Abstract
BackgroundPolyploidy, frequently termed “whole genome duplication”, is a major force in the evolution of many eukaryotes. Indeed, most angiosperm species have undergone at least one round of polyploidy in their evolutionary history. Despite enormous progress in our understanding of many aspects of polyploidy, we essentially have no information about the role of chromosome divergence in the establishment of young polyploid populations. Here we investigate synthetic lines and natural populations of two recently and recurrently formed allotetraploids Tragopogon mirus and T. miscellus (formed within the past 80 years) to assess the role of aberrant meiosis in generating chromosomal/genomic diversity. That diversity is likely important in the formation, establishment and survival of polyploid populations and species.Methodology/Principal FindingsApplications of fluorescence in situ hybridisation (FISH) to natural populations of T. mirus and T. miscellus suggest that chromosomal rearrangements and other chromosomal changes are common in both allotetraploids. We detected extensive chromosomal polymorphism between individuals and populations, including (i) plants monosomic and trisomic for particular chromosomes (perhaps indicating compensatory trisomy), (ii) intergenomic translocations and (iii) variable sizes and expression patterns of individual ribosomal DNA (rDNA) loci. We even observed karyotypic variation among sibling plants. Significantly, translocations, chromosome loss, and meiotic irregularities, including quadrivalent formation, were observed in synthetic (S0 and S1 generations) polyploid lines. Our results not only provide a mechanism for chromosomal variation in natural populations, but also indicate that chromosomal changes occur rapidly following polyploidisation.Conclusions/SignificanceThese data shed new light on previous analyses of genome and transcriptome structures in de novo and establishing polyploid species. Crucially our results highlight the necessity of studying karyotypes in young (<150 years old) polyploid species and synthetic polyploids that resemble natural species. The data also provide insight into the mechanisms that perturb inheritance patterns of genetic markers in synthetic polyploids and populations of young natural polyploid species.
Highlights
Polyploidy has played a major role in generating angiosperm biodiversity
GISH labelling enabled the genomic origin of the chromosomes to be determined by fluorescence colour: digoxingenin-labelled genomic DNA of T. dubius labelled chromosomes of T. dubius origin green or yellow (D-genome) and biotin-labelled genomic DNA of either T. pratensis or T. porrifolius labelled the P-genome orange or red
The homologous group assigned to each chromosome (A–F) was determined using size, arm ratio, position of 5S and 45S ribosomal DNA (rDNA), as described in Pires et al [24], and by using DAPI bright bands that were revealed after denaturation in some metaphases
Summary
Polyploidy has played a major role in generating angiosperm biodiversity. Chromosome counts suggest that between 30 and 80% of angiosperm species are polyploid, while genomic studies of selected model and crop species reveal evidence of extensive ancient genome-wide multiplications. Recent genomic investigations indicate that most, if not all, angiosperm species have undergone at least one genome duplication event in their evolutionary history, and several have evidence of multiple polyploidy-diploidisation-polyploidy cycles [1,2,3]. Angiosperm genomes are astonishingly plastic in their ability to tolerate considerable karyotypic (e.g. chromosome number variation, translocations), genetic (mutations, retroelement transpositon, deletions) and epigenetic (DNA methylation, histone methylation/acetylation) variability. This tolerance enables polyploids to form and establish and has contributed significantly to their widespread occurrence [4]. That diversity is likely important in the formation, establishment and survival of polyploid populations and species
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