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

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Corrigendum: PolymapR - Linkage analysis and genetic map construction from F 1 populations of outcrossing polyploids
Bourke, Peter M. ; Geest, Geert Van; Voorrips, Roeland E. ; Jansen, Johannes ; Kranenburg, Twan ; Shahin, Arwa ; Visser, Richard G.F. ; Arens, Paul ; Smulders, Marinus J.M. ; Maliepaard, Chris - \ 2018
Bioinformatics 35 (2018)3. - ISSN 1367-4803 - p. 540 - 540.

In the original article, there was an incorrect formula. The formula appears in section 2.2.2, 'Linkage analysis in the presence of preferential chromosomal pairing', on page 3498. The correct formula is below in the context in which it appears. This gives rise to the likelihood function (Formula Presented) , which when solved leads to the following maximumlikelihood estimate for (Formula Presented). This has been corrected

PolymapR-linkage analysis and genetic map construction from F1 populations of outcrossing polyploids
Bourke, Peter M. ; Geest, Geert van; Voorrips, Roeland E. ; Jansen, Johannes ; Kranenburg, Twan ; Shahin, Arwa ; Visser, Richard G.F. ; Arens, Paul ; Smulders, Marinus J.M. ; Maliepaard, Chris - \ 2018
Bioinformatics 34 (2018)20. - ISSN 1367-4803 - p. 3496 - 3502.

Motivation: Polyploid species carry more than two copies of each chromosome, a condition found in many of the world's most important crops. Genetic mapping in polyploids is more complex than in diploid species, resulting in a lack of available software tools. These are needed if we are to realize all the opportunities offered by modern genotyping platforms for genetic research and breeding in polyploid crops.

Results: polymapR is an R package for genetic linkage analysis and integrated genetic map construction from bi-parental populations of outcrossing autopolyploids. It can currently analyse triploid, tetraploid and hexaploid marker datasets and is applicable to various crops including potato, leek, alfalfa, blueberry, chrysanthemum, sweet potato or kiwifruit. It can detect, estimate and correct for preferential chromosome pairing, and has been tested on high-density marker datasets from potato, rose and chrysanthemum, generating high-density integrated linkage maps in all of these crops.

Availability and implementation: polymapR is freely available under the general public license from the Comprehensive R Archive Network (CRAN) at http://cran.r-project.org/package=polymapR.

Supplementary information: Supplementary data are available at Bioinformatics online.

Chrysanthemum x morifolium Variation
Geest, G.A. van; Voorrips, R.E. ; Esselink, G. ; Post, Aike ; Visser, R.G.F. ; Arens, P.F.P. - \ 2017
PRJNA369315 - Chrysanthemum x morifolium
RNA was sequenced of thirteen chrysanthemum cultivars for SNP discovery.
Better genes for tricky plants
Maliepaard, Chris ; Geest, Geert van - \ 2017
An ultra-dense integrated linkage map for hexaploid chrysanthemum enables multi-allelic QTL analysis
Geest, Geert van; Bourke, Peter M. ; Voorrips, Roeland E. ; Marasek-Ciolakowska, Agnieszka ; Liao, Yanlin ; Post, Aike ; Meeteren, Uulke van; Visser, Richard G.F. ; Maliepaard, Chris ; Arens, Paul - \ 2017
Theoretical and Applied Genetics 130 (2017)12. - ISSN 0040-5752 - p. 2527 - 2541.
Key message: We constructed the first integrated genetic linkage map in a polysomic hexaploid. This enabled us to estimate inheritance of parental haplotypes in the offspring and detect multi-allelic QTL.Abstract: Construction and use of linkage maps are challenging in hexaploids with polysomic inheritance. Full map integration requires calculations of recombination frequency between markers with complex segregation types. In addition, detection of QTL in hexaploids requires information on all six alleles at one locus for each individual. We describe a method that we used to construct a fully integrated linkage map for chrysanthemum (Chrysanthemum × morifolium, 2n = 6x = 54). A bi-parental F1 population of 406 individuals was genotyped with an 183,000 SNP genotyping array. The resulting linkage map consisted of 30,312 segregating SNP markers of all possible marker dosage types, representing nine chromosomal linkage groups and 107 out of 108 expected homologues. Synteny with lettuce (Lactuca sativa) showed local colinearity. Overall, it was high enough to number the chrysanthemum chromosomal linkage groups according to those in lettuce. We used the integrated and phased linkage map to reconstruct inheritance of parental haplotypes in the F1 population. Estimated probabilities for the parental haplotypes were used for multi-allelic QTL analyses on four traits with different underlying genetic architectures. This resulted in the identification of major QTL that were affected by multiple alleles having a differential effect on the phenotype. The presented linkage map sets a standard for future genetic mapping analyses in chrysanthemum and closely related species. Moreover, the described methods are a major step forward for linkage mapping and QTL analysis in hexaploids.
Disentangling hexaploid genetics : towards DNA-informed breeding for postharvest performance in chrysanthemum
Geest, Geert van - \ 2017
Wageningen University. Promotor(en): R.G.F. Visser, co-promotor(en): U. van Meeteren; P.F.P. Arens. - Wageningen : Wageningen University - ISBN 9789463436427 - 142
chrysanthemum - plant breeding - postharvest quality - hexaploidy - polyploidy - quantitative trait loci - phenotypes - linkage mapping - metabolomics - polymorphism - dna - chrysanthemum - plantenveredeling - kwaliteit na de oogst - hexaploïdie - polyploïdie - loci voor kwantitatief kenmerk - fenotypen - koppelingskartering - metabolomica - polymorfisme - dna

DNA-informed selection can strongly improve the process of plant breeding. It requires the detection of DNA polymorphisms, calculation of genetic linkage, access to reliable phenotypes and methods to detect genetic loci associated with phenotypic traits of interest. Cultivated chrysanthemum is an outcrossing hexaploid with an unknown mode of inheritance. This complicates the development of resources and methods that enable the detection of trait loci. Postharvest performance is an essential trait in chrysanthemum, but is difficult to measure. This makes it an interesting but challenging trait to phenotype and detect associated genetic loci. In this thesis I describe the development of resources and methods to enable phenotyping for postharvest performance, genetic linkage map construction and detection of quantitative trait loci in hexaploid chrysanthemum.

Postharvest performance is a complicated trait because it is related to many different disorders that reduce quality. One of these disorders in chrysanthemum is disk floret degreening, which occurs after long storage. In chapter 2, we show that degreening can be prevented by feeding the flower heads with sucrose, suggesting carbohydrate starvation plays a role in the degreening process. To investigate the response to carbohydrate starvation of genotypes with different sensitivity to disk floret degreening, we investigated the metabolome of sugar-fed and carbohydrate-starved disk florets by 1H-NMR and HPAEC. We show that the metabolome is severely altered at carbohydrate starvation. In general, starvation results in an upregulation of amino acid and secondary metabolism. Underlying causes of genotypic differences explaining variation in disk floret degreening in the three investigated genotypes remained to be elucidated, but roles of regulation of respiration rate and camphor metabolism were posed as possible candidates.

In chapter 3, disk floret degreening was found to be the most important postharvest disorder after 3 weeks of storage among 44 white chrysanthemum cultivars. To investigate the inheritance of disk floret degreening, we crossed two genotypes with opposite phenotypic values of both disk floret degreening and carbohydrate content to obtain a population segregating for disk floret degreening. To phenotype the cultivar panel and the bi-parental population precisely and in a high throughput manner, we developed a method that quantified colour of detached capitula over time. This method was validated with visual observations of disk floret degreening during vase life tests. In a subset of the bi-parental population we measured carbohydrate content of the disk florets at harvest. The amount of total carbohydrates co-segregated with sensitivity to degreening, which shows that the difference in disk floret degreening sensitivity between the parents could be explained by their difference in carbohydrate content. However, the correlation was rather weak, indicating carbohydrate content is not the only factor playing a role.

In order to develop resources for DNA-informed breeding, one needs to be able to characterize DNA polymorphisms. In chapter 4, we describe the development of a genotyping array containing 183,000 single nucleotide polymorphisms (SNPs). These SNPs were acquired by sequencing the transcriptome of 13 chrysanthemum cultivars. By comparing the genomic dosage based on the SNP assay and the dosage as estimated by the read depth from the transcriptome sequencing data, we show that alleles are expressed conform the genomic dosage, which contradicts to what is often found in disomic polyploids. In line with this finding, we conclusively show that cultivated chrysanthemum exhibits genome-wide hexasomic inheritance, based on the segregation ratios of large numbers of different types of markers in two different populations.

Tools for genetic analysis in diploids are widely available, but these have limited use for polyploids. In chapter 5, we present a modular software package that enables genetic linkage map construction in tetraploids and hexaploids. Because of the modularity, functionality for other ploidy levels can be easily added. The software is written in the programming language R and we named it polymapR. It can generate genetic linkage maps from marker dosage scores in an F1 population, while taking the following steps: data inspection and filtering, linkage analysis, linkage group assignment and marker ordering. It is the first software package that can handle polysomic hexaploid and partial polysomic tetraploid data, and has advantages over other polyploid mapping software because of its scalability and cross-platform applicability.

With the marker dosage scores of the bi-parental F1 population from the genotyping array and the developed methods to perform linkage analysis we constructed an integrated genetic linkage map for the hexaploid bi-parental population described in chapter 3 and 4. We describe this process in chapter 6. With this integrated linkage map, we reconstructed the inheritance of parental haplotypes for each individual, and expressed this as identity-by-descent (IBD) probabilities. The phenotypic data on disk floret degreening sensitivity that was acquired as described in chapter 3, was used in addition to three other traits to detect quantitative trait loci (QTL). These QTL were detected based on the IBD probabilities of 1 centiMorgan intervals of each parental homologue. This enabled us to study genetic architecture by estimating the effects of each separate allele within a QTL on the trait. We showed that for many QTL the trait was affected by more than two alleles.

In chapter 7, the findings in this thesis are discussed in the context of breeding for heterogeneous traits, the implications of the mode of inheritance for breeding and the advantages and disadvantages of polyploidy in crop breeding. In conclusion, this thesis provides in general a significant step for DNA-informed breeding in polysomic hexaploids, and for postharvest performance in chrysanthemum in particular.

Conclusive evidence for hexasomic inheritance in chrysanthemum based on analysis of a 183 k SNP array
Geest, Geert van; Voorrips, Roeland E. ; Esselink, Danny ; Post, Aike ; Visser, Richard G.F. ; Arens, Paul - \ 2017
BMC Genomics 18 (2017). - ISSN 1471-2164
Allelic expression bias - Disomic - Hexaploid - Polyploid - Polysomic - RNA-seq - SNP array - SNP retrieval
Background: Cultivated chrysanthemum is an outcrossing hexaploid (2n = 6× = 54) with a disputed mode of inheritance. In this paper, we present a single nucleotide polymorphism (SNP) selection pipeline that was used to design an Affymetrix Axiom array with 183 k SNPs from RNA sequencing data (1). With this array, we genotyped four bi-parental populations (with sizes of 405, 53, 76 and 37 offspring plants respectively), and a cultivar panel of 63 genotypes. Further, we present a method for dosage scoring in hexaploids from signal intensities of the array based on mixture models (2) and validation of selection steps in the SNP selection pipeline (3). The resulting genotypic data is used to draw conclusions on the mode of inheritance in chrysanthemum (4), and to make an inference on allelic expression bias (5). Results: With use of the mixture model approach, we successfully called the dosage of 73,936 out of 183,130 SNPs (40.4%) that segregated in any of the bi-parental populations. To investigate the mode of inheritance, we analysed markers that segregated in the large bi-parental population (n = 405). Analysis of segregation of duplex x nulliplex SNPs resulted in evidence for genome-wide hexasomic inheritance. This evidence was substantiated by the absence of strong linkage between markers in repulsion, which indicated absence of full disomic inheritance. We present the success rate of SNP discovery out of RNA sequencing data as affected by different selection steps, among which SNP coverage over genotypes and use of different types of sequence read mapping software. Genomic dosage highly correlated with relative allele coverage from the RNA sequencing data, indicating that most alleles are expressed according to their genomic dosage. Conclusions: The large population, genotyped with a very large number of markers, is a unique framework for extensive genetic analyses in hexaploid chrysanthemum. As starting point, we show conclusive evidence for genome-wide hexasomic inheritance.
Betere genen voor lastige planten
Maliepaard, Chris ; Geest, Geert van - \ 2017

Plantenveredelaars krijgen steeds meer grip op de genetisch meest ingewikkelde gewassen. Goed nieuws voor bijvoorbeeld chrysantentelers die hun bloemen steeds verder over de grens verkopen. Met de juiste genen zien de chrysanten er ook na transport naar verre oorden nog fris uit.

Partial preferential chromosome pairing is genotype dependent in tetraploid rose
Bourke, Peter M. ; Arens, Paul ; Voorrips, Roeland E. ; Esselink, Danny ; Koning-Boucoiran, Carole F.S. ; Westende, Wendy van 't; Santos Leonardo, Tiago ; Wissink, Patrick ; Zheng, Chaozhi ; Geest, Geert van; Visser, Richard G.F. ; Krens, Frans A. ; Smulders, Rene ; Maliepaard, Chris - \ 2017
The Plant Journal 90 (2017)2. - ISSN 0960-7412 - p. 330 - 343.
high-density integrated map - meiotic chromosomal pairing behaviour - polyploid genetic linkage map - Rosa hybrida - segmental allopolyploid

It has long been recognised that polyploid species do not always neatly fall into the categories of auto- or allopolyploid, leading to the term ‘segmental allopolyploid’ to describe everything in between. The meiotic behaviour of such intermediate species is not fully understood, nor is there consensus as to how to model their inheritance patterns. In this study we used a tetraploid cut rose (Rosa hybrida) population, genotyped using the 68K WagRhSNP array, to construct an ultra-high-density linkage map of all homologous chromosomes using methods previously developed for autotetraploids. Using the predicted bivalent configurations in this population we quantified differences in pairing behaviour among and along homologous chromosomes, leading us to correct our estimates of recombination frequency to account for this behaviour. This resulted in the re-mapping of 25 695 SNP markers across all homologues of the seven rose chromosomes, tailored to the pairing behaviour of each chromosome in each parent. We confirmed the inferred differences in pairing behaviour among chromosomes by examining repulsion-phase linkage estimates, which also carry information about preferential pairing and recombination. Currently, the closest sequenced relative to rose is Fragaria vesca. Aligning the integrated ultra-dense rose map with the strawberry genome sequence provided a detailed picture of the synteny, confirming overall co-linearity but also revealing new genomic rearrangements. Our results suggest that pairing affinities may vary along chromosome arms, which broadens our current understanding of segmental allopolyploidy.

High-Density SNP Maps in Rose to Understand the Meiotic Behavior and Determine the Synteny with Fragaria
Smulders, M.J.M. ; Bourke, P.M. ; Arens, P.F.P. ; Voorrips, R.E. ; Geest, G.A. van; Krens, F.A. ; Visser, R.G.F. ; Maliepaard, C.A. - \ 2017
Tetraploid rose is thought to have been derived from hybridisation between up to 10 different species. This would imply it should be considered as an allopolyploid. Nevertheless, its inheritance pattern is usually considered to be that of an autopolyploid, but this has not been studied in detail. It may also fall under the term “segmental allopolyploid” to describe an in-between situation
We used a tetraploid cut rose population, genotyped using the 68K WagRhSNP Axiom array, to construct an ultra-high density linkage map using methods previously developed for autotetraploids. We mapped many markers per bin as the dense map is also intended to assist in assembly of the rose genome. Using the predicted bivalent configurations in this population, we uncovered differences in pairing behaviour between linkage groups, leading us to correct our recombination frequency estimates to take account of this behaviour. This resulted in the re-mapping of 25,695 SNP markers across the seven rose chromosomes, tailored to the pairing behaviour of each chromosome. We confirmed our findings by examining repulsion-phase linkage estimates, which also carry information about preferential pairing.

A comparison of these rose maps with the Fragaria vesca genome sequence provided a detailed picture of their synteny, which is largely colinear but also contains a few rearrangements. Our results suggest that pairing affinities may vary along chromosome arms, which may help broaden our current understanding of segmental allopolyploidy.
Breeding for postharvest performance in chrysanthemum by selection against storage-induced degreening of disk florets
Geest, Geert van; Post, Aike ; Arens, Paul ; Visser, Richard G.F. ; Meeteren, Uulke van - \ 2017
Postharvest Biology and Technology 124 (2017). - ISSN 0925-5214 - p. 45 - 53.
Breeding for postharvest performance in ornamentals is challenging, since many different deteriorative processes determine vase life. In order to improve postharvest performance by breeding, selection should take place on these processes separately. To define processes that are important for chrysanthemum postharvest performance, vase life was assessed after two weeks of cold storage in a set of 44 chrysanthemum cultivars. Since disk floret degreening was the most frequent reason for ending vase life, we further investigated this trait in a large biparental population (n = 381). To quantify disk floret degreening in this large number of genotypes, we developed a high-throughput phenotyping method. The method consists of the quantification of loss of green color as expressed by an increase of intensity of red divided by the intensity of green (R/G) in dark-held detached capitula. R/G increases when disk florets lose green color. The increase in R/G correlated significantly with the number of days until disk floret degreening occurred during vase life. This was the case for the 44-cultivar cultivar panel (Pearson’s correlation coefficient (ρ) of −0.70; p < 0.0001) as well as in a subset of the biparental pulation (n = 145; ρ = −0.67; p < 0.0001). R/G increase segregated in a quantitative manner in the full biparental population, and had a moderately high heritability of 0.73. Carbohydrate content after harvest was measured in a smaller subset of the biparental population (n = 55). The R/G increase correlated with carbohydrate content (ρ=-0.56; p < 0.0001). Since carbohydrate content did not explain all variation in degreening sensitivity, we discuss different possible mechanisms to cope with carbohydrate starvation and avoid degreening. In conclusion, disk floret degreening is an important postharvest trait in chrysanthemum, and it is related to carbohydrate starvation. The quantitative segregation suggests involvement of multiple alleles, probably at multiple loci. The moderately high heritability makes it a suitable trait for QTL mapping, which we will commence in the near future.
The role of carbohydrates in storage induced disk floret degreening in chrysanthemum
Geest, G.A. van; Post, Aike ; Arens, P. ; Meeteren, U. van - \ 2016
Acta Horticulturae 1131 (2016). - ISSN 0567-7572 - p. 81 - 86.
carbohydrate starvation, Chrysanthemum × morifolium, fructan, postharvest
Dutch-grown cut chrysanthemums are often shipped over long distances resulting in storage times of up to four weeks. One problem occurring after storage is premature degreening of disk florets. We want to understand the physiological background of disk floret degreening in order to allow breeding against sensitivity to degreening. Disk floret degreening occurs in two steps: first, there is loss of green colour resulting in yellowing, and after that, disk florets turn brown. Sucrose feeding after storage prevents disk floret degreening. Pulsing flower stems with potassium chloride with the same osmolarity compared to the sucrose treatment did not have an effect on degreening. Therefore, the effect of sucrose did not seem to be osmotic but related to energy metabolism. Because of this relation with carbohydrate metabolism, we hypothesized that genotypic differences are explained by their carbohydrate content during the postharvest phase. However, the carbohydrate content of a sensitive and insensitive genotype did not explain these genotypic differences. The sensitive genotype showed higher carbohydrate content during the postharvest phase compared to the insensitive genotype. Our results indicate that storage induced disk floret browning is caused by carbohydrate starvation, but genotypic differences are probably explained by a difference in sensitivity to carbohydrate starvation.
De ideale chrysant
Geest, Geert van - \ 2016
Hoe maak je een chrysant die niet alleen fraai is, maar ook lang fris blijft in de vaas? Tot voor kort was het een kwestie van kruisen en afwachten wat ervan komt. Maar promovendus Geert van Geest werkt gerichter, met genetische merkers. ‘Een revolutie in de bloemveredeling.’
Genotypic differences in metabolomic changes during storage induced-degreening of chrysanthemum disk florets
Geest, Geert van; Choi, Young Hae ; Arens, Paul ; Post, Aike ; Liu, Ying ; Meeteren, Uulke van - \ 2016
Postharvest Biology and Technology 115 (2016). - ISSN 0925-5214 - p. 48 - 59.
Carbohydrate starvation - Chrysanthemum - Metabolomics - Respiration - Senescence - Storage

Selecting chrysanthemum cultivars with long storability and vase life is a major challenge for breeders. The rate of degreening of disk florets during the postharvest phase is an important determinant of vase life. There is large genotypic variation in susceptibility to disk floret degreening. Our aim was to understand these genotypic differences at the physiological level. Carbohydrate starvation seemed to play a role, since application of sugars prevented degreening and degreening only occurred if florets had a long-term low carbohydrate content. In order to find out which metabolic processes could explain genotypic differences, we used 1H Nuclear Magnetic Resonance (NMR) spectroscopy profiling, High Performance Anion Exchange Chromatography (HPAEC) and respiration measurements to compare metabolic responses of three genotypes to carbohydrate starvation. HPAEC and NMR measurements showed that carbohydrate content could not fully explain genotypic differences. A genotype with intermediate sensitivity to degreening showed similar carbohydrate content compared to an insensitive one. However, respiration rate declined faster under carbohydrate starvation in a sensitive and intermediate sensitive genotype compared to an insensitive genotype, suggesting a more abrupt constraint on the mitochondrial electron transport chain and with that oxidative stress. Changes in the metabolic profile under carbohydrate starvation were diverse and revealed candidate processes associated with disk floret degreening. Camphor content increased and correlated positively with degreening insensitivity. Phenylpropanoids and flavonoids also increased upon carbohydrate starvation and the response was genotype specific. We propose the upregulation of the phenylpropanoid metabolism as important source of nitrogen in the form of harmful ammonia during carbohydrate starvation. Our results provide a framework to identify processes associated with genotypic differences in the response to carbohydrate starvation and susceptibility to floret degreening.

Can Phenotyping for Water Balance Improve Breeding for Vase Life?
Geest, G.A. van; Meeteren, U. van; Arens, P. - \ 2015
In: Proceedings of the 25th International Eucarpia Symposium Section Ornamentals: Crossing Borders. - - p. 149 - 154.
Water deficit is a main cause for early wilting of cut flowers during vase life. To prevent water deficit, water uptake from the vase should compensate transpiration. Our goal is to identify parameters characterizing water balance that explain genotypic differences in vase life. This allows more precise phenotyping of vase life related traits. In two independent experiments 19 chrysanthemum genotypes were characterized for three water balance parameters during their vase life: the maximum weight gain (MWG; maximum weight increase after placement in water) and weight loss rate (WLR; % of weight loss per time unit after MWG is reached), which together explain time to negative water balance (tWB
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