Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

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

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Solanum lycopersicum callose synthase 12 gene, partial cds
    Santillán Martínez, Miguel I. ; Bracuto, Valentina ; Koseoglou, Eleni ; Appiano, Michela ; Jacobsen, Evert ; Visser, Richard G.F. ; Wolters, Anne-Marie A. ; Bai, Yuling - \ 2020
    Wageningen University & Research
    MT521499-MT521504 - Solanum lycopersicum
    Abstract Background The development of CRISPR/Cas9 technology has facilitated targeted mutagenesis in an efficient and precise way. Previously, RNAi silencing of the susceptibility (S) gene PowderyMildewResistance 4 (PMR4) in tomato has been shown to enhance resistance against the powdery mildew pathogen Oidium neolycopersici (On). Results To study whether full knock-out of the tomato PMR4 gene would result in a higher level of resistance than in the RNAi-silenced transgenic plants we generated tomato PMR4 CRISPR mutants. We used a CRISPR/Cas9 construct containing four single-guide RNAs (sgRNAs) targeting the tomato PMR4 gene to increase the possibility of large deletions in the mutants. After PCR-based selection and sequencing of transformants, we identified five different mutation events, including deletions from 4 to 900-bp, a 1-bp insertion and a 892-bp inversion. These mutants all showed reduced susceptibility to On based on visual scoring of disease symptoms and quantification of relative fungal biomass. Histological observations revealed a significantly higher occurrence of hypersensitive response-like cell death at sites of fungal infection in the pmr4 mutants compared to wild-type plants. Both haustorial formation and hyphal growth were diminished but not completely inhibited in the mutants. Conclusion CRISPR/Cas-9 targeted mutagenesis of the tomato PMR4 gene resulted in mutants with reduced but not complete loss of susceptibility to the PM pathogen On. Our study demonstrates the efficiency and versatility of the CRISPR/Cas9 system as a powerful tool to study and characterize S-genes by generating different types of mutations.
    Identification of candidate genes for quantitative downy mildew resistance in cucumber - a review
    Berg, J.A. ; Hermans, F.W.K. ; Vriezen, W.H. ; Bai, Y. ; Schouten, H.J. - \ 2020
    Acta Horticulturae 1294 (2020). - ISSN 0567-7572 - p. 113 - 120.
    AAP genes - Cucumber (Cucumis sativus) - Downy mildew (Pseudoperonospora cubensis) - PI 197088 - Plant-pathogen interactions - QTL mapping - RLK genes

    Cucurbit downy mildew (DM), caused by the obligate biotrophic oomycete Pseudoperonospora cubensis, is a major foliar disease of cucumber. Cucumber accession PI197088 was previously shown to be one of the most promising donors for DM resistance. The resistance in PI197088 is controlled by multiple quantitative trait loci (QTL), each with a relatively small effect. We developed a cucumber line with a 12 Mb introgression from PI197088 in a susceptible background. This introgression line was partially resistant to DM. Subsequently, we combined fine mapping data with RNAseq and whole genome resequencing to identify candidate genes for the resistance conferred by this introgression. Interestingly, fine-mapping data suggested that the partial resistance is caused by a combination of multiple genetically linked genes, leading to three subQTL, each with a different effect on the disease phenotype. In one of these subQTL we identified several Receptor Like Kinase genes (RLK). A novel RLK gene appeared to be present in resistant genotypes. In susceptible genotypes, including the reference genotype “Chinese Long 9930”, this novel gene has a 551 base pair deletion, and was therefore not correctly predicted during the annotation of the cucumber genome. In another subQTL, we found a loss-of-function mutation in the novel susceptibility gene (S-gene) CsAAP2A, encoding an amino acid transporter. In the resistant genotype a non-functional allele of this gene is present due to integration of a transposable element in its coding sequence.

    Identification of novel loci and candidate genes for cucumber downy mildew resistance using GWAS
    Liu, Xiaoping ; Lu, Hongwei ; Liu, Panna ; Miao, Han ; Bai, Yuling ; Gu, Xingfang ; Zhang, Shengping - \ 2020
    Plants 9 (2020)12. - ISSN 2223-7747 - p. 1 - 15.
    Allele-mining - Downy mildew resistance - GWAS - Polygenic - Recessive

    Downy mildew (DM) is one of the most serious diseases in cucumber. Multiple quantitative trait loci (QTLs) for DM resistance have been detected in a limited number of cucumber accessions. In this study we applied genome-wide association analysis (GWAS) to detected genetic loci for DM resistance in a core germplasm (CG) of cucumber lines that represent diverse origins and ecotypes. Phenotypic data on responses to DM infection were collected in four field trials across three years, 2014, 2015, and 2016. With the resequencing data of these CG lines, GWAS for DM resistance was performed and detected 18 loci that were distributed on all the seven cucumber chromosomes. Of these 18 loci, only six (dmG1.4, dmG4.1, dmG4.3, dmG5.2, dmG7.1, and dmG7.2) were detected in two experiments, and were considered as loci with a stable effect on DM resistance. Further, 16 out of the 18 loci colocalized with the QTLs that were reported in previous studies and two loci, dmG2.1 and dmG7.1, were novel ones identified only in this study. Based on the annotation of homologous genes in Arabidopsis and pairwise LD correlation analysis, several candidate genes were identified as potential causal genes underlying the stable and novel loci, including Csa1G575030 for dmG1.4, Csa2G060360 for dmG2.1, Csa4G064680 for dmG4.1, Csa5G606470 for dmG5.2, and Csa7G004020 for dmG7.1. This study shows that the CG germplasm is a very valuable resource carrying known and novel QTLs for DM resistance. The potential of using these CG lines for future allele-mining of candidate genes was discussed in the context of breeding cucumber with resistance to DM.

    Analysis of QTL DM4.1 for Downy Mildew Resistance in Cucumber Reveals Multiple subQTL : A Novel RLK as Candidate Gene for the Most Important subQTL
    Berg, Jeroen A. ; Hermans, Freddy W.K. ; Beenders, Frank ; Lou, Lina ; Vriezen, Wim H. ; Visser, Richard G.F. ; Bai, Yuling ; Schouten, Henk J. - \ 2020
    Frontiers in Plant Science 11 (2020). - ISSN 1664-462X
    cucumber (Cucumis sativus) - downy mildew (Pseudoperonospora cubensis) - leaf rust kinase 10-like (LRK10L) - PI 197088 - plant–pathogen interactions - QTL mapping - receptor-like kinase (RLK) - transcriptomics

    One of the biggest problems in cucumber cultivation is cucurbit downy mildew (DM), caused by the obligate biotroph Pseudoperonospora cubensis. Whereas DM in cucumber was previously efficiently controlled by the dm-1 gene from Indian cucumber accession PI 197087, this resistance was broken by new DM strains, prompting the search for novel sources of resistance. A promising source of resistance is the wild cucumber accession PI 197088. It was previously shown that DM resistance in this genotype inherits polygenically. In this paper, we put the focus on one of the QTL, DM4.1 that is located on chromosome 4. QTL DM4.1 was shown to consist of three subQTL: DM4.1.1 affected pathogen-induced necrosis, DM4.1.2 was shown to have an additive effect on sporulation, and DM4.1.3 had a recessive effect on chlorosis as well as an effect on sporulation. Near-isogenic lines (NILs) were produced by introgressing the subQTLs into a susceptible cucumber line (HS279) with good horticultural traits. Transcriptomic analysis revealed that many genes in general, and defense pathway genes in particular, were differentially expressed in NIL DM4.1.1/.2 compared to NIL DM4.1.3 and the susceptible parent HS279. This indicates that the resistance from subQTL DM4.1.1 and/or subQTL DM4.1.2 likely involves defense signaling pathways, whereas resistance due to subQTL DM4.1.3 is more likely to be independent of known defense pathways. Based on fine-mapping data, we identified the RLK gene CsLRK10L2 as a likely candidate for subQTL DM4.1.2, as this gene was found to have a loss-of-function mutation in the susceptible parent HS279, and was strongly upregulated by P. cubensis inoculation in NIL DM4.1.1/.2. Heterologous expression of this gene triggered necrosis, providing further evidence that this gene is indeed causal for subQTL DM4.1.2.

    Comparative genomics reveals the in planta-secreted Verticillium dahliae Av2 effector protein recognized in tomato plants that carry the V2 resistance locus
    Chavarro-Carrero, Edgar A. ; Vermeulen, Jasper P. ; E. Torres, David ; Usami, Toshiyuki ; Schouten, Henk J. ; Bai, Yuling ; Seidl, Michael F. ; Thomma, Bart P.H.J. - \ 2020
    Environmental Microbiology (2020). - ISSN 1462-2912

    Plant pathogens secrete effector molecules during host invasion to promote colonization. However, some of these effectors become recognized by host receptors to mount a defence response and establish immunity. Recently, a novel resistance was identified in wild tomato, mediated by the single dominant V2 locus, to control strains of the soil-borne vascular wilt fungus Verticillium dahliae that belong to race 2. With comparative genomics of race 2 strains and resistance-breaking race 3 strains, we identified the avirulence effector that activates V2 resistance, termed Av2. We identified 277 kb of race 2-specific sequence comprising only two genes encoding predicted secreted proteins that are expressed during tomato colonization. Subsequent functional analysis based on genetic complementation into race 3 isolates and targeted deletion from the race 1 isolate JR2 and race 2 isolate TO22 confirmed that one of the two candidates encodes the avirulence effector Av2 that is recognized in V2 tomato plants. Two Av2 allelic variants were identified that encode Av2 variants that differ by a single acid. Thus far, a role in virulence could not be demonstrated for either of the two variants.

    On the origin and dispersal of cultivated spinach (Spinacia oleracea L.)
    Ribera, Arnau ; Treuren, R. van; Kik, C. ; Bai, Y. ; Wolters, A.M.A. - \ 2020
    Genetic Resources and Crop Evolution (2020). - ISSN 0925-9864
    Spinach (Spinacia oleracea L.) is an economically important crop that is cultivated and consumed worldwide. Spinach is interfertile with the wild species S. tetrandra Steven ex M. Bieb. and S. turkestanica Iljin that therefore are presumed to include the most likely crop ancestor. Here we studied variation in 60 Single Nucleotide Polymorphisms (SNP) previously identified in S. oleracea to address the issue of crop ancestry and domestication region. For this purpose we investigated 95 accessions, including 54 spinach landraces from a wide geographic area in Europe and Asia and 16 S. tetrandra and 25 S. turkestanica populations of which the majority had only recently become available. Compared to S. tetrandra substantially higher levels of amplification success and higher levels of variation were detected for S. turkestanica, indicating that S. oleracea is genetically closer to S. turkestanica than to S. tetrandra. Our phylogenetic and population structure analysis supported the conclusion that S. turkestanica is the most likely ancestor of cultivated spinach. In addition, these analyses revealed a group of S. oleracea landraces from Eastern and Southern Asia with a strong genetic resemblance to S. turkestanica. This group includes landraces from Afghanistan and Pakistan, which are part of the native distribution range of S. turkestanica. The domestication of spinach may therefore have occurred more eastwards than generally assumed. Furthermore, our study provides support for the hypothesis that after domestication, spinach was introduced into China via Nepal. Additional collecting of spinach landraces is recommended in order to allow the more precise reconstruction of the crop migration routes.
    The NLR Protein Encoded by the Resistance Gene Ty-2 Is Triggered by the Replication-Associated Protein Rep/C1 of Tomato Yellow Leaf Curl Virus
    Shen, Xuexue ; Yan, Zhe ; Wang, Xiaoxuan ; Wang, Yinlei ; Arens, Marjon ; Du, Yongchen ; Visser, Richard G.F. ; Kormelink, Richard ; Bai, Yuling ; Wolters, Anne Marie A. - \ 2020
    Frontiers in Plant Science 11 (2020). - ISSN 1664-462X
    avirulence factor - cloning - NLR gene - Rep/C1 - Ty-2 - TYLCV

    The whitefly-transmitted tomato yellow leaf curl virus (TYLCV) is one of the most destructive viral pathogens of cultivated tomato. To combat TYLCV, resistance gene Ty-2 has been introduced into cultivated tomato (Solanum lycopersicum) from wild tomato species Solanum habrochaites by interspecific crossing. Introgression lines with Ty-2 contain a large inversion compared with S. lycopersicum, which causes severe suppression of recombination and has hampered the cloning of Ty-2 so far. Here, we report the fine-mapping and cloning of Ty-2 using crosses between a Ty-2 introgression line and several susceptible S. habrochaites accessions. Ty-2 was shown to encode a nucleotide-binding leucine-rich repeat (NLR) protein. For breeding purposes, a highly specific DNA marker tightly linked to the Ty-2 gene was developed permitting marker-assisted selection. The resistance mediated by Ty-2 was effective against the Israel strain of TYLCV (TYLCV-IL) and tomato yellow leaf curl virus-[China : Shanghai2] (TYLCV-[CN : SH2]), but not against tomato yellow leaf curl Sardinia virus (TYLCSV) and leafhopper-transmitted beet curly top virus (BCTV). By co-infiltration experiments we showed that transient expression of the Rep/C1 protein of TYLCV, but not of TYLCSV triggered a hypersensitive response (HR) in Nicotiana benthamiana plants co-expressing the Ty-2 gene. Our results indicate that the Rep/C1 gene of TYLCV-IL presents the avirulence determinant of Ty-2-mediated resistance.

    CRISPR/Cas9-targeted mutagenesis of the tomato susceptibility gene PMR4 for resistance against powdery mildew
    Santillán Martínez, Miguel I. ; Bracuto, Valentina ; Koseoglou, Eleni ; Appiano, Michela ; Jacobsen, Evert ; Visser, Richard G.F. ; Wolters, Anne-Marie A. ; Bai, Yuling - \ 2020
    BMC Plant Biology 20 (2020)1. - ISSN 1471-2229
    CRISPR/Cas9 - PMR4 - Powdery mildew - Susceptibility gene - Targeted mutagenesis

    Background: The development of CRISPR/Cas9 technology has facilitated targeted mutagenesis in an efficient and precise way. Previously, RNAi silencing of the susceptibility (S) gene P owdery M ildew R esistance 4 (PMR4) in tomato has been shown to enhance resistance against the powdery mildew pathogen Oidium neolycopersici (On). Results: To study whether full knock-out of the tomato PMR4 gene would result in a higher level of resistance than in the RNAi-silenced transgenic plants we generated tomato PMR4 CRISPR mutants. We used a CRISPR/Cas9 construct containing four single-guide RNAs (sgRNAs) targeting the tomato PMR4 gene to increase the possibility of large deletions in the mutants. After PCR-based selection and sequencing of transformants, we identified five different mutation events, including deletions from 4 to 900-bp, a 1-bp insertion and a 892-bp inversion. These mutants all showed reduced susceptibility to On based on visual scoring of disease symptoms and quantification of relative fungal biomass. Histological observations revealed a significantly higher occurrence of hypersensitive response-like cell death at sites of fungal infection in the pmr4 mutants compared to wild-type plants. Both haustorial formation and hyphal growth were diminished but not completely inhibited in the mutants. Conclusion: CRISPR/Cas-9 targeted mutagenesis of the tomato PMR4 gene resulted in mutants with reduced but not complete loss of susceptibility to the PM pathogen On. Our study demonstrates the efficiency and versatility of the CRISPR/Cas9 system as a powerful tool to study and characterize S-genes by generating different types of mutations.

    Correlation between total hypha length and haustoria number of Pseudoidium neolycopersici in type I trichome cells of tomato leaves
    Suzuki, T. ; Nakao, Y. ; Ura, R. ; Nakaba, M. ; Nishiyama, T. ; Takikawa, Y. ; Matsuda, Y. ; Kakutani, K. ; Bai, Y. ; Nonomura, T. - \ 2020
    Australasian Plant Pathology 49 (2020). - ISSN 0815-3191 - p. 451 - 460.
    Conidial germination - Haustorial formation - Hyphal elongation - Solanum lycopersicum - Tomato powdery mildew

    Powdery mildew haustoria are easier to be observed by light microscopy in trichome cells compared to epidermal cells of infected leaves. The objective of this study was to explore the relationship between the hyphal length and the number of haustoria in type I trichome cells of tomato (Solanum lycopersicum Mill.) leaves. The trichome cells of tomato cv. Moneymaker were inoculated with conidia of tomato powdery mildew (Pseudoidium neolycopersici L. Kiss), isolate KTP-04. On these cells, the P. neolycopersici isolate produced a maximum of four vigorously elongated hyphae per conidium. At 12 days after inoculation, KTP-04 formed two to five haustoria per conidium. Field-emission scanning electron microscopy showed that the haustorium consisted of a haustorial body and several lobes embedded in an extrahaustorial matrix. The number of haustoria per hypha and hyphal length on trichomes were positively correlated. Also, the tips of one to four hypha per conidium (excluding germ tubes and primary appressoria) were injured using a minute glass needle installed on micromanipulator under a high-fidelity digital microscope, and their total hyphal lengths were compared. Wounded hyphae possessed the same number of haustoria in trichome cells as non-wounded hyphae, and total hyphal lengths were similar between treatment groups. In this study, a new model was developed to study the infection mechanisms of powdery mildews that will be useful in future gene expression studies.

    A review on the genetic resources, domestication and breeding history of spinach (Spinacia oleracea L.)
    Ribera, Arnau ; Bai, Y. ; Wolters, A.M.A. ; Treuren, R. van; Kik, C. - \ 2020
    Euphytica 216 (2020)48. - ISSN 0014-2336 - 21 p.
    This paper addresses the genetic resources, domestication and breeding history of spinach as a comprehensive review of these crop aspects is currently unavailable. It is shown that the availability of genetic resources of wild relatives belonging to the primary gene pool is currently very limited, which hampers breeding and research activities. Therefore, new collecting expeditions are clearly warranted. The domestication of spinach is discussed on the basis of its presumed migration routes and the traits that were probably involved in the domestication syndrome. Spinach is thought to have domesticated in former Persia. Migration then occurred eastwards to China and westwards to Europe, but additional genetic data are needed to reveal the most likely migration routes. Morphological changes in pistillate flowers and loss of dormancy are identified as the main traits involved in the domestication syndrome of spinach. To a large extent we could re-construct the relationships between spinach cultivars that were developed until the 1950s, but this appeared difficult for the more recent cultivars due to intellectual property protection by breeding companies. Resistance against downy mildew has been the main breeding target in spinach. The introgression of NBS-LRR resistance genes from wild relatives is the major strategy to develop downy mildew resistant cultivars. However, the use of loss-of-function alleles of susceptibility genes may provide a more durable strategy to develop resistant cultivars. So far, abiotic resistance and quality traits have received minor attention in spinach research and breeding. This is expected to change considering the potential effects of climate change on these traits.
    Ty-1, a universal resistance gene against geminiviruses that is compromised by co-replication of a betasatellite
    Voorburg, Corien M. ; Yan, Zhe ; Bergua-Vidal, Maria ; Wolters, Anne Marie A. ; Bai, Yuling ; Kormelink, Richard - \ 2020
    Molecular Plant Pathology 21 (2020)2. - ISSN 1464-6722 - p. 160 - 172.
    beet curly top virus - betasatellite - geminivirus - resistance - RNA interference - tomato yellow leaf curl virus - Ty-1

    Tomato yellow leaf curl virus (TYLCV), a begomovirus, causes large yield losses and breeding for resistance is an effective way to combat this viral disease. The resistance gene Ty-1 codes for an RNA-dependent RNA polymerase and has recently been shown to enhance transcriptional gene silencing of TYLCV. Whereas Ty-1 was earlier shown to also confer resistance to a bipartite begomovirus, here it is shown that Ty-1 is probably generic to all geminiviruses. A tomato Ty-1 introgression line, but also stable transformants of susceptible tomato cv. Moneymaker and Nicotiana benthamiana (N. benthamiana) expressing the Ty-1 gene, exhibited resistance to begomoviruses as well as to the distinct, leafhopper-transmitted beet curly top virus, a curtovirus. Stable Ty-1 transformants of N. benthamiana and tomato showed fewer symptoms and reduced viral titres on infection compared to wild-type plants. TYLCV infections in wild-type N. benthamiana plants in the additional presence of a betasatellite led to increased symptom severity and a consistent, slightly lowered virus titre relative to the high averaged levels seen in the absence of the betasatellite. On the contrary, in Ty-1 transformed N. benthamiana viral titres increased in the presence of the betasatellite. The same was observed when these Ty-1-encoding plants were challenged with TYLCV and a potato virus X construct expressing the RNA interference suppressor protein βC1 encoded by the betasatellite. The resistance spectrum of Ty-1 and the durability of the resistance are discussed in light of antiviral RNA interference and viral counter defence strategies.

    CRISPR/Cas inactivation of RECQ4 increases homeologous crossovers in an interspecific tomato hybrid
    Maagd, Ruud A. de; Loonen, Annelies ; Chouaref, Jihed ; Pelé, Alexandre ; Meijer-Dekens, Fien ; Fransz, Paul ; Bai, Yuling - \ 2020
    Plant Biotechnology Journal 18 (2020)3. - ISSN 1467-7644 - p. 805 - 813.
    class II crossover pathway - interspecific crosses - introgression breeding - meiosis - RECQ4

    Crossover formation during meiosis in plants is required for proper chromosome segregation and is essential for crop breeding as it allows an (optimal) combination of traits by mixing parental alleles on each chromosome. Crossover formation commences with the production of a large number of DNA double-strand breaks, of which only a few result in crossovers. A small number of genes, which drive the resolution of DNA crossover intermediate structures towards non-crossovers, have been identified in Arabidopisis thaliana. In order to explore the potential of modification of these genes in interspecific hybrids between crops and their wild relatives towards increased production of crossovers, we have used CRISPR/Cas9-mutagenesis in an interspecific tomato hybrid to knockout RecQ4. A biallelic recq4 mutant was obtained in the F1 hybrid of Solanum lycopersicum and S. pimpinellifolium. Compared with the wild-type F1 hybrid, the F1 recq4 mutant was shown to have a significant increase in crossovers: a 1.53-fold increase when directly observing ring bivalents in male meiocytes microscopically and a 1.8-fold extension of the genetic map when measured by analysing SNP markers in the progeny (F2) plants. This is one of the first demonstrations of increasing crossover frequency in interspecific hybrids by manipulating genes in crossover intermediate resolution pathways and the first to do so by directed mutagenesis. Significance statement: Increasing crossover frequency during meiosis can speed up or simplify crop breeding that relies on meiotic crossovers to introduce favourable alleles controlling important traits from wild relatives into crops. Here we show for the first time that knocking out an inhibitor of crossovers in an interspecific hybrid between tomato and its relative wild species using CRISPR/Cas9-mutagenesis results in increased recombination between the two genomes.

    Breeding Has Increased the Diversity of Cultivated Tomato in The Netherlands
    Schouten, Henk J. ; Tikunov, Yury ; Verkerke, Wouter ; Finkers, Richard ; Bovy, Arnaud ; Bai, Yuling ; Visser, Richard G.F. - \ 2019
    Frontiers in Plant Science 10 (2019). - ISSN 1664-462X
    breeding - diversity - introgressions - metabolomics - tomato varieties

    It is generally believed that domestication and breeding of plants has led to genetic erosion, including loss of nutritional value and resistances to diseases, especially in tomato. We studied the diversity dynamics of greenhouse tomato varieties in NW Europe, especially The Netherlands, over the last seven decades. According to the used SNP array, the genetic diversity was indeed very low during the 1960s, but is now eight times higher when compared to that dip. The pressure since the 1970s to apply less pesticides led to the introgression of many disease resistances from wild relatives, representing the first boost of genetic diversity. In Europe a second boost ensued, largely driven by German popular media who named poor tasting tomatoes Wasserbomben (water bombs). The subsequent collapse of Dutch tomato exports to Germany fueled breeding for fruit flavor, further increasing diversity since the 1990s. The increased diversity in composition of aroma volatiles observed starting from 1990s may reflect the efforts of breeders to improve fruit quality. Specific groups of aroma compounds showed different quantitative trend over the decades studied. Our study provides compelling evidence that breeding has increased the diversity of tomato varieties considerably since the 1970s.

    Breeding crops with resistance to diseases and pests
    Niks, R.E. ; Parlevliet, J.E. ; Lindhout, P. ; Bai, Y. - \ 2019
    Wageningen : Wageningen Academic Publishers - ISBN 9789086863280 - 204
    'Breeding crops with resistance to diseases and pests' is the most up-to-date textbook on this topic targeted towards students in Plant Sciences. This book describes the most basic elements in plant pathogen interactions and defence strategies in plants. The scientific background is explained as far as it is relevant for breeders to make sensible choices in designing and running their breeding work. A major part of the book presents the options plant breeders have to consider such as what strategy to follow, what aspects to evaluate or measure, and whether it is best to apply mixtures of pathotypes or to test pathotypes one by one. Professionals, notably in the field of Plant Breeding, may also use it as a manual for disease resistance breeding. The book should be of interest to anyone interested in plant defence strategies and the enhancement of resistance in modern cultivars. In order to enliven and illustrate the text, background reading, interesting examples and exceptions, concrete cases of application and further reading are given. Supplementary reading is readily distinguished from the main text by a different typography, so it is clear what material is most relevant and what is meant as examples supporting the main story lines. Most sections are followed by exercises so that students can test whether they understood the material that was presented.
    Resistance to tomato yellow leaf curl virus in tomato germplasm
    Yan, Zhe ; Pérez-de-Castro, Ana ; Díez, Maria J. ; Hutton, Samuel F. ; Visser, Richard G.F. ; Wolters, Anne-Marie A. ; Bai, Yuling ; Li, Junming - \ 2018
    Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
    Begomovirus - Resistance - S. chilense - S. peruvianum - Solanum lycopersicum - Tomato - TYLCV

    Tomato yellow leaf curl virus (TYLCV) is a virus species causing epidemics in tomato (Solanum lycopersicum) worldwide. Many efforts have been focused on identification of resistance sources by screening wild tomato species. In many cases, the accession numbers were either not provided in publications or not provided in a consistent manner, which led to redundant screenings. In the current study, we summarized efforts on the screenings of wild tomato species for TYLCV resistance from various publications. In addition, we screened 708 accessions from 13 wild tomato species using different inoculation assays (i.e., whitefly natural infection and Agrobacterium-mediated inoculation) from which 138 accessions exhibited no tomato yellow leaf curl disease (TYLCD) symptoms. These symptomless accessions include 14 accessions from S. arcanum, 43 from S. chilense, 1 from S. chmielewskii, 28 from S. corneliomulleri, 5 from S. habrochaites, 4 from S. huaylasense, 2 from S. neorickii, 1 from S. pennellii, 39 from S. peruvianum, and 1 from S. pimpinellifolium. Most of the screened S. chilense accessions remained symptomless. Many symptomless accessions were also identified in S. arcanum, S. corneliomulleri, and S. peruvianum. A large number of S. pimpinellifolium accessions were screened. However, almost all of the tested accessions showed TYLCD symptoms. Further, we studied allelic variation of the Ty-1/Ty-3 gene in few S. chilense accessions by applying virus-induced gene silencing and allele mining, leading to identification of a number of allele-specific polymorphisms. Taken together, we present a comprehensive overview on TYLCV resistance and susceptibility in wild tomato germplasm, and demonstrate how to study allelic variants of the cloned Ty-genes in TYLCV-resistant accessions.

    Tomato disease resistances in the post-genomics era
    Bai, Yuling ; Yan, Zhe ; Moriones, E. ; Fernández-Muñoz, R. - \ 2018
    In: Proceedings of the 5th International Symposium on Tomato Diseases. - International Society for Horticultural Science (Acta Horticulturae ) - ISBN 9789462612037 - p. 1 - 17.
    CRISPR/CAS9 - Effector target - Effector-assisted R gene identification - Gene editing - Mutagenesis - Recessive resistance - Resilience to combined stresses - TILLING

    Disease in tomato (Solanum lycopersicum) can be caused by many pathogenic organisms, including cellular pathogens (e.g., fungi, bacteria, phytoplasmas, oomycetes and nematodes) and non-cellular pathogens (e.g., viruses and viroids). To respond to pathogen attack, tomato plants, like other sessile organisms, have developed an immune system, where pathogen effectors and plant receptor proteins (e.g., resistance proteins) play a central role. With advances in the genomics era, our understanding of plant-pathogen interactions is evolving rapidly. For example, pathogen genomics has allowed a genome-wide study on the structure, function and evolution of effectors in pathogen genomes. So-called effectoromics offers a high-throughput functional approach to study effector-associated plant genes such as resistance (R) genes and susceptibility (S) genes. In tomato, “genome to germplasms” is facilitating a genome dimension to the exploration of plant diversity in resistance by sequencing and re-sequencing of genomes of available germplasm resources. Together with this breakthrough and powerful techniques for genome editing, novel strategies are being developed for breeding tomatoes with durable resistance to pathogens. Using examples of several tomato diseases, this review focuses on (1) layers of plant immune system, (2) the exploitation of plant S genes in resistance breeding, (3) rapid identification of R and S genes, and (4) novel routes for durable resistance to pathogens. Finally, the topic of breeding for resilience to combined biotic and abiotic stresses is discussed based on our results, which show extensive crosstalk between loci/pathways for resistance to pathogens and tolerance to abiotic stresses.

    The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses
    Bai, Yuling ; Sunarti, Sri ; Kissoudis, Christos ; Visser, Richard G.F. ; Linden, C.G. van der - \ 2018
    Frontiers in Plant Science 9 (2018). - ISSN 1664-462X
    Abiotic stress - Biotic stress - Combined stresses - Disease resistance - Effector-triggered immunity (ETI) - PAMP-triggered immunity (PTI)

    In the field, plants constantly face a plethora of abiotic and biotic stresses that can impart detrimental effects on plants. In response to multiple stresses, plants can rapidly reprogram their transcriptome through a tightly regulated and highly dynamic regulatory network where WRKY transcription factors can act as activators or repressors. WRKY transcription factors have diverse biological functions in plants, but most notably are key players in plant responses to biotic and abiotic stresses. In tomato there are 83 WRKY genes identified. Here we review recent progress on functions of these tomato WRKY genes and their homologs in other plant species, such as Arabidopsis and rice, with a special focus on their involvement in responses to abiotic and biotic stresses. In particular, we highlight WRKY genes that play a role in plant responses to a combination of abiotic and biotic stresses.

    Plant behaviour under combined stress : tomato responses to combined salinity and pathogen stress
    Bai, Yuling ; Kissoudis, Christos ; Yan, Zhe ; Visser, Richard G.F. ; Linden, Gerard van der - \ 2018
    The Plant Journal 93 (2018)4. - ISSN 0960-7412 - p. 781 - 793.
    combined biotic and abiotic stresses - plant disease - resistance gene - salinity stress - stress interaction - stress tolerance
    Crop plants are subjected to a variety of stresses during their lifecycle, including abiotic stress factors such as salinity and biotic stress factors such as pathogens. Plants have developed a multitude of defense and adaptation responses to these stress factors. In the field, different stress factors mostly occur concurrently resulting in a new state of stress, the combined stress. There is evidence that plant resistance to pathogens can be attenuated or enhanced by abiotic stress factors. With stress tolerance research being mostly focused on plant responses to individual stresses, the understanding of a plant's ability to adapt to combined stresses is limited. In the last few years, we studied powdery mildew resistance under salt stress conditions in the model crop plant tomato with the aim to understand the requirements to achieve plant resilience to a wider array of combined abiotic and biotic stress combinations. We uncovered specific responses of tomato plants to combined salinity-pathogen stress, which varied with salinity intensity and plant resistance genes. Moreover, hormones, with their complex regulation and cross-talk, were shown to play a key role in the adaptation of tomato plants to the combined stress. In this review, we attempt to understand the complexity of plant responses to abiotic and biotic stress combinations, with a focus on tomato responses (genetic control and cross-talk of signaling pathways) to combined salinity and pathogen stresses. Further, we provide recommendations on how to design novel strategies for breeding crops with a sustained performance under diverse environmental conditions.
    Trichomes: interaction sites of tomato leaves with biotrophic powdery mildew pathogens
    Suzuki, Tomoko ; Murakami, Tomoe ; Takizumi, Yoshihiro ; Ishimaru, Hiroyuki ; Kudo, Daiki ; Takikawa, Yoshihiro ; Matsuda, Yoshinori ; Kakutani, Koji ; Bai, Yuling ; Nonomura, Teruo - \ 2018
    European Journal of Plant Pathology 150 (2018)1. - ISSN 0929-1873 - p. 115 - 125.
    Delayed cell death - Erysiphe trifoliorum - Hypersensitive cell death - Papilla formation - Podosphaera xanthii - Pseudoidium neolycopersici

    The present study aimed to explore the possibility of using the type I trichomes of tomato (Solanum lycopersicum) to monitor the infection processes of powdery mildews by microscopy. Individual trichome cells of two tomato genotypes were inoculated with pathogenic and non-pathogenic powdery mildew species, Pseudoidium neolycopersici, Erysiphe trifoliorum and Podosphaera xanthii. On the trichome cells of the tomato cultivar Moneymaker, hyphae of the pathogenic Pseudoidium neolycopersici (isolates KTP-03 and KTP-04) grew vigorously; whereas hyphal growth of the non-pathogenic Erysiphe trifoliorum and Podosphaera xanthii ceased after appressorium formation, which was associated with papilla formation and hypersensitive cell death, respectively. Similar infection processes of the tested powdery mildews were seen in Moneymaker epidermal cells. Therefore, tomato trichomes are suitable for analysing, at individual cell level, the infection processes of different pathotypes of powdery mildews and for observing the cytological responses of plants by non-pathogenic powdery mildews. On the other hand, it was observed that both isolates KTP-03 and KTP-04 failed to produce conidiophores on the hyphae elongating on Moneymaker trichomes. Similarly, no conidiophores were produced on the hyphae elongating on trichomes of Solanum peruvianum LA2172, which is resistant to KTP-03 and susceptible to KTP-04. Interestingly, delayed cell death occurred in LA2172 epidermal cells, which were attacked by KTP-03 hyphae elongating from trichomes and conidiophores were formed on new hyphae growing from the leaf epidermal cells. Thus, leaf trichomes and epidermal cells of the wild tomato species LA2172 reacted differently to the avirulent isolate KTP-03.

    Functional characterization of cucumber (Cucumis sativus L.) Clade V MLO genes
    Berg, J.A. ; Appiano, Michela ; Bijsterbosch, G. ; Visser, R.G.F. ; Schouten, H.J. ; Bai, Y. - \ 2017
    cucumber - cucumis sativus - powdery mildew - MLO - susceptiblity genes - gene expression
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