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

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Measuring stress-induced DNA methylation in apomictic Dandelions
Gurp, Thomas P. van - \ 2017
Wageningen University. Promotor(en): W.H. van der Putten, co-promotor(en): K.J.F. Verhoeven; A. Biere. - Wageningen : Wageningen University - ISBN 9789463436045 - 176
taraxacum officinale - epigenetics - dna methylation - inheritance - apomixis - environmental factors - taraxacum officinale - epigenetica - dna-methylering - overerving - apomixis - milieufactoren

The success or continuous existence of species requires continuous adaptation to changes in the environment to survive and contribute offspring to the next generation. Selection acts on the phenotype, which is in turn determined by the complex interplay of genetic, epigenetic and environmental variation. (Natural) selection leads to ‘survival of the fittest’ or best-adapted individuals to their local environment, ultimately determining which individuals contribute offspring to the next generation. Understanding the mechanisms by which epigenetic and genetic variation can arise and get passed on through generations determines our understanding of inheritance and evolution. Hitherto, the mechanistic understanding of genetics has shaped the scientific view of inheritance and evolution, leading to the gene-centered paradigm of Neo-Darwinism. However, recent studies indicate that besides genetic (DNA sequence) variation, epigenetic variation can also be transmitted between generations. Further studies on the properties and transgenerational dynamics of epigenetic variation are needed to enhance our understanding of heritability and evolution.

Epigenetic variation has distinct properties and different transgenerational dynamics compared to genetic variation. Epigenetic variation helps to regulate gene expression and determines the different cell types and function in eukaryotes. The main function of DNA methylation, an important part of the epigenetic code, is to prevent the spread of selfish genetic elements in the genome and to establish the different cellular profiles observed in multicellular organisms. One differentiating feature of epigenetic variation compared to genetic variation is that (specific) epigenetic variation can arise under the influence of stress. This can enable a trans-generational stress-response of organisms which can have a positive influence on the phenotype and (natural) selection on either the (enhanced level of) transgenerational phenotypic plasticity or the epigenetic variation itself, potentially influencing natural selection and ultimately evolution. Where genetic variation can be characterized as hard-inheritance, the inheritance of epigenetic variation is often referred to as ‘soft-inheritance’ due to the lower transgenerational stability and resetting that occurs in the intergenerational transfer of epigenetic variation. Epigenetic variation is also often dependent on, or a downstream consequence, of genetic variation, suggesting that it is (in part) determined by genetic variation.

Mechanistic studies in model species have contributed greatly to the understanding of the molecular mechanisms that control the dynamics of different epigenetic marks present in multicellular organisms. In plants, studies in the model plant Arabidopsis thaliana have resulted in deciphering the most important molecular mechanisms and actors, giving an ever-increasing insight into the dynamics of epigenetic regulation of cells and organisms. A key feature of model systems is the ability to ‘switch’ off certain genes or molecular pathways, for instance via the experimental use of mutants, enabling the study of their role in the heritability of epigenetic marks. DNA methylation is a well-studied epigenetic mark, which has shown high stability even in transgenerational experiments.

From the perspective of studying epigenetic variation, plants are particularly interesting for several reasons, most importantly: 1) The separation between soma and germline, the Weismann barrier, is less strict in plants compared to other eukaryotes, as in higher plants

germline cells are formed during floral development from somatic cells (which can occur throughout the life of the plant), whereas in most eukaryotes germline cell development is restricted to a defined point (early) in the organismal development. 2) The sessile nature of plants makes an adaptive plastic response to changing environments an important feature, a plant cannot just walk away when the going gets tough. 3) The transgenerational stability of DNA methylation is higher in plants compared to other eukaryotes such as mammals, in which epigenetic information is erased during germline reprogramming. These factors combined suggest that the potential importance of epigenetic variation in plants might be high.

In this thesis, I focus on studying DNA methylation in apomictic Dandelions, applying Next Generation Sequencing (NGS) approaches to the study of this non-model plant species. Apomictic dandelions produce seeds that are genetically identical to the ‘mother’ plant, which makes it easier to study the influence of epigenetic variation without confounding effects of genetic variation. Working with Next Generation Sequencing data is still relatively new and therefore not always optimized for specific types of analysis. I discovered a distinct error pattern in RNAseq data that indicated an artificial source of variation that could be traced back to the way the RNAseq libraries were constructed. The first publication of this thesis contains a technical analysis of such artefacts present in RNAseq data, suggesting that these errors are related to random hexamer mispriming during library construction (Chapter 2).

The main goal of my work is to better understand the role of epigenetic variation in adaptation and plasticity of plants. This role remains poorly understood. This is in part due to the lack of high-resolution techniques that allow for the detailed study of epigenetic marks such as DNA methylation in non-model organisms. Existing techniques for measuring DNA methylation such as methylation sensitive AFLPs offer only information on DNA methylation variation in an anonymous and limited fashion. The plummeting costs of sequencing techniques have enabled large-scale genotyping efforts (focusing on genetic variation only) for a wide variety of non-model organisms. Here, I extended this popular genotyping by sequencing technique, to allow for sequencing-based epigenotyping or epiGBS (chapter 3), which allows for measuring DNA methylation and genetic variation in hundreds of samples simultaneously. I have extensively validated the approach, providing evidence that with the right design, the accuracy of the DNA methylation measurements with epiGBS are as high as those with the gold standard Whole Genome Bisulfite Sequencing.

An important aim of my PhD research was to investigate the stability of (stress induced) DNA methylation variation in apomictic dandelions and the potential of phenotypic variation underpinned by DNA methylation variation to be subjected to selection. I therefore studied the transgenerational stability of both stress induced and natural DNA methylation variation in different genotypes of apomictic dandelions in a six-generation experiment, comparing DNA methylation patterns between generations and tracking changes in them (chapter 4) using epiGBS. I found clear but limited evidence for environmental induction of heritable DNA methylation changes after application of Jasmonic Acid. Furthermore, I found a significant negative relation between the similarity of DNA methylation patterns and intergenerational distance, indicating epigenetic divergence over generations. I conclude that DNA methylation in both CG and CHG (where H can be any nucleotide except for G) sequence context are heritable and that environmental perturbation can result in heritable DNA methylation changes which are however not widespread.

A prerequisite for epigenetic variation to contribute to adaptation is that epigenetic variants that affect the phenotype are heritable. To test whether an epigenetics-based selection response is possible, at least over the time course of a few generations, I selected early flowering for two subsequent generations in three genotypes of apomictic dandelions. This selection effort included lines that received a stress pre-treatment with either Jasmonic Acid or 5-azacytidine, to determine if stress-induced DNA methylation variation would increase the capacity to respond to selection. The selection experiment on flowering time (chapter 5) resulted in a shift in flowering time for all treatments in a young apomict, suggesting that natural and heritable epigenetic variation can underpin quantitative traits such as flowering time. I also found evidence for treatment induced (epi)genetic variation leading to a stronger selection response in one out of 3 genotypes. This suggests that stress- induced heritable epigenetic variation can lead to a selection response. Further study is however required to rule out genetic variants and to study the long-term stability of the variation selected upon.

Finally, in the General Discussion I summarize the findings, putting them in context with recently published studies. I reflect on the state of the field of ecological epigenetics and in what sense the epiGBS technique that I developed and other emerging techniques can contribute to a better understanding of the role of epigenetic variation in ecology and evolution. I reflect on the place of epiGBS compared to other techniques. I point out that with the growing evidence of the inadequacy and misinterpretation of MS-AFLP results a systematic review of such results by replicating the studies employing sequencing based techniques such as epiGBS instead of MS-AFLP is in order.

Concealed diversity : taxonomical, phytogeographical and phytosociological notes on brambles (Rubus L. subgen. Rubus) in north-west Europe
Haveman, Rense - \ 2017
Wageningen University. Promotor(en): Joop Schaminee, co-promotor(en): Rienk Jan Bijlsma. - Wageningen : Wageningen University - ISBN 9789463431019 - 200
rubus - diversity - taxonomy - phytogeography - geographical distribution - biogeography - apomixis - northwestern europe - rubus - diversiteit - taxonomie - plantengeografie - geografische verdeling - biogeografie - apomixis - noordwest-europa

Rubus subgen. Rubus (bramble) is one of the large plant genera in Europe, consisting of only a few sexual biological species and at least 700 apomictic lineages. In this thesis, it is argued that the stabilised apomict lineages should best be regarded species, even if their distribution area doesn’t meet the requirements of a regional species as defined in several publications by Weber. Included is a checklist of Dutch bramble species, comprising 191 species belonging to Rubus subgen. Rubus. In the Netherlands, 97 of the 191 species are classified as regional species, with a distribution area diameter under 500 km. On the basis of distribution data of bramble species in Ireland, the UK, Denmark, Germany, and the Netherlands, 12 phytogeographical bramble-regions are distinguished. Although ecological factors play a role in the realisation of these regions, it is argued that the found patterns are primarily the result of evolutionary processes. The density and species composition of Rubus scrubs in the Netherlands is studied using landscape transects. At landscape scale, the bramble species in the scrubs are not randomly distributed, causing a spatial clustering of floristically similar bramble scrubs. It was concluded that only a part of the diversity of Rubus scrubs was accounted for in the Dutch national vegetation classification, and a new scrub type (the Rubetum taxandriae) was described on the basis of these findings. Rubus scrubs are an important biotope for rare shrub species and endemic Rubus species. Additionally, scrubs rich in bramble species are important because they provide foraging and nesting habitats for numerous vertebrates and invertebrates. It is recommended to include the apomict Rubus species in biodiversity accounts, for instance in the national standard list of plant species, as well as the Red List.

Epigenetic inheritance in apomictic dandelions : stress-induced and heritable modifications in DNA methylation and small RNA
Preite, V. - \ 2016
Wageningen University. Promotor(en): Wim van der Putten, co-promotor(en): K.J.F. Verhoeven. - Wageningen : Wageningen University - ISBN 9789462578715 - 152
taraxacum officinale - epigenetics - inheritance - apomixis - dna methylation - rna - heritability - stress - taraxacum officinale - epigenetica - overerving - apomixis - dna-methylering - rna - heritability - stress

Epigenetic variation, such as changes in DNA methylations, regulatory small RNAs (sRNAs) and chromatin modifications can be induced by environmental stress. There is increasing information that such induced epigenetic modifications can be transmitted to offspring, potentially mediating adaptive transgenerational responses to environmental changes. However, it is unclear if this phenomenon is common and relevant for adaptation under natural conditions. My thesis study aimed to examine epigenetic inheritance in common and widespread apomictic dandelions (Taraxacum officinale Wig.). Due to their asexual reproduction mode by producing clonal seeds offspring from seeds are genetically uniform and thus suitable to investigate epigenetic effects that are not confounded with genetic variation.

I exposed apomictic dandelion lineages to drought and salicylic acid (SA) stress, which induces plant defense responses following pathogen attack, and found effects on patterns of DNA methylation up to two stress-free offspring generations after exposure. However, a heritable stress signal was not present in all tests and was stress- and lineage-dependent. Drought stress triggered a weak and lineage-dependent signal that was lost again in the second offspring generation. SA treatment revealed a stress-related increased rate of DNA methylation changes in the two offspring generations, but no stress signal was found in the stressed generation itself. I also observed changes in small RNA production due the drought and SA stress experienced two generations ago. These transgenerational sRNA effects showed association with gene functions related to grandparental drought and SA stress, which suggests functional relevance of the transgenerational effects.

I used a reciprocal transplantation field experiment to investigate whether exposing dandelions to natural field stresses also triggers DNA methylation changes. The experiment revealed evidence of adaptive divergence between the populations, suggesting that non-native habitats are experienced as more stressful. However, under these field conditions no induction-based DNA methylation changes were found that persisted into offspring.

By using AFLP and MS-AFLP screening of natural apomictic dandelion populations across a north-south transect in Europe I examined if natural, heritable DNA methylation variation reflects underlying genetic variation, or if it shows patterns that are not predictable from underlying genetics. I found that a large part of heritable DNA methylation differentiation along the north-south transect was correlated with genetic differentiation. However, a fraction of differentiation in heritable DNA methylation was independent from genetic variation. This suggests a potential of epigenetics to play an evolutionary role independently, at least to some extent, from underlying genetics. Overall, I found indications of epigenetic inheritance in apomictic dandelions. Whether epigenetic variation would result in adaptive phenotypic variation in nature and whether it would persist long enough to play a relevant role in adaptation remains unclear and requires further study.

Natural epigenetic variation contributes to heritable flowering divergence in a widespread asexual dandelion lineage
Wilschut, Rutger ; Oplaat, C. ; Snoek, L.B. ; Kirschner, J. ; Verhoeven, K.J.F. - \ 2016
Molecular Ecology 25 (2016)8. - ISSN 0962-1083 - p. 1759 - 1768.
dna methylation - epigenetic inheritance - apomixis - asexual reproduction - adaptation
Epigenetic variation has been proposed to contribute to the success of asexual plants, either as a contributor to phenotypic plasticity or by enabling transient adaptation via selection on transgenerationally stable, but reversible, epialleles. While recent studies in experimental plant populations have shown the potential for epigenetic mechanisms to contribute to adaptive phenotypes, it remains unknown if heritable variation in ecologically relevant traits is at least partially epigenetically determined in natural populations. Here, we tested the hypothesis that DNA methylation variation contributes to heritable differences in flowering time within a single widespread apomictic clonal lineage of the common dandelion (Taraxacum officinale s. lat.). Apomictic clone members of the same apomictic lineage collected from different field sites showed heritable differences in flowering time, which was correlated with inherited differences in methylation-sensitive AFLP marker profiles. Differences in flowering between apomictic clone members were significantly reduced after in vivo de-methylation using the DNA methyltransferase inhibitor zebularine. This synchronization of flowering times suggests that flowering time divergence within an apomictic lineage was mediated by differences in DNA methylation. While the underlying basis of the methylation polymorphism at functional flowering time-affecting loci remains to be demonstrated, our study shows that epigenetic variation contributes to heritable phenotypic divergence in ecologically relevant traits in natural plant populations. This result also suggests that epigenetic mechanisms can facilitate adaptive divergence within genetically uniform asexual lineages.
Fluorescent in situ hybridization shows DIPLOSPOROUS located on one of the NOR chromosomes in apomictic dandelions (Taraxacum) in the absence of a large hemizygous chromosomal region
Vasut, R.J. ; Vijverberg, K. ; Dijk, P.J. van; Jong, J.H.S.G.M. de - \ 2014
Genome 57 (2014)11-12. - ISSN 0831-2796 - p. 609 - 620.
genomic region - pennisetum-squamulatum - cenchrus-ciliaris - transposable elements - bdelloid rotifers - sequence-analysis - paspalum-simplex - gamete formation - mapping reveals - apomixis
Apomixis in dandelions (Taraxacum: Asteraceae) is encoded by two unlinked dominant loci and a third yet undefined genetic factor: diplosporous omission of meiosis (DIPLOSPOROUS, DIP), parthenogenetic embryo development (PARTHENOGENESIS, PAR), and autonomous endosperm formation, respectively. In this study, we determined the chromosomal position of the DIP locus in Taraxacum by using fluorescent in situ hybridization (FISH) with bacterial artificial chromosomes (BACs) that genetically map within 1.2-0.2 cM of DIP. The BACs showed dispersed fluorescent signals, except for S4-BAC 83 that displayed strong unique signals as well. Under stringent blocking of repeats by C(0)t-DNA fragments, only a few fluorescent foci restricted to defined chromosome regions remained, including one on the nucleolus organizer region (NOR) chromosomes that contains the 45S rDNAs. FISH with S4-BAC 83 alone and optimal blocking showed discrete foci in the middle of the long arm of one of the NOR chromosomes only in triploid and tetraploid diplosporous dandelions, while signals in sexual diploids were lacking. This agrees with the genetic model of a single dose, dominant DIP allele, absent in sexuals. The length of the DIP region is estimated to cover a region of 1-10 Mb. FISH in various accessions of Taraxacum and the apomictic sister species Chondrilla juncea, confirmed the chromosomal position of DIP within Taraxacum but not outside the genus. Our results endorse that, compared to other model apomictic species, expressing either diplospory or apospory, the genome of Taraxacum shows a more similar and less diverged chromosome structure at the DIP locus. The different levels of allele sequence divergence at apomeiosis loci may reflect different terms of asexual reproduction. The association of apomeiosis loci with repetitiveness, dispersed repeats, and retrotransposons commonly observed in apomictic species may imply a functional role of these shared features in apomictic reproduction, as is discussed.
Outcrossing frequency in selfing and apomictic plant species subject to containment measures in GMO development regulation
Wiel, C.C.M. van de - \ 2007
Bilthoven : Cogem (Cogem Report ) - 48
transgene planten - uitkruisen - apomixis - zelfbestuiving (selfing) - transgenic plants - outcrossing - selfing
This report was commissioned by the COGEM in order to reassess the knowledge basis on outcrossing in the plant species presently categorised as basically having a selfing breeding system in the so-called “Lijst van inhullingsverplichtingen” (“ list of inflorescence bagging regulations”), formerly called “Appendix C”
Diploid apomicts of the Boechera holboelli complex display large scale chromosome substitutions and aberrant chromosomes
Kantama, L. ; Sharbel, T.F. ; Schranz, M.E. ; Mitchell-Olds, T. ; Vries, S.C. de; Jong, J.H.S.G.M. de - \ 2007
Proceedings of the National Academy of Sciences of the United States of America 104 (2007). - ISSN 0027-8424 - p. 14026 - 14031.
in-situ hybridization - gene-expression - pennisetum-squamulatum - cenchrus-ciliaris - arabis-drummondii - b-chromosome - brassicaceae - evolution - arabidopsis - apomixis
We conducted a cytogenetic study of sexual lines of Boechera stricta and Boechera holboellii (2n = 14) and seven diploid apomictic accessions of their interspecific hybrid Boechera divaricarpa and B. holboellii (2n = 14 or 15). By studying chromosome morphology, rDNA repeats, genome painting, male meiosis, pollen morphology, and flow-cytometry seed screens, we revealed an unexpected plethora of chromosome forms, pairing behavior, and hybrid composition in all apomictic lines. Genome painting demonstrated that the apomicts are alloploid with variable numbers of B. stricta and B. holboellii-like chromosomes. We assume that large-scale homeologous chromosome substitutions took place in the apomictic hybrids that resulted from recurrent diploid-polyploid transitions through restitutional meiosis and polyploicly-diploid transitions through reductional meiosis. A second peculiarity was the presence of a largely heterochromatic chromosome (Het) in all apomictic accessions (2n = 14 and 15) and an additional smaller chromosome (Den in the aneuploids (2n = 15). Both chromosomes share repetitive pericentromere repeats with those from the sexual B. stricta, suggesting that they originated from this species. Pairing and behavior at meiosis I of the Het share features with both Y and B chromosomes and suggest that the Del arose from a translocation event or homeologous recombination between a B. holboellii (or related taxon) and a B. stricta chromosome. Based on its presence exclusively in apomictic accessions, we propose that the Het chromosome plays a role in the genetic control of apomixis.
Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apomixis in Boechera ( Brassicaceae).
Schranz, M.E. ; Kantama, L. ; Jong, J.H.S.G.M. de; Mitchell-Olds, T. - \ 2006
New Phytologist 171 (2006)2. - ISSN 0028-646X - p. 425 - 438.
holboellii brassicaceae - dandelions taraxacum - molecular markers - arabis-drummondii - poa-pratensis - apomixis - apospory - evolution - populations - inheritance
Understanding apomixis (asexual reproduction through seeds) is of great interest to both plant breeders and evolutionary biologists. The genus Boechera is an excellent system for studying apomixis because of its close relationship to Arabidopsis, the occurrence of apomixis at the diploid level, and its potentially simple inheritance by transmission of a heterochromatic (Het) chromosome. ¿ Diploid sexual Boechera stricta and diploid apomictic Boechera divaricarpa (carrying a Het chromosome) were crossed. Flow cytometry, karyotype analysis, genomic in situ hybridization, pollen staining and seed-production measurements were used to analyse the parents and resulting F1, F2 and selected F3 and test-cross (TC) generations. ¿ The F1 plant was a low-fertility triploid that produced a swarm of aneuploid and polyploid F2 progeny. Two of the F2 plants were fertile near-tetraploids, and analysis of their F3 and TC progeny revealed that they were sexual and genomically stabilized. ¿ The apomictic phenotype was not transmitted by genetic crossing as a single dominant locus on the Het chromosome, suggesting a complex genetic control of apomixis that has implications for future genetic and evolutionary analyses in this group
Use of the SSLP-based method for detection of rare apomictic events in a sexual AtSERK1 transgenic Arabidopsis population
Kantama, L. ; Lambert, J.M. ; Hu, H. ; Jong, H. de; Vries, S.C. de; Russinova, E. - \ 2006
Sexual Plant Reproduction 19 (2006)2. - ISSN 0934-0882 - p. 73 - 82.
polycomb group gene - poa-pratensis l - somatic embryogenesis - apomixis - expression - fertilization - seeds - embryos - growth - strategies
Here we present a screening method to evaluate the potential of genes to transfer aspects of apomixis into sexual crop plants. Based on the assumption that an apomictic progeny is an exact genetic replica of the mother plant we employed a set of single sequence length polymorphism (SSLP) markers to identify individuals displaying heterozygosity fixation in segregating sexual populations as an indication of rare apomictic events. Here we present the results of such a study using the Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 (AtSERK1) gene expressed under the control of the AtLTP1 promoter in sexual Arabidopsis plants. In one of the three tested F2 transgenic populations expressing the AtLTP1::AtSERK1 construct we observed two plants with heterozygosity maintenance for the full set of SSLP markers indicating a possible clonal inheritance. However, as their offspring revealed a close to binomial segregation for a number of heterozygous loci, it was concluded that these two putative apomictic plants either lost their clonal ability in the next generation or resulted from incidental recombination events displaying the genotype of the parent
Unique genomic configuration revealed by microsatellite DNA in polyploid dogroses, Rosa sect.Caninae.
Nybom, H. ; Esselink, G.D. ; Werlemarkt, G. ; Leus, I.E. ; Vosman, B.J. - \ 2006
Journal of Evolutionary Biology 19 (2006)2. - ISSN 1010-061X - p. 635 - 648.
skewed distribution - molecular markers - origin - evolution - l. - inheritance - apomixis - behavior - complex - crosses
An allopolyploid complex with high genomic integrity has been studied. Dogroses transmit only seven chromosomes (from seven bivalents) through the pollen, whereas 21, 28 or 35 chromosomes (from seven bivalents and 14, 21 or 28 univalents) come from the egg cells. Seedlings derived from two interspecific crosses were analysed with flow cytometry and molecular markers to determine ploidy level, mode of reproduction and genomic constitution. Evidence was obtained for the formation of unreduced male and female gametes, which can take part in fertilization (producing seedlings with higher ploidy than the parental plants) or in apomictic reproduction. Random amplified polymorphic DNA (RAPD) and microsatellite analyses indicated that three seedlings (5%) were derived through apomixis, whereas the other 49 were hybrids. Bivalent formation appears to involve chromosomes that consistently share the same microsatellite alleles. Allele-sharing between the maternally transmitted and highly conserved univalent-forming chromosomes reflected the taxonomic distance between different genotypes. The frequently recombining bivalent-forming chromosomes were taxonomically less informative
Chromosome studies and genetic analysis of natural and synthetic apomictic model species
Kantama, L. - \ 2005
Wageningen University. Promotor(en): Sacco de Vries, co-promotor(en): Hans de Jong; E.T. Russinova. - [S.l.] : S.n. - ISBN 9085043212 - 120
chromosoomanalyse - genetische analyse - karyotypen - apomixis - brassicaceae - chromosome analysis - genetic analysis - karyotypes - apomixis - brassicaceae
Biogeographic distribution of polyploidy and B chromosomes in the apomictic Boechera holboellii complex
Sharbel, T.F. ; Mitchell-Olds, T. ; Dobes, C. ; Kantama, L. ; Jong, J.H.S.G.M. de - \ 2005
Cytogenetic and Genome Research 109 (2005)1-3. - ISSN 1424-8581 - p. 283 - 292.
arabis-holboellii - molecular systematics - natural-populations - rust infection - brassicaceae - evolution - plants - arabidopsis - mechanisms - apomixis
The Boechera holboellii complex comprises B. holboellii and B. drummondii, both of which can reproduce through sex or apomixis. Sexuality is associated with diploid individuals, whereas apomictic individuals are diploid or triploid and may additionally have B chromosomes. Using flow cytometry and karyotype analysis, we have shown that B chromosomes (a) occur in both diploid and triploid apomictic B. holboellii, (b) may occur in triploid B. drummondii, and (c) are dispensable for the plant. Both diploid and triploid karyotypes are found in multiple chloroplast haplotypes of both species, suggesting that triploid forms have originated multiple times during the evolution of this complex. B chromosome carriers are found in geographically and genetically distinct popu-lations, but it is unknown whether the extra chromosomes are shared by common descent (single origin) or have originated via introgressive hybridization and repeated transitions from diploidy to triploidy. Diploid plants containing the Bs reproduce apomictically, suggesting that the supernumerary elements are associated with apomixis. Finally, our analyses of pollen size and viability suggest that irregular chromosome segregation in some triploid lineages may lead to the generation of diploid individuals which carry the B chromosomes.
Is the aneuploid chromosome in an apomictic Boechera holboellii a genuine B chromosome?
Sharbel, T.F. ; Voigt, M.L. ; Mitchell-Olds, T. ; Kantama, L. ; Jong, J.H.S.G.M. de - \ 2004
Cytogenetic and Genome Research 106 (2004)2-4. - ISSN 1424-8581 - p. 173 - 183.
arabis-holboellii - evolutionary genetics - molecular systematics - natural-populations - rust infection - brassicaceae - apomixis - arabidopsis - plants - parthenogenesis
The Boechera holboellii complex comprises B. holboellii and B. drummondii, both of which can reproduce through sex or apomixis. Sexuality is associated with diploidy, whereas apomictic individuals can either be diploid, aneuploid or triploid. Aneuploid individuals are found in geographically and genetically distinct populations and contain a single extra chromosome. It is unknown whether the supernumerary chromosomes are shared by common descent (single origin) or have originated via introgressive hybridizations associated with the repeated transition from diploidy to triploidy. Diploid plants containing the extra chromosome(s) reproduce apomictically, suggesting that the supernumerary elements are associated with apomixis. In this study we compared flow cytometry data, chromosome morphology, and DNA sequences of sexual diploid and apomictic aneuploids in order to establish whether the extra chromosome fits the classical concept of a B chromosome. Karyotype analyses revealed that the supernumerary chromosome in the metaphase complement is heterochromatic and often smaller than the A chromosomes, and differs in length between apomictic plants from different populations. DNA sequence analyses furthermore demonstrated elevated levels of non-synonymous substitutions in one of the alleles, likely that on the aneuploid chromosome. Although the extra chromosome in apomictic Boechera does not go through normal reductional meiosis, in which it may get eliminated or accumulated by a B-chromosome-specific process, its variable size and heterochromatic nature does meet the remaining criteria for a genuine B chromosome in other species. Its prevalence and conserved genetic composition nonetheless implies that this chromosome, if truly a B, may be atypical with respect to its influence on its carriers. Copyright (C) 2004 S. Karger AG, Basel.
Microsatellite DNA marker inheritance indicates preferential pairing between two highly homologous genomes in polyploid and hemisexual dogroses, Rosa L. sect. Caninae DC
Nybom, H. ; Esselink, D. ; Werlemarkt, G. ; Vosman, B.J. - \ 2004
Heredity 92 (2004)3. - ISSN 0018-067X - p. 139 - 150.
cultivar identification - skewed distribution - ssr markers - plants - drawings - rapd - hybridization - dogroses - apomixis - crosses
According to previous cytological evidence, the hemisexual dog-rose species, Rosa sect. Caninae, transmit only seven chromosomes (derived from seven bivalents) through their pollen grains, whereas egg cells contain 21, 28 or 35 chromosomes (derived from seven bivalents and 14, 21 or 28 univalents) depending on ploidy level. Two sets of reciprocal pairwise interspecific crosses involving the pentaploid species pair R. dumalis and R. rubiginosa, and the pentaploid/tetraploid species pair R. sherardii and R. villosa, were analysed for 13 and 12 microsatellite DNA loci, respectively. Single loci were represented by a maximum of three simultaneously occurring alleles in R. villosa, and four alleles in the other three parental plants. In the experimentally derived offspring, the theoretical maximum of five alleles was found for only one locus in the pentaploid progenies. Microsatellite DNA allele composition was identical with that of the maternal parent in 10 offspring plants, which were probably derived through apomixis. Almost all microsatellite DNA alleles were shared with the maternal parent also in the remaining offspring, but 1-4 alleles shared only with the paternal parent, indicating sexual seed formation. Analysis of quantitative peak differences allowed a tentative estimation of allelic configuration in the individual plants, and suggested that bivalent formation preferentially takes place between chromosomes that consistently share the same microsatellite alleles and therefore appear to be highly homologous. Moreover, alleles that were shared between the species in each cross combination comparatively often appear to reside on the bivalent-forming chromosomes, whereas species-specific alleles instead occur comparatively often on the univalent-forming chromosomes and are therefore inherited through the maternal parent only. Recombination then takes place between very similar genomes also in interspecific crosses, resulting in a reproduction system that is essentially a mixture between apomixis and selfing.
A genetic linkage map of the diplosporous chromosomal region in Taraxacum officinale (common dandelion; Asteracaea)
Vijverberg, K. ; Hulst, R.G.M. van der; Lindhout, W.H. ; Dijk, P.J. - \ 2004
Theoretical and Applied Genetics 108 (2004)4. - ISSN 0040-5752 - p. 725 - 732.
linked molecular markers - paspalum-simplex - resistance genes - apomixis - apospory - identification - hybrids - locus - parthenogenesis - hemizygosity
In this study, we mapped the diplosporous chromosomal region in Taraxacum officinale, by using amplified fragment length polymorphism technology (AFLP) in 73 plants from a segregating population. Taraxacum serves as a model system to investigate the genetics, ecology, and evolution of apomixis. The genus includes sexual diploid as well as apomictic polyploid, mostly triploid, plants. Apomictic Taraxacum is diplosporous, parthenogenetic, and has autonomous endosperm formation. Previous studies have indicated that these three apomixis elements are controlled by more than one locus in Taraxacum and that diplospory inherits as a dominant, monogenic trait (Ddd; DIP). A bulked segregant analysis provided 34 AFLP markers that were linked to DIP and were, together with two microsatellite markers, used for mapping the trait. The map length was 18.6 cM and markers were found on both sides of DIP, corresponding to 5.9 and 12.7 cM, respectively. None of the markers completely co-segregated with DIP. Eight markers were selected for PCR-based marker development, of which two were successfully converted. In contrast to all other mapping studies of apomeiosis to date, our results showed no evidence for suppression of recombination around the DIP locus in Taraxacum. No obvious evidence for sequence divergence between the DIP and non-DIP homologous loci was found, and no hemizygosity at the DIP locus was detected. These results may indicate that apomixis is relatively recent in Taraxacum.
Taraxacum sect. Erythrosperma in Moravia (Czech Republic): Taxonomic notes and the distribution of previously described species
Vasut, R. - \ 2003
Preslia 75 (2003)4. - ISSN 0032-7786 - p. 311 - 338.
apomictic dandelions taraxacum - population-structure - ruderalia - evolution - apomixis - recombination - clonality - sections - crosses - europe
Dandelions (Taraxacum) of the section Erythrosperma were studied in Moravia, Czech Republic, where both sexual diploid and apomictic polyploid species occur. Diploid species T. erythrospermum grows in the warmest part of southern Moravia and is confined to natural dry grasslands, whereas some apomictic species have ranges extending up to the submontane regions and prefer ruderal habits. Altogether, 21 apomictic types were found repeatedly but only seven were identified as previously described species: T. arcuatum, T. danubium, T. lacistophylloides, T. parnassicum, T. plumbeum, T. proximum and T. scanicum. Descriptions, notes on variation and distribution in Moravia, dot maps and pictures are given for eight species.
Sexual and apomictic reproduction in Hieracium sub genus Pilosella are closely interrelated developmental pathways
Tucker, M.R. ; Araujo, A.C.G. ; Paech, N.A. ; Hecht, V. ; Schmidt, E.D.L. ; Rossel, J.B. ; Vries, S.C. de; Koltunow, A.M. - \ 2003
The Plant Cell 15 (2003). - ISSN 1040-4651 - p. 1524 - 1537.
endosperm development - arabidopsis-thaliana - pattern-formation - ovule development - seed development - apomixis - expression - gene - embryo - fertilization
Seed formation in flowering plants requires meiosis of the megaspore mother cell (MMC) inside the ovule, selection of a megaspore that undergoes mitosis to form an embryo sad, and double fertilization to initiate embryo and endosperm formation. During apomixis, or asexual seed formation, in Hieracium ovules, a somatic aposporous initial (All) cell divides to form a structurally variable aposporous embryo sac and embryo. This entire process, including endosperm development, is fertilization independent. Introduction of reproductive tissue marker genes into sexual and apomictic Hieracium showed that Al cells do not express a MMC marker. Spatial and temporal gene expression patterns of other introduced genes were conserved commencing with the first nuclear division of the Al cell in apomicts and the mitotic initiation of embryo sac formation in sexual plants. Conservation in expression patterns also occurred during embryo and endosperm development, indicating that sexuality and apomixis are interrelated pathways that share regulatory components. The induction of a modified sexual reproduction program in Al cells may enable the manifestation of apomixis in Hieracium.
Comparative cyto-embryological investigations of sexual and apomictic dandelions (Taraxacum) and their apomictic hybrids
Baarlen, P. van; Jong, J.H. de; Dijk, P.J. - \ 2002
Sexual Plant Reproduction 15 (2002)1. - ISSN 0934-0882 - p. 31 - 38.
apomixis - crosses
In the autonomous apomictic Taraxacum offinale (common dandelion), parthenogenetic egg cells develop into embryos and central cells into endosperm without prior fertilisation. Unreduced (2n) megaspores are formed via meiotic diplospory, a nonreductional type of meiosis. In this paper, we describe the normal developmental pathways of sexual and apomictic reproduction and compare these with the development observed in the apomictic hybrids. In sexual diploids, a standard type of megasporogenesis and embryo sac development is synchronised between florets in individual capitula. In contrast, we observed that megasporogenesis and gametogenesis proceeded asynchronously between florets within a single capitulum of natural triploid apomicts. In addition, autonomous endosperm and embryo development initiated independently within individual florets. Parthenogenetic initiation of embryo development in outdoor apomicts was found to be temperature-dependent. Egg cells produced in natural apomicts were not fertilised after pollination with haploid pollen grains although pollen tubes were observed to grow into their embryo sacs. Both reductional and diplosporous megasporogenesis were observed in individual inflorescences of triploid apomictic hybrids. Embryo and endosperm development initiated independently in natural and hybrid apomicts.
Apomixis in Taraxacum : an embryological and genetic study = Apomixie in Taraxacum : een embryologische en genetische studie
Baarlen, P. van - \ 2001
Wageningen University. Promotor(en): R.F. Hoekstra; P.J. van Dijk; J.H. de Jong. - S.l. : S.n. - ISBN 9789058084736 - 127
taraxacum - apomixis - embryologie - genetica - taraxacum - apomixis - embryology - genetics

Apomixis is asexual plant reproduction through seeds that are produced with no prior genome reduction or fertilisation. The use of apomixis holds enormous potential for future plant breeding and production. The outcome of the research described in this thesis suggests that the genetic basis for apomixis in Taraxacum (dandelions) comprises three major dominant genes whose timely expression may be influenced by modifier genes. Its also suggests that genome interactions effect successful establishment of apomixis in polyploid hybrids of sexual x apomictic dandelions. The work consisted of cytogenetic and embryological studies performed at the Laboratory of Genetics, Wageningen University, and the analysis of inheritance of apomixis in sexual x apomict crossings performed at the Netherlands Institute of Ecology, Centre for Terrestrial Ecology, (NIOO-CTO), Heteren, the Netherlands. A theoretical model for the Taraxacum type of apomixis is described. As a conclusion, we discuss several aspects of the evolution of apomixis in Taraxacum which serve to explain why Taraxacum is a very successful genus.

Apomixis in Brachiaria decumbens Stapf
Dusi, D.M.A. - \ 2001
Wageningen University. Promotor(en): M.T.M. Willemse. - S.l. : S.n. - ISBN 9789058083579 - 167
urochloa decumbens - poaceae - apomixis - koolhydraatmetabolisme - moleculaire genetica - genexpressie - urochloa decumbens - poaceae - apomixis - carbohydrate metabolism - molecular genetics - gene expression

Apomixis is asexual reproduction leading to a seed. It is the predominant mode of reproduction in grasses of the genus Brachiaria.

Brachiaria decumbens is one of the widely cultivated species of grasses in the tropical areas. The knowledge about the mechanisms of apomixis and the possibility of controlling this system will extend the possibilities of introducing variability in Brachiaria and will maintain the apomictic character desirable for its propagation.

A comparison of gametophyte development between a sexual diploid (D4) and an apomictic tetraploid (D58) genotype of Brachiaria decumbens was made.

A calendar made based on the development in time show the differences between sexual and apomictic development. The aposporic embryo sac of the Panicum type grows faster than the Polygonum meiotic one. The apospore initials in Brachiaria decumbens were observed very early in the ovule, next to archespore or to the meiocyte. During microspore and ovule development, the pattern of callose deposition was different in sexual and apomictic plants.The distribution of the nuclei, positioned in one pole in the aposporic embryo sac allowed to differentiate them from the bipolar distribution of the nuclei observed in meiotic embryo sacs of the sexual plants. Cellularisation took place early in aposporic embryo sac and by the time of anthesis embryogenesis had already started in the apomict. In ovules of apomictic plants many embryo sacs developed. Apomixis expressed in the female side, had also an influence on the male side.

Histochemical tests developed to localise the in situ sucrose synthase or invertase activity were used during ovule development in an apomictic and a sexual genotype of Brachiaria decumbens . A delay of activity of both enzymes was observed in apomictic compared to the sexual development. This delay was also reflected by the amount of carbohydrates detected in a HPLC assay. Furthermore antibodies were used to localise the enzyme in the cell. The higher level of carbohydrates detected in the early stages of development in the sexual plant is in line with the amount of enzyme and its activity. The retarded metabolism of carbohydrate in the apomict could be related to the entrance of the apospore directly in gametophytic pathway leading to a faster embryo sac development.

Total mRNA pattern as observed by labelling poly A tails did not detect the differences in expression in sexual and apomictic plant ovules. But the difference found in the in situ amount of total RNA showed a change in metabolism of cells that are differentiating from nucellar cells in the chalazal side of the archespore or meiocyte during aposporic development. Such cells the first initial apospores also showed ribosome population that differ from other nucellar cells. In the sexual plant, the presence of some particular cells in the nucellus at chalazal side of the meiocyte suggested a silent aposporic capacity of this tissue. If such cells could develop into apospore initials under other conditions, like polyploidisation, is not known. In our observations the diploid plants never developed apospores in any stage of ovule development. Only studies with artificial polyploids could give a clue to these questions.

Differential display of mRNA was used for identifying and cloning differentially expressed genes related to apomictic and sexual ovule development. The in situ pattern of expression of two selected sequences showed that the differential bands were in reality not exclusively expressed in one stage and one type of reproductive development. Yet, one of the sequences (4-29), similar to a membrane protein, had a pattern of expression that differs in ovules of sexual and apomictic plants and during the stages of ovule development.

An in situ pattern of expression of a somatic embryogenesis receptor-like kinase gene isolated from Arabidopsis thaliana (AtSERK1) is presented on the sexual and apomictic plant. This gene was expressed in early stages of somatic and zygotic embryogenesis. It is though to play important function in cells with embryonic capacity. In an apomictic and sexual genotypes of Brachiaria decumbens , distinct pattern of expression of this gene was observed in mature ovules before and after anthesis. The occasional expression of this gene before anthesis in the egg apparatus of the apomict pointed to briefly and transiently expression of this gene, that in contrary might be necessary for longer time in the development of the zygotic embryo.

Finally, the data found in the sexual and apomictic plant of Brachiaria was compiled to characterise the reproduction processes. The existing theories about the origin of apomixis are summarised and some consideration was made based on the data observed in Brachiaria .

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