately resistant cv. Sante were assessed in France, Norway, and the United Kingdom in 2001 and in Switzerland in 2001 and 2002. Population structures differed considerably between the four P. infestans populations. Those from France, Switzerland and the UK were mainly clonal populations showing restricted levels of genetic diversity, whilst those from Norway were mixed A1 and A2 mating type populations with high levels of genetic diversity, suggesting periodical sexual reproduction. Isolates collected from cv. Bintje were on average more aggressive than or comparable to isolates from cv. Sante. Race complexity varied considerably between the regional P. infestans populations, with isolates from France and Switzerland showing the highest number of virulence factors. In all pathogen samples but the French, isolates collected from cv. Sante were more complex than isolates collected from cv. Bintje. No directional selection towards increased aggressiveness towards the more resistant cultivar Sante was observed. This suggests that there is no shift towards increased levels of pathogenicity in P. infestans populations following the large-scale introduction of more resistant potato varieties in organic production systems in Europe.
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