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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    Exploration of a Resequenced Tomato Core Collection for Phenotypic and Genotypic Variation in Plant Growth and Fruit Quality Traits
    Roohanitaziani, Raana ; Maagd, R.A. de; Lammers, M. ; Molthoff, J.W. ; Meijer-Dekens, R.G. ; Kaauwen, M.P.W. van; Finkers, H.J. ; Tikunov, Y.M. ; Visser, R.G.F. ; Bovy, A.G. - \ 2020
    Genes 11 (2020)11. - ISSN 2073-4425 - 22 p.
    A tomato core collection consisting of 122 gene bank accessions, including landraces, old cultivars, and wild relatives, was explored for variation in several plant growth, yield and fruit quality traits. The resequenced accessions were also genotyped with respect to a number of mutations or variations in key genes known to underlie these traits. The yield-related traits fruit number and fruit weight were much higher in cultivated varieties when compared to wild accessions, while, in wild tomato accessions, Brix was higher than in cultivated varieties. Known mutations in fruit size and shape genes could well explain the fruit size variation, and fruit colour variation could be well explained by known mutations in key genes of the carotenoid and flavonoid pathway. The presence and phenotype of several plant architecture affecting mutations, such as self-pruning (sp), compound inflorescence (s), jointless-2 (j-2), and potato leaf (c) were also confirmed. This study provides valuable phenotypic information on important plant growth- and quality-related traits in this collection. The allelic distribution of known genes that underlie these traits provides insight into the role and importance of these genes in tomato domestication and breeding. This resource can be used to support (precision) breeding strategies for tomato crop improvement.
    The rin, nor and Cnr spontaneous mutations inhibit tomato fruit ripening in additive and epistatic manners
    Wang, Rufang ; Lammers, Michiel ; Tikunov, Yury ; Bovy, Arnaud G. ; Angenent, Gerco C. ; Maagd, Ruud A. de - \ 2020
    Plant Science 294 (2020). - ISSN 0168-9452
    Colorless non-ripening - Fruit ripening - non-ripening - ripening inhibitor - Spontaneous mutation - Tomato

    Tomato fruit ripening is regulated by transcription factors (TFs), their downstream effector genes, and the ethylene biosynthesis and signalling pathway. Spontaneous non-ripening mutants ripening inhibitor (rin), non-ripening (nor) and Colorless non-ripening (Cnr) correspond with mutations in or near the TF-encoding genes MADS-RIN, NAC-NOR and SPL-CNR, respectively. Here, we produced heterozygous single and double mutants of rin, nor and Cnr and evaluated their functions and genetic interactions in the same genetic background. We showed how these mutations interact at the level of phenotype, individual effector gene expression, and sensory and quality aspects, in a dose-dependent manner. Rin and nor have broadly similar quantitative effects on all aspects, demonstrating their additivity in fruit ripening regulation. We also found that the Cnr allele is epistatic to rin and nor and that its pleiotropic effects on fruit size and volatile production, in contrast to the well-known dominant effect on ripening, are incompletely dominant, or recessive.

    Revisiting the Role of Master Regulators in Tomato Ripening
    Wang, Rufang ; Angenent, Gerco C. ; Seymour, Graham ; Maagd, Ruud A. de - \ 2020
    Trends in Plant Science 25 (2020)3. - ISSN 1360-1385 - p. 291 - 301.
    CRISPR- mutagenesis - gain-of-function - mutants - ripening - tomato - transcription factors

    The study of transcriptional regulation of tomato ripening has been led by spontaneous mutations in transcription factor (TF) genes that completely inhibit normal ripening, suggesting that they are ‘master regulators’. Studies using CRISPR/Cas9 mutagenesis to produce knockouts of the underlying genes indicate a different picture, suggesting that the regulation is more robust than previously thought. This requires us to revisit our model of the regulation of ripening and replace it with one involving a network of partially redundant components. At the same time, the fast rise of CRISPR/Cas mutagenesis, resulting in unexpectedly weak phenotypes, compared with knockdown technology, suggests that compensatory mechanisms may obscure protein functions. This emphasises the need for assessment of these mechanisms in plants and for the careful design of mutagenesis experiments.

    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.

    Re-evaluation of transcription factor function in tomato fruit development and ripening with CRISPR/Cas9-mutagenesis
    Wang, Rufang ; Rocha Tavano, Eveline Carla da; Lammers, Michiel ; Martinelli, Adriana Pinheiro ; Angenent, Gerco C. ; Maagd, Ruud A. de - \ 2019
    Scientific Reports 9 (2019)1. - ISSN 2045-2322

    Tomato (Solanum lycopersicum) is a model for climacteric fleshy fruit ripening studies. Tomato ripening is regulated by multiple transcription factors together with the plant hormone ethylene and their downstream effector genes. Transcription Factors APETALA2a (AP2a), NON-RIPENING (NOR) and FRUITFULL (FUL1/TDR4 and FUL2/MBP7) were reported as master regulators controlling tomato fruit ripening. Their proposed functions were derived from studies of the phenotype of spontaneous mutants or RNAi knock-down lines rather than, as it appears now, actual null mutants. To study TF function in tomato fruit ripening in more detail, we used CRISPR/Cas9-mediated mutagenesis to knock out the encoding genes, and phenotypes of these mutants are reported for the first time. While the earlier ripening, orange-ripe phenotype of ap2a mutants was confirmed, the nor null mutant exhibited a much milder phenotype than the spontaneous nor mutant. Additional analyses revealed that the severe phenotype in the spontaneous mutant is caused by a dominant-negative allele. Our approach also provides new insight into the independent and overlapping functions of FUL1 and FUL2. Single and combined null alleles of FUL1 and FUL2 illustrate that these two genes have partially redundant functions in fruit ripening, but also unveil an additional role for FUL2 in early fruit development.

    De CRISPR/Cas-revolutie in de biologie
    Maagd, Ruud de - \ 2018
    Quick and simple gene repairs
    Groenen, M. ; Maagd, R.A. de; Oost, J. van der - \ 2017
    Inhibition of bolting and flowering of a beta vulgaris plant
    Maagd, R.A. de; Arkel, J. van; Angenent, G.C. ; Wurbs, David ; Kraus, Josef - \ 2017
    Octrooinummer: WO2017072304, gepubliceerd: 2017-05-04.
    The present invention provides means for inhibiting the bolting and flowering of a Beta vulgaris plant, including an isolated nucleic acid, which can be used to produce a transgenic Beta vulgaris plant, where bolting and flowering is inhibited after vernalization. Furthermore, the invention discloses vectors, transgenic and non-transgenic, non-bolting plants and parts thereof, and methods for producing such plants.
    CRISPR/Cas: de techniek en zijn toepassing in plantenonderzoek en -veredeling
    Maagd, Ruud de - \ 2017
    CRISPR/Cas: de techniek en de kansen voor de veredeling
    Maagd, Ruud de - \ 2017
    Snel en simpel genen repareren: opmars DNA-bewerkingstechniek CRISPR-Cas
    Oost, J. van der; Groenen, M. ; Maagd, R.A. de - \ 2017
    Identification of loci affecting accumulation of secondary metabolites in tomato fruit of a Solanum lycopersicum × Solanum chmielewskii introgression line population
    Ballester Frutos, A.R. ; Tikunov, Yury ; Molthoff, Jos ; Grandillo, Silvana ; Viquez-Zamora, Marcela ; Vos, Ric de; Maagd, Ruud A. de; Heusden, Sjaak van; Bovy, Arnaud G. - \ 2016
    Frontiers in Plant Science 7 (2016). - ISSN 1664-462X
    Alkaloids - Flavonoids - Introgression lines - QTL analysis - Tomato (Solanum lycopersicum)

    Semi-polar metabolites such as flavonoids, phenolic acids, and alkaloids are very important health-related compounds in tomato. As a first step to identify genes responsible for the synthesis of semi-polar metabolites, quantitative trait loci (QTLs) that influence the semi-polar metabolite content in red-ripe tomato fruit were identified, by characterizing fruits of a population of introgression lines (ILs) derived from a cross between the cultivated tomato Solanum lycopersicum and the wild species Solanum chmielewskii. By analyzing fruits of plants grown at two different locations, we were able to identify robust metabolite QTLs for changes in phenylpropanoid glycoconjugation on chromosome 9, for accumulation of flavonol glycosides on chromosome 5, and for alkaloids on chromosome 7. To further characterize the QTLs we used a combination of genome sequencing, transcriptomics and targeted metabolomics to identify candidate key genes underlying the observed metabolic variation.

    Relevance of Bt toxin interaction studies for environmental risk assessment of genetically modified crops
    Schrijver, Adinda De; Clercq, Patrick De; Maagd, R.A. de; Frankenhuyzen, Kees van - \ 2015
    Plant Biotechnology Journal 13 (2015)9. - ISSN 1467-7644 - p. 1221 - 1223.
    Bt protein - Genetically modified plants - Interaction - Nontarget effects - Risk assessment - Specificity

    In recent years, different Bacillus thuringiensis (Bt) toxin-encoding genes have been combined or 'stacked' in genetically modified (GM) crops. Synergism between Bt proteins may occur and thereby increase the impact of the stacked GM event on nontarget invertebrates compared to plants expressing a single Bt gene. On the basis of bioassay data available for Bt toxins alone or in combination, we argue that the current knowledge of Bt protein interactions is of limited relevance in environmental risk assessment (ERA).

    Plant Reproduction, recent achievements and technologies
    Angenent, G.C. ; Immink, R.G.H. ; Boutilier, K.A. ; Maagd, R.A. de; Groot, S.P.C. - \ 2015
    Our Expertise: Our research group at Wageningen UR studies several aspects of the plant reproduction process and how the various steps in reproduction, from flower to seed and fruit, are regulated at the genetic, physiological and molecular level. What do we offer: • Genes that regulate important traits related to reproduction, • Knowledge about the regulation of these genes and the influence of the environment, • Protocols and screening methods to improve in vitro propagation and doubledhaploid (DH) production systems, • Approaches for gene function determination, • Methods for determining quality and storability of seeds.
    The cell size distribution of tomato fruit can be changed by overexpression of CDKA1
    Czerednik, A. ; Busscher, M. ; Angenent, G.C. ; Maagd, R.A. de - \ 2015
    Plant Biotechnology Journal 13 (2015)2. - ISSN 1467-7644 - p. 259 - 268.
    cyclin-dependent kinase - lycopersicon-esculentum mill - plant development - arabidopsis - endoreduplication - growth - gene - expression - division - dna
    Tomato is one of the most cultivated vegetables in the world and an important ingredient of the human diet. Tomato breeders and growers face a continuous challenge of combining high quantity (production volume) with high quality (appearance, taste and perception for the consumers, processing quality for the processing industry). To improve the quality of tomato, it is important to understand the regulation of fruit development and of fruit cellular structure, which is in part determined by the sizes and numbers of cells within a tissue. The role of the cell cycle therein is poorly understood. Plant cyclin-dependent kinases (CDKs) are homologues of yeast cdc2, an important cell cycle regulator conserved throughout all eukaryotes. CDKA1 is constitutively expressed during the cell cycle and has dual functions in S- and M-phase progression. We have produced transgenic tomato plants with increased expression of CDKA1 under the control of the fruit-specific TPRP promoter, which despite a reduced number of seeds and diminished amount of jelly, developed fruits with weight and shape comparable to that of wild-type fruits. However, the phenotypic changes with regard to the pericarp thickness and placenta area were remarkable. Fruits of tomato plants with the highest expression of CDKA1 had larger septa and columella (placenta), compared with wild-type fruits. Our data demonstrate the possibility of manipulating the ratio between cell division and expansion by changing the expression of a key cell cycle regulator and probably its activity with substantial effects on structural traits of the harvested fruit.
    Bacillus thuringiensis-based Products for Insect Pest Control
    Maagd, R.A. de - \ 2015
    In: Principles of Plant-Microbe Interactions : Microbes for Sustainable Agriculture / Lugtenberg, B., Springer - ISBN 9783319085746 - p. 185 - 192.
    Bacillus thuringiensis (or Bt, as it has become generally known) is one of the oldest and widely used biological control agents and has a long history of use. Bt and a number of related bacteria produce a variety of toxins, mostly—but not exclusively- localized in the parasporal crystals, which are, together with the spores themselves, the components of the typical spore/crystal mixtures. These are used to control insect pests in agricultural crops. While Bt products quietly kept holding the first place in biological pesticide sales, interest in Bt was increased by the production and commercialization of transgenic crop plants expressing one or more Bt toxins since 1996. Here I will present a brief overview of the history, biology, and practical uses of Bt and its toxins.
    Fruit illumination stimulates cell division but has no detectable effect on fruit size in tomato (Solanum lycopersicum)
    Okello, R.C. ; Heuvelink, E. ; Visser, P.H.B. de; Lammers, M. ; Maagd, R.A. de; Marcelis, L.F.M. ; Struik, P.C. - \ 2015
    Physiologia Plantarum 154 (2015)1. - ISSN 0031-9317 - p. 114 - 127.
    arabidopsis-thaliana - elongation growth - plant development - seed development - sink metabolism - cucumber fruits - gene-expression - hormone-levels - abscisic-acid - phytochrome-b
    Light affects plant growth through assimilate availability and signals regulating development. The effects of light on growth of tomato fruit were studied using cuvettes with light-emitting diodes providing white, red or blue light to individual tomato trusses for different periods during daytime. Hypotheses tested were as follows: (1) light-grown fruits have stronger assimilate sinks than dark-grown fruits, and (2) responses depend on light treatment provided, and fruit development stage. Seven light treatments [dark, 12-h white, 24-h white, 24-h red and 24-h blue light, dark in the first 24 days after anthesis (DAA) followed by 24-h white light until breaker stage, and its reverse] were applied. Observations were made between anthesis and breaker stage at fruit, cell and gene levels. Fruit size and carbohydrate content did not respond to light treatments while cell division was strongly stimulated at the expense of cell expansion by light. The effects of light on cell number and volume were independent of the combination of light color and intensity. Increased cell division and decreased cell volume when fruits were grown in the presence of light were not clearly corroborated by the expression pattern of promoters and inhibitors of cell division and expansion analyzed in this study, implying a strong effect of posttranscriptional regulation. Results suggest the existence of a complex homeostatic regulatory system for fruit growth in which reduced cell division is compensated by enhanced cell expansion.
    A multilevel analysis of fruit growth of two tomato cultivars in response to fruit temperature
    Okello, R.C. ; Visser, P.H.B. de; Heuvelink, E. ; Lammers, M. ; Maagd, R.A. de; Struik, P.C. ; Marcelis, L.F.M. - \ 2015
    Physiologia Plantarum 153 (2015)3. - ISSN 0031-9317 - p. 403 - 418.
    cell-division - size - endoreduplication - arabidopsis - expression - expansion - genotype - plants - genes - cycle
    Fruit phenotype is a resultant of inherent genetic potential in interaction with impact of environment experienced during crop and fruit growth. The aim of this study was to analyze the genetic and physiological basis for the difference in fruit size between a small (‘Brioso’) and intermediate (‘Cappricia’) sized tomato cultivar exposed to different fruit temperatures. It was hypothesized that fruit heating enhances expression of cell cycle and expansion genes, rates of carbon import, cell division and expansion, and shortens growth duration, whereas increase in cell number intensifies competition for assimilates among cells. Unlike previous studies in which whole-plant and fruit responses cannot be separated, we investigated the temperature response by varying fruit temperature using climate-controlled cuvettes, while keeping plant temperature the same. Fruit phenotype was assessed at different levels of aggregation (whole fruit, cell and gene) between anthesis and breaker stage. We showed that: (1) final fruit fresh weight was larger in ‘Cappricia’ owing to more and larger pericarp cells, (2) heated fruits were smaller because their mesocarp cells were smaller than those of control fruits and (3) no significant differences in pericarp carbohydrate concentration were detected between heated and control fruits nor between cultivars at breaker stage. At the gene level, expression of cell division promoters (CDKB2, CycA1 and E2Fe-like) was higher while that of the inhibitory fw2.2 was lower in ‘Cappricia’. Fruit heating increased expression of fw2.2 and three cell division promoters (CDKB1, CDKB2 and CycA1). Expression of cell expansion genes did not corroborate cell size observations.
    Can interactions between Bt proteins be predicted and how should effects on non-target organisms of GM crops with multiple Bt Proteins be assessed?
    Schrijver, A. De; Clercq, P. de; Booij, K. ; Maagd, R.A. de; Frankenhuyzen, K. van - \ 2014
    Bilthoven : Cogem (CGM 2014-05) - 95 p.
    Genes expressing Bacillus thuringiensis (Bt) toxins have been incorporated into genetically modified (GM) plants to render these resistant to certain insect pests. Of particular interest have been the genes encoding Cry (Crystal) proteins, but also the gene encoding the vegetative insecticidal protein Vip3Aa has been incorporated into crop plants. Over the last decennium, GM events have been crossed through traditional breeding, resulting in stacked GM events expressing several Bt insect resistance genes. Experiments demonstrate that interactions between two or more toxins can either enhance or decrease their activity. It is thus possible that interactions between Bt proteins produced by GM plants occur and thereby influence their effect on non-target invertebrates compared to GM plants expressing just a single Bt gene. This report has been drafted as a response to a call of the Netherlands Commission of Genetic Modification (COGEM) to address two main questions: (1) can interactions between Bt proteins be predicted and (2) to what extent are studies on interactions relevant for risk/safety assessment of GM crops. The questions were tackled from an eco-toxicological angle, in particular taking into account those types of information that are relevant for risk/safety assessment of GM crops. Answering the questions was done by reviewing and considering the current knowledge on the specificity of Bt proteins, on known interactions between Bt proteins and the methods to assess these interactions, and available guidance for risk/safety assessment of GM crops combining multiple Bt proteins. Also the information reviewed in a parallel project addressing the same questions, but from a biochemical and toxicological perspective (Eco¿tat, 2014), was taken into account when formulating conclusions.
    Transcriptional control of fleshy fruit development and ripening
    Karlova, R.B. ; Chapman, N. ; David, K. ; Angenent, G.C. ; Seymour, G.B. ; Maagd, R.A. de - \ 2014
    Journal of Experimental Botany 65 (2014)16. - ISSN 0022-0957 - p. 4527 - 4541.
    mads-box gene - tomato fruit - abscisic-acid - draft genome - carotenoid accumulation - climacteric fruit - down-regulation - anthocyanin accumulation - ethylene biosynthesis - hormonal-regulation
    Fleshy fruits have evolved to be attractive to frugivores in order to enhance seed dispersal, and have become an indispensable part of the human diet. Here we review the recent advances in the understanding of transcriptional regulation of fleshy fruit development and ripening with a focus on tomato. While aspects of fruit development are probably conserved throughout the angiosperms, including the model plant Arabidopsis thaliana, it is shown that the likely orthologues of Arabidopsis genes have distinct functions in fleshy fruits. The model for the study of fleshy fruit development is tomato, because of the availability of single gene mutants and transgenic knock-down lines. In other species, our knowledge is often incomplete or absent. Tomato fruit size and shape are co-determined by transcription factors acting during formation of the ovary. Other transcription factors play a role in fruit chloroplast formation, and upon ripening impact quality aspects such as secondary metabolite content. In tomato, the transcription factors NON-RIPENING (NOR), COLORLESS NON-RIPENING (CNR), and RIPENING INHIBITOR (MADS-RIN) in concert with ethylene signalling regulate ripening, possibly in response to a developmental switch. Additional components include TOMATO AGAMOUS-LIKE1 (TAGL1), APETALA2a (AP2a), and FRUITFULL (FUL1 and FUL2). The links between this highly connected regulatory network and downstream effectors modulating colour, texture, and flavour are still relatively poorly understood. Intertwined with this network is post-transcriptional regulation by fruit-expressed micro-RNAs targeting several of these transcription factors. This important developmental process is also governed by changes in DNA methylation levels and possibly chromatin remodelling.
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