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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    Data presented in the PhD thesis "Cucumber Mildew Resistance Identification of Cucumber Genes Involved in Susceptibility and Resistance to Powdery and Downy Mildew"
    Berg, J.A. - \ 2019
    Wageningen University & Research
    cucumber - downy mildew - plant-pathogen interactions - powdery mildew - susceptibility genes
    The aims of this thesis were to identify genes involved in cucumber-mildew interactions, in order to better understand these pathosystems, thus providing new leads for the breeding of mildew resistant cucumbers. As resistances against both PM and DM were previously shown to be usually recessive, special attention is given to the concept of susceptibility genes (S genes), loss-of-function alleles of which can contribute to effective and durable resistance.
    Natural loss-of-function mutation of EDR1 conferring resistance to tomato powdery mildew in Arabidopsis thaliana accession C24
    Gao, D. ; Appiano, M. ; Huibers, R.P. ; Loonen, A.E.H.M. ; Visser, R.G.F. ; Wolters, A.M.A. ; Bai, Y. - \ 2015
    Molecular Plant Pathology 16 (2015)1. - ISSN 1464-6722 - p. 71 - 82.
    salicylic-acid - downy mildew - gene - defense - plants - microsatellites - mechanism - evolution - cloning - kinase
    To screen for potentially novel types of resistance to tomato powdery mildew Oidium neolycopersici, a disease assay was performed on 123 Arabidopsis thaliana accessions. Forty accessions were fully resistant, and one, C24, was analysed in detail. By quantitative trait locus (QTL) analysis of an F2 population derived from C24 × Sha (susceptible accession), two QTLs associated with resistance were identified in C24. Fine mapping of QTL-1 on chromosome 1 delimited the region to an interval of 58¿kb encompassing 15 candidate genes. One of these was Enhanced Disease Resistance 1 (EDR1). Evaluation of the previously obtained edr1 mutant of Arabidopsis accession Col-0, which was identified because of its resistance to powdery mildew Golovinomyces cichoracearum, showed that it also displayed resistance to O.¿neolycopersici. Sequencing of EDR1 in our C24 germplasm (referred to as C24-W) revealed two missing nucleotides in the second exon of EDR1 resulting in a premature stop codon. Remarkably, C24 obtained from other laboratories does not contain the EDR1 mutation. To verify the identity of C24-W, a DNA region containing a single nucleotide polymorphism (SNP) unique to C24 was sequenced showing that C24-W contains the C24-specific nucleotide. C24-W showed enhanced resistance to O.¿neolycopersici compared with C24 not containing the edr1 mutation. Furthermore, C24-W displayed a dwarf phenotype, which was not associated with the mutation in EDR1 and was not caused by the differential accumulation of pathogenesis-related genes. In conclusion, we identified a natural edr1 mutant in the background of C24.
    A mixed-model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce
    Wei, Z. ; Julkowska, M.M. ; Laloe, J.O. ; Hartman, Y. ; Boer, G.J. ; Michelmore, R.W. ; Tienderen, P.H. van; Testerink, C. ; Schranz, M.E. - \ 2014
    Molecular Breeding 34 (2014)3. - ISSN 1380-3743 - p. 1389 - 1400.
    quantitative trait loci - root-system architecture - salinity tolerance - high-density - plant-root - nonhost resistance - lactuca-saligna - downy mildew - linkage maps - bread wheat
    Cultivated lettuce is more sensitive to salinity stress than its wild progenitor species potentially due to differences in root architecture and/or differential uptake and accumulation of sodium. We have identified quantitative trait locis (QTLs) associated with salt-induced changes in root system architecture (RSA) and ion accumulation using a recombinant inbred line population derived from a cross between cultivated lettuce (Lactuca sativa ‘Salinas’) and wild lettuce (L. serriola). Components of RSA were quantified by replicated measurements of seedling growth on vertical agar plates containing different concentrations of NaCl in a controlled growth chamber environment. Accumulation of sodium and potassium ions was measured in replicates of greenhouse-grown plants watered with 100 mM NaCl water. A total of 14 QTLs were identified using multi-trait linkage analysis, including three major QTLs associated with general root development, root growth in salt stress condition, and ion accumulation. The three major QTLs, qRC9.1, qRS2.1, and qLS7.2, were linked with markers E35/M59-F-425, LE9050, and LE1053, respectively. This study provides regions of lettuce genome contributing to salt-induced changes in RSA and ion accumulation. Future fine-mapping of major QTLs will identify candidate genes underlying salt stress tolerance in cultivated lettuce.
    Seed and leaf treatments with natural compounds to induce resistance against Peronospora parasitica in Brassica oleracea
    Wolf, J.M. van der; Michta, A. ; Zouwen, P.S. van der; Boer, W.J. de; Davelaar, E. ; Stevens, L.H. - \ 2012
    Crop Protection 35 (2012). - ISSN 0261-2194 - p. 78 - 84.
    systemic acquired-resistance - induced disease resistance - defense responses - fusarium-wilt - downy mildew - damping-off - plants - protection - cucumber - growth
    Seed and leaf treatments with natural compounds having a low risk profile (LRP) were evaluated for their potential to induce resistance in cabbage plants (Brassica oleracea) against Peronospora parasitica, causal organism of downy mildew. The selection of 34 LRP compounds comprised micronutrients, organic compounds such as proline, riboflavin, oligogalacturonides, aminolignosulfonates, bacterial lipopolysaccharides, and bacterial and fungal extracts. Treatments with the synthetic chemical inducers 2,6-dichloroisonicotinic acid (INA), d,l-ß-aminobutyric acid, salicylic acid, benzothiadiazole and the fungicide Previcur™ were included as controls. After seed treatment a maximum reduction of 27% diseased leaf area was found with an extract of a Lysobacter strain, compared to a reduction of 99% for INA, the most effective synthetic inducer. Seed treatments with extracts of Pectobacterium carotovorum subsp. carotovorum, Bacillus macerans, Pseudomonas syringae, Streptomyces and Xanthomonas campestris strains also reduced downy mildew infection significantly. After leaf treatment, a maximum reduction of 85% was again found with the Lysobacter extract, compared to a reduction of 99% for INA, the most effective synthetic inducer. Leaf treatments with CuSO4 (=1 mM), MnCl2 (=10 mM), K2HPO4 (100 mM), and extracts of P. syringae, P. carotovorum subsp. carotovorum, Streptomyces, X. campestris and B. macerans strains also reduced the diseased leaf area, but CuSO4 was highly phytotoxic. For seed and leaf treatments with Lysobacter extract, proline, MnCl2 and INA the effect on the induction of chitinase and glucanase activity was tested, using two pathogenesis-related proteins as markers for induced resistance. For seed treatments only INA and for leaf treatments INA, proline and MnCl2 treatments resulted in increased activity of both enzymes. The rate of enzyme activity induced by INA was dependent on the time seeds were exposed to the compound. Highlights ¿ Seed treatments with isonicotinic acid protects Brassica seedlings from Peronospora infections. ¿ Treatments of seedlings with extracts of Lysobacter protects against Peronospora infections. ¿ Effect of seed treatments is dependent on the time of incubation with the elicitor
    Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants
    Gilroy, E.M. ; Breen, S. ; Whisson, S.C. ; Squires, J. ; Hein, I. ; Kaczmarek, M. ; Turnbull, D. ; Boevink, P.C. ; Lokossou, A.A. ; Cano, L.M. ; Morales, J. ; Avrova, A.O. ; Pritchard, L. ; Randall, E. ; Lees, A. ; Govers, F. ; West, P. van; Kamoun, S. ; Vleeshouwers, V.G.A.A. ; Cooke, D.E.L. ; Birch, P.R.J. - \ 2011
    New Phytologist 191 (2011)3. - ISSN 0028-646X - p. 763 - 776.
    rxlr effectors - pathogen phytophthora - disease resistance - oomycete effectors - avirulence genes - downy mildew - potato - locus - avr3a - protein
    # A detailed molecular understanding of how oomycete plant pathogens evade disease resistance is essential to inform the deployment of durable resistance (R) genes. # • Map-based cloning, transient expression in planta, pathogen transformation and DNA sequence variation across diverse isolates were used to identify and characterize PiAVR2 from potato late blight pathogen Phytophthora infestans. # • PiAVR2 is an RXLR-EER effector that is up-regulated during infection, accumulates at the site of haustoria formation, and is recognized inside host cells by potato protein R2. Expression of PiAVR2 in a virulent P. infestans isolate conveys a gain-of-avirulence phenotype, indicating that this is a dominant gene triggering R2-dependent disease resistance. PiAVR2 presence/absence polymorphisms and differential transcription explain virulence on R2 plants. Isolates infecting R2 plants express PiAVR2-like, which evades recognition by R2. PiAVR2 and PiAVR2-like differ in 13 amino acids, eight of which are in the C-terminal effector domain; one or more of these determines recognition by R2. Nevertheless, few polymorphisms were observed within each gene in pathogen isolates, suggesting limited selection pressure for change within PiAVR2 and PiAVR2-like. # • Our results direct a search for R genes recognizing PiAVR2-like, which, deployed with R2, may exert strong selection pressure against the P. infestans population.
    Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome
    Baxter, L. ; Tripathy, S. ; Ishaque, N. ; Boot, N. ; Cabral, A. ; Kemen, E. ; Thines, M. ; Ah-Fong, A. ; Anderson, R. ; Badejoko, W. ; Bittner-Eddy, P. ; Boore, J.L. ; Chibucos, M.C. ; Coates, M. ; Dehal, P. ; Delehaunty, K. ; Dong, S. ; Downton, P. ; Dumas, B. ; Fabro, G. ; Fronick, C. ; Fuerstenberg, S.I. ; Fulton, L. ; Gaulin, E. ; Govers, F. ; Hughes, L. ; Humphray, S. ; Jiang, R.H.Y. ; Judelson, H. ; Kamoun, S. ; Kyung, K. ; Meijer, H.J.G. ; Minx, P. ; Morris, P. ; Nelson, J. ; Phuntumart, V. ; Qutob, D. ; Rehmany, A. ; Rougon-Cardoso, A. ; Ryden, P. ; Torto-Alalibo, T. ; Studholme, D. ; Wang, Y. ; Win, J. ; Wood, J. ; Clifton, S.W. ; Rogers, J. ; Ackerveken, G. van den; Jones, J.D.G. ; McDowell, J.M. ; Beynon, J. ; Tyler, B.M. - \ 2010
    Science 330 (2010)6010. - ISSN 0036-8075 - p. 1549 - 1551.
    sojae-effector avr1b - downy mildew - phytophthora - plant - thaliana - cells - suppression - parasites - proteins - delivery
    Many oomycete and fungal plant pathogens are obligate biotrophs, which extract nutrients only from living plant tissue and cannot grow apart from their hosts. Although these pathogens cause substantial crop losses, little is known about the molecular basis or evolution of obligate biotrophy. Here, we report the genome sequence of the oomycete Hyaloperonospora arabidopsidis (Hpa), an obligate biotroph and natural pathogen of Arabidopsis thaliana. In comparison with genomes of related, hemibiotrophic Phytophthora species, the Hpa genome exhibits dramatic reductions in genes encoding (i) RXLR effectors and other secreted pathogenicity proteins, (ii) enzymes for assimilation of inorganic nitrogen and sulfur, and (iii) proteins associated with zoospore formation and motility. These attributes comprise a genomic signature of evolution toward obligate biotrophy
    Rin4 Causes Hybrid Necrosis and Race-Specific Resistance in an Interspecific Lettuce Hybrid
    Jeuken, M.J.W. ; Zhang, N. ; McHale, L.K. ; Pelgrom, K.T.B. ; Boer, E. den; Lindhout, P. ; Michelmore, R. ; Visser, R.G.F. ; Niks, R.E. - \ 2009
    The Plant Cell 21 (2009)10. - ISSN 1040-4651 - p. 3368 - 3378.
    cf-2-dependent disease resistance - backcross inbred lines - lactuca-saligna - bremia-lactucae - nonhost resistance - effector avrrpt2 - gene-expression - downy mildew - wild lettuce - arabidopsis
    Some inter- and intraspecific crosses may result in reduced viability or sterility in the offspring, often due to genetic incompatibilities resulting from interactions between two or more loci. Hybrid necrosis is a postzygotic genetic incompatibility that is phenotypically manifested as necrotic lesions on the plant. We observed hybrid necrosis in interspecific lettuce (Lactuca sativa and Lactuca saligna) hybrids that correlated with resistance to downy mildew. Segregation analysis revealed a specific allelic combination at two interacting loci to be responsible. The allelic interaction had two consequences: (1) a quantitative temperature-dependent autoimmunity reaction leading to necrotic lesions, lethality, and quantitative resistance to an otherwise virulent race of Bremia lactucae; and (2) a qualitative temperature-independent race-specific resistance to an avirulent race of B. lactucae. We demonstrated by transient expression and silencing experiments that one of the two interacting genes was Rin4. In Arabidopsis thaliana, RIN4 is known to interact with multiple R gene products, and their interactions result in hypersensitive resistance to Pseudomonas syringae. Site-directed mutation studies on the necrosis-eliciting allele of Rin4 in lettuce showed that three residues were critical for hybrid necrosis
    The Cyst Nematode SPRYSEC Protein RBP-1 Elicits Gpa2- and RanGAP2-Dependent Plant Cell Death
    Sacco, M.A. ; Koropacka, K.B. ; Grenier, E. ; Jaubert, M.J. ; Blanchard, A. ; Goverse, A. ; Smant, G. ; Moffett, P. - \ 2009
    PLoS Pathogens 5 (2009)8. - ISSN 1553-7366
    disease resistance genes - rich repeat protein - nb-lrr protein - globodera-pallida - downy mildew - sequence alignment - avirulence genes - virus-resistance - potato - arabidopsis
    Plant NB-LRR proteins confer robust protection against microbes and metazoan parasites by recognizing pathogen-derived avirulence (Avr) proteins that are delivered to the host cytoplasm. Microbial Avr proteins usually function as virulence factors in compatible interactions; however, little is known about the types of metazoan proteins recognized by NB-LRR proteins and their relationship with virulence. In this report, we demonstrate that the secreted protein RBP-1 from the potato cyst nematode Globodera pallida elicits defense responses, including cell death typical of a hypersensitive response (HR), through the NB-LRR protein Gpa2. Gp-Rbp-1 variants from G. pallida populations both virulent and avirulent to Gpa2 demonstrated a high degree of polymorphism, with positive selection detected at numerous sites. All Gp-RBP-1 protein variants from an avirulent population were recognized by Gpa2, whereas virulent populations possessed Gp-RBP-1 protein variants both recognized and non-recognized by Gpa2. Recognition of Gp-RBP-1 by Gpa2 correlated to a single amino acid polymorphism at position 187 in the Gp-RBP-1 SPRY domain. Gp-RBP-1 expressed from Potato virus X elicited Gpa2-mediated defenses that required Ran GTPase-activating protein 2 (RanGAP2), a protein known to interact with the Gpa2 N terminus. Tethering RanGAP2 and Gp-RBP-1 variants via fusion proteins resulted in an enhancement of Gpa2-mediated responses. However, activation of Gpa2 was still dependent on the recognition specificity conferred by amino acid 187 and the Gpa2 LRR domain. These results suggest a two-tiered process wherein RanGAP2 mediates an initial interaction with pathogen-delivered Gp-RBP-1 proteins but where the Gpa2 LRR determines which of these interactions will be productive
    Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato
    Champouret, N. ; Bouwmeester, K. ; Rietman, H. ; Lee, T. van der; Maliepaard, C.A. ; Heupink, A. ; Vondervoort, P.J.I. van de; Jacobsen, E. ; Visser, R.G.F. ; Vossen, E.A.G. van der; Govers, F. ; Vleeshouwers, V.G.A.A. - \ 2009
    Molecular Plant-Microbe Interactions 22 (2009)12. - ISSN 0894-0282 - p. 1535 - 1545.
    late blight resistance - mediated plant transformation - broad-spectrum resistance - nevado-de-toluca - solanum-bulbocastanum - central mexico - downy mildew - cell-death - population-structure - cultivated potato
    A strategy to control the devastating late blight disease is providing potato cultivars with genes that are effective in resistance to a broad spectrum of Phytophthora infestans isolates. Thus far, most late blight resistance (R) genes that were introgressed in potato were quickly defeated. In contrast, the Rpi-blb1 gene originating from Solanum bulbocastanum has performed as an exclusive broad-spectrum R gene for many years. Recently, the RXLR effector family ipiO was identified to contain Avr-blb1. Monitoring the genetic diversity of the ipiO family in a large set of isolates of P. infestans and related species resulted in 16 ipiO variants in three distinct classes. Class I and class II but not class III ipiO variants induce cell death when coinfiltrated with Rpi-blb1 in Nicotiana benthamiana. Class I is highly diverse and is represented in all analyzed P. infestans isolates except two Mexican P. infestans isolates, and these were found virulent on Rpi-blb1 plants. In its C-terminal domain, IPI-O contains a W motif that is essential for triggering Rpi-blb1-mediated cell death and is under positive selection. This study shows that profiling the variation of Avr-blb1 within a P. infestans population is instrumental for predicting the effectiveness of Rpi-blb1-mediated resistance in potato.
    Differential recognition of Phytophthora infestans races in potato R4 breeding lines
    Poppel, P.M.J.A. van; Huigen, D.J. ; Govers, F. - \ 2009
    Phytopathology 99 (2009)10. - ISSN 0031-949X - p. 1150 - 1155.
    blight resistance - disease resistance - avirulence genes - downy mildew - virulence - effector - inheritance - markers - locus - specificities
    Introgression breeding has resulted in several potato lines that are resistant to late blight, a devastating plant disease caused by the oomycete Phytophthora infestans. The traditional differential set consists of potato lines with 11 late blight resistance specificities, referred to as R1 to R11. With the exception of the R4 locus, all the resistance loci in these lines have been genetically mapped or positioned in resistance (R) gene clusters. In this study, we show that potato lines that are defined to carry R4 do not necessarily recognize the same P. infestans strains. Field isolates appeared to be avirulent on either the R4 differential developed by Mastenbroek or the one developed by Black but not on both. Previously, we identified the avirulence gene PiAvr4, which is a member of the RXLR effector family. In planta expression of PiAvr4 revealed that recognition of PiAvr4 is strictly confined to the Mastenbroek R4 differential. Segregation of the trait in two independent F1 progenies showed that late blight resistance in this differential is determined by a single dominant gene, now referred to as R4Ma.
    Recognition of Phytophthora infestans Avr4 by potato R4 is triggered by C-terminal domains comprising W motifs
    Poppel, P.M.J.A. van; Jiang, R.H.Y. ; Sliwka, J. ; Govers, F. - \ 2009
    Molecular Plant Pathology 10 (2009)5. - ISSN 1464-6722 - p. 611 - 620.
    sojae-effector avr1b - avirulence gene - downy mildew - cell-death - arabidopsis - resistance - proteins - expression - origin - blight
    Oomycete RXLR-dEER effector proteins are rapidly evolving proteins with the selective pressure targeted predominantly at their C-terminal ends. The majority of RXLR-dEER proteins have recognizable motifs of 21-30 amino acids in the C-terminal domain that are named after conserved amino acid residues at fixed positions within the respective motifs. In this article, it is reported that the Phytophthora infestans RXLR-dEER protein Avr4 contains three W motifs and one Y motif in its C-terminal domain. Agroinfection assays using constructs encoding modified forms of PiAvr4 have shown that the region containing the W2 motif, in combination with either the W1 or W3 motif, triggers a necrotic response in potato plants carrying the resistance gene R4. By mining the superfamily of avirulence homologues (Avh) deduced from three sequenced Phytophthora genomes, several Avh proteins were identified as homologues of PiAvr4: six in P. infestans, one in P. ramorum and seven in P. sojae. One very close homologue of PiAvr4 was cloned from the sibling species, P. mirabilis. This species is not pathogenic on potato but, similar to PiAvr4, PmirAvh4 triggered a necrotic response on potato clones carrying R4, but not on clones lacking R4. Genes encoding RXLR-dEER effectors are often located in regions showing genome rearrangements. Alignment of the genomic region harbouring PiAvr4 with syntenic regions in P. sojae and P. ramorum revealed that PiAvr4 is located on a 100-kb indel block and is surrounded by transposable elements.
    Exploiting Knowledge of R/Avr Genes to Rapidly Clone a New LZ-NBS-LRR Family of Late Blight Resistance Genes from Potato Linkage Group IV
    Lokossou, A.A. ; Park, T.H. ; Arkel, G. van; Arens, M.J.B. ; Ruyter-Spira, C.P. ; Morales, J. ; Whisson, S.C. ; Birch, P.R.J. ; Visser, R.G.F. ; Jacobsen, E. ; Vossen, E.A.G. van der - \ 2009
    Molecular Plant-Microbe Interactions 22 (2009)6. - ISSN 0894-0282 - p. 630 - 641.
    phytophthora-infestans mont - broad-spectrum resistance - plant immune-system - disease resistance - solanum-bulbocastanum - downy mildew - r-gene - quantitative resistance - arabidopsis-thaliana - oomycete effectors
    In addition to the resistance to Phytophthora infestans (Rpi) genes Rpi-blb1 and Rpi-blb2, Solanum bulbocastanum appears to harbor Rpi-blb3 located at a major late blight resistance locus on LG IV, which also harbors Rpi-abpt, R2, R2-like, and Rpi-mcd1 in other Solanum spp. Here, we report the cloning and functional analyses of four Rpi genes, using a map-based cloning approach, allele-mining strategy, Gateway technology, and transient complementation assays in Nicotiana benthamiana. Rpi-blb3, Rpi-abpt, R2, and R2-like contain all signature sequences characteristic of leucine zipper nucleotide binding site leucine-rich repeat (LZ-NBS-LRR) proteins, and share amino-acid sequences 34.9% similar to RPP13 from Arabidopsis thaliana. The LRR domains of all four Rpi proteins are highly homologous whereas LZ and NBS domains are more polymorphic, those of R2 being the most divergent. Clear blocks of sequence affiliation between the four functional resistance proteins and those encoded by additional Rpi-blb3 gene homologs suggest exchange of LZ, NBS, and LRR domains, underlining the modular nature of these proteins. All four Rpi genes recognize the recently identified RXLR effector PiAVR2
    The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector
    Poppel, P.M.J.A. van; Jun Guo, J. ; Vondervoort, P.J.I. van de; Jung, M.W.M. ; Birch, P.R.J. ; Whisson, S.C. ; Govers, F. - \ 2008
    Molecular Plant-Microbe Interactions 21 (2008)11. - ISSN 0894-0282 - p. 1460 - 1470.
    broad-spectrum resistance - late blight resistance - host-plant cells - solanum-bulbocastanum - downy mildew - pathogen phytophthora - secreted proteins - innate immunity - powdery mildew - ipio gene
    Resistance in potato against the oomycete Phytophthora infestans is conditioned by resistance (R) genes that are introgressed from wild Solanum spp. into cultivated potato. According to the gene-for-gene model, proteins encoded by R genes recognize race-specific effectors resulting in a hypersensitive response (HR). We isolated P. infestans avirulence gene PiAvr4 using a combined approach of genetic mapping, transcriptional profiling, and bacterial artificial chromosome marker landing. PiAvr4 encodes a 287-amino-acid-protein that belongs to a superfamily of effectors sharing the putative host-cell-targeting motif RXLR-dEER. Transformation of P. infestans race 4 strains with PiAvr4 resulted in transformants that were avirulent on R4 potato plants, demonstrating that PiAvr4 is responsible for eliciting R4-mediated resistance. Moreover, expression of PiAvr4 in R4 plants using PVX agroinfection and agroinfiltration showed that PiAvr4 itself is the effector that elicits HR on R4 but not r0 plants. The presence of the RXLR-dEER motif suggested intracellular recognition of PiAvr4. This was confirmed in agroinfiltration assays but not with PVX agroinfection. Because there was always recognition of PiAvr4 retaining the signal peptide, extracellular recognition cannot be excluded. Deletion of the RXLR-dEER domain neither stimulated nor prevented elicitor activity of PiAvr4. Race 4 strains have frame shift mutations in PiAvr4 that result in truncated peptides; hence, PiAvr4 is apparently not crucial for virulence.
    RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members
    Jiang, R.H.Y. ; Tripathy, S. ; Govers, F. ; Tyler, B.M. - \ 2008
    Proceedings of the National Academy of Sciences of the United States of America 105 (2008)12. - ISSN 0027-8424 - p. 4874 - 4879.
    amino-acid sites - proteins reveals - downy mildew - avirulence - selection - genes - recognition - arabidopsis - virulence - secretome
    Pathogens secrete effector molecules that facilitate the infection of their hosts. A number of effectors identified in plant pathogenic Phytophthora species possess N-terminal motifs (RXLR-dEER) required for targeting these effectors into host cells. Here, we bioinformatically identify >370 candidate effector genes in each of the genomes of P. sojae and P. ramorum. A single superfamily, termed avirulence homolog (Avh) genes, accounts for most of the effectors. The Avh proteins show extensive sequence divergence but are all related and likely evolved from a common ancestor by rapid duplication and divergence. More than half of the Avh proteins contain conserved C-terminal motifs (termed W, Y, and L) that are usually arranged as a module that can be repeated up to eight times. The Avh genes belong to the most rapidly evolving part of the genome, and they are nearly always located at synteny breakpoints. The superfamily includes all experimentally identified oomycete effector and avirulence genes, and its rapid pace of evolution is consistent with a role for Avh proteins in interaction with plant hosts
    Conserved C-Terminal Motifs Required for Avirulence and Suppression of Cell Death by Phytophthora sojae effector Avr1b
    Dou, D. ; Kale, S.D. ; Wang, X. ; Chen, Y. ; Wang, Q. ; Jiang, R.H.Y. ; Arredondo, F.D. ; Anderson, R.G. ; Thakur, P.B. ; McDowell, J.M. ; Wang, Y. ; Tyler, B.M. - \ 2008
    The Plant Cell 20 (2008). - ISSN 1040-4651 - p. 1118 - 1133.
    broad-spectrum resistance - plant-disease-resistance - nucleotide-binding-site - late blight resistance - host-targeting signal - e3 ubiquitin ligase - phytopathogenic bacteria - solanum-bulbocastanum - innate immunity - downy mildew
    The sequenced genomes of oomycete plant pathogens contain large superfamilies of effector proteins containing the protein translocation motif RXLR-dEER. However, the contributions of these effectors to pathogenicity remain poorly understood. Here, we show that the Phytophthora sojae effector protein Avr1b can contribute positively to virulence and can suppress programmed cell death (PCD) triggered by the mouse BAX protein in yeast, soybean (Glycine max), and Nicotiana benthamiana cells. We identify three conserved motifs (K, W, and Y) in the C terminus of the Avr1b protein and show that mutations in the conserved residues of the W and Y motifs reduce or abolish the ability of Avr1b to suppress PCD and also abolish the avirulence interaction of Avr1b with the Rps1b resistance gene in soybean. W and Y motifs are present in at least half of the identified oomycete RXLR-dEER effector candidates, and we show that three of these candidates also suppress PCD in soybean. Together, these results indicate that the W and Y motifs are critical for the interaction of Avr1b with host plant target proteins and support the hypothesis that these motifs are critical for the functions of the very large number of predicted oomycete effectors that contain them
    Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution
    Stergiopoulos, I. ; Kock, M.J.D. de; Lindhout, P. ; Wit, P.J.G.M. de - \ 2007
    Molecular Plant-Microbe Interactions 20 (2007)10. - ISSN 0894-0282 - p. 1271 - 1283.
    amino-acid sites - cf-2-dependent disease resistance - avirulence gene - plant-pathogen - cf-4-mediated resistance - extracellular proteins - positive selection - virulence factor - fungal pathogen - downy mildew
    The allelic variation in four avirulence (Avr) and four extracellular protein (Ecp)¿encoding genes of the tomato pathogen Cladosporium fulvum was analyzed for a worldwide collection of strains. The majority of polymorphisms observed in the Avr genes are deletions, point mutations, or insertions of transposon-like elements that are associated with transitions from avirulence to virulence, indicating adaptive evolution of the Avr genes to the cognate C. fulvum resistance genes that are deployed in commercial tomato lines. Large differences in types of polymorphisms between the Avr genes were observed, especially between Avr2 (indels) and Avr4 (amino-acid substitutions), indicating that selection pressure favors different types of adaptation. In contrast, only a limited number of polymorphisms were observed in the Ecp genes, which mostly involved synonymous modifications. A haplotype network based on the polymorphisms observed in the effector genes revealed a complex pattern of evolution marked by reticulations that suggests the occurrence of genetic recombination in this presumed asexual fungus. This, as well as the identification of strains with identical polymorphisms in Avr and Ecp genes but with opposite mating-type genes, suggests that development of complex races can be the combined result of positive selection and genetic recombination.
    Phytophthora genomics: the plant destroyers' genome decoded
    Govers, F. ; Gijzen, M. - \ 2006
    Molecular Plant-Microbe Interactions 19 (2006)12. - ISSN 0894-0282 - p. 1295 - 1301.
    pathogen phytophthora - oomycete pathogen - saprolegnia-parasitica - microsatellite markers - expressed sequences - downy mildew - infestans - sojae - avirulence - ramorum
    The year 2004 was an exciting one for the Phytophthora research community. The United States Department of Energy Joint Genome Institute (JGI) completed the draft genome sequence of two Phytophthora species, Phytophthora sojae and Phytophthora ramorum. In August of that year over 50 people gathered at JGI in Walnut Creek, California, for an annotation jamboree and searched for the secrets and surprises that the two genomes have in petto. This culminated in a paper in Science in September of this year describing the highlights of the sequencing project and emphasizing the power of having the genome sequences of two closely related organisms. This MPMI Focus issue on Phytophthora genomics contains a number of more specialized manuscripts centered on gene annotation and genome organization, and complemented with manuscripts that rely on genomics resources
    Comparative analysis of Phytophthora genes encoding secreted proteins reveals conserved synteny and lineage-specific gene duplications and deletions
    Jiang, R.H.Y. ; Tyler, B.M. ; Govers, F. - \ 2006
    Molecular Plant-Microbe Interactions 19 (2006)12. - ISSN 0894-0282 - p. 1311 - 1321.
    pathogen phytophthora - comparative genomics - cladosporium-fulvum - magnaporthe-grisea - effector proteins - downy mildew - resistance - avirulence - elicitor - locus
    Comparative analysis of two Phytophthora genomes revealed overall colinearity in four genomic regions consisting of a 1.5-Mb sequence of Phytophthora sojae and a 0.9-Mb sequence of R ramorum. In these regions with conserved synteny, the gene order is largely similar; however, genome rearrangements also have occurred. Deletions and duplications often were found in association with genes encoding secreted proteins, including effectors that are important for interaction with host plants. Among secreted protein genes, different evolutionary patterns were found. Elicitin genes that code for a complex family of highly conserved Phytophthora-specific elicitors show conservation in gene number and order, and often are clustered. In contrast, the race-specific elicitor gene Avr1b-1 appeared to be missing from the region with conserved synteny, as were its five homologs that are scattered over the four genomic regions. Some gene families encoding secreted proteins were found to be expanded in one species compared with the other. This could be the result of either repeated gene duplications in one species or specific deletions in the other. These different evolutionary patterns may shed light on the functions of these secreted proteins in the biology and pathology of the two Phytophthora spp.
    Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis
    Tyler, B.M. ; Tripathy, S. ; Zhang, X. ; Dehal, P. ; Jiang, R.H.Y. ; Aerts, A. ; Arredondo, F.D. ; Baxter, L. ; Bensasson, D. ; Beynon, J.L. ; Chapman, J. ; Damasceno, C.M.B. ; Dorrance, A.E. ; Dou, D. ; Dickerman, A.W. ; Dubchak, I.L. ; Garbelotto, M. ; Gijzen, M. ; Gordon, S.G. ; Govers, F. ; Grunwald, N.J. ; Huang, W. ; Ivors, K.L. ; Jones, R.W. ; Kamoun, S. ; Krampis, K. ; Lamour, K.H. ; Lee, M.K. ; McDonald, W.H. ; Medina, M. ; Meijer, H.J.G. ; Nordberg, E.K. ; Maclean, D.J. ; Ospina-Giraldo, M.D. ; Morris, P.F. ; Phuntumart, V. ; Putnam, N.H. ; Rash, S. ; Rose, J.K.C. ; Sakihama, Y. ; Salamov, A.A. ; Savidor, A. ; Scheuring, C.F. ; Smith, B.M. ; Sobral, B.W.S. ; Terry, A. ; Torto-Alalibo, T.A. ; Win, J. ; Xu, Z. ; Zhang, H. ; Grigoriev, I.V. ; Rokhsar, D.S. ; Boore, J.L. - \ 2006
    Science 313 (2006)5791. - ISSN 0036-8075 - p. 1261 - 1266.
    effector proteins - downy mildew - resistance - arabidopsis - avirulence - genes - locus - sojae - expression - virulence
    Draft genome sequences have been determined for the soybean pathogen Phytophthora sojae and the sudden oak death pathogen Phytophthora ramorum. Oömycetes such as these Phytophthora species share the kingdom Stramenopila with photosynthetic algae such as diatoms, and the presence of many Phytophthora genes of probable phototroph origin supports a photosynthetic ancestry for the stramenopiles. Comparison of the two species' genomes reveals a rapid expansion and diversification of many protein families associated with plant infection such as hydrolases, ABC transporters, protein toxins, proteinase inhibitors, and, in particular, a superfamily of 700 proteins with similarity to known oömycete avirulence genes
    A cDNA-AFLP based strategy to identify transcripts associated with avirulence in Phytophthora infestans
    Jun Guo, J. ; Jiang, R.H.Y. ; Kamphuis, L.G. ; Govers, F. - \ 2006
    Fungal Genetics and Biology 43 (2006)2. - ISSN 1087-1845 - p. 111 - 123.
    bulked segregant analysis - disease-resistance - plant defense - downy mildew - gene - potato - locus - arabidopsis - protein - identification
    Expression profiling using cDNA-AFLP is commonly used to display the transcriptome of a specific tissue or developmental stage. Here, cDNA-AFLP was used to identify transcripts in a segregating F1 population of Phytophthora infestans, the oomycete pathogen that causes late blight. To find transcripts derived from putative avirulence (Avr) genes germinated cyst cDNA from F1 progeny with defined avirulence phenotypes was pooled and used in a bulked segregant analysis (BSA). Over 30,000 transcript derived fragments (TDFs) were screened resulting in 99 Avr-associated TDFs as well as TDFs with opposite pattern. With 142 TDF sequences homology searches and database mining was carried out. cDNA-AFLP analysis on individual F1 progeny revealed 100% co-segregation of four TDFs with particular AVR phenotypes and this was confirmed by RT-PCR. Two match the same P. infestans EST with unknown sequence and this is a likely candidate for Avr4. The other two are associated with the Avr3b-Avr10-Avr11 locus. This combined cDNA-AFLP/BSA strategy is an efficient approach to identify Avr-associated transcriptome markers that can complement positional cloning
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