Rapid Chromosome Evolution in Recently Formed Polyploids in Tragopogon (Asteraceae)

University of Massachusetts Amherst, United States of America
PLoS ONE (Impact Factor: 3.53). 10/2008; 3(10):e3353. DOI: 10.1371/journal.pone.0003353
Source: PubMed

ABSTRACT Polyploidy, 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.
Applications 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 (S(0) and S(1) 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.
These 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.

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Available from: Jennifer A Tate, Jul 31, 2015
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    • "Interestingly , premeiotic, somatic events are reported in Drosophila that have led to rDNA locus deletion (Ritossa et al., 1966). Aberrant karyotypes can also occur at high frequencies among individuals of wild Tragopogon allotetraploids (Lim et al., 2008), reflecting meiotic instability. Potentially, karyotypic changes and deletions of rDNA Figure 5 Methylation levels of C's in the P-genome promoter. "
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    ABSTRACT: To study the relationship between uniparental rDNA (encoding 18S, 5.8S and 26S ribosomal RNA) silencing (nucleolar dominance) and rRNA gene dosage, we studied a recently emerged (within the last 80 years) allotetraploid Tragopogon mirus (2n=24), formed from the diploid progenitors T. dubius (2n=12, D-genome donor) and T. porrifolius (2n=12, P-genome donor). Here, we used molecular, cytogenetic and genomic approaches to analyse rRNA gene activity in two sibling T. mirus plants (33A and 33B) with widely different rRNA gene dosages. Plant 33B had ~400 rRNA genes at the D-genome locus, which is typical for T. mirus, accounting for ~25% of total rDNA. We observed characteristic expression dominance of T. dubius-origin genes in all organs. Its sister plant 33A harboured a homozygous macrodeletion that reduced the number of T. dubius-origin genes to about 70 copies (~4% of total rDNA). It showed biparental rDNA expression in root, flower and callus, but not in leaf where D-genome rDNA dominance was maintained. There was upregulation of minor rDNA variants in some tissues. The RNA polymerase I promoters of reactivated T. porrifolius-origin rRNA genes showed reduced DNA methylation, mainly at symmetrical CG and CHG nucleotide motifs. We hypothesise that active, decondensed rDNA units are most likely to be deleted via recombination. The silenced homeologs could be used as a 'first reserve' to ameliorate mutational damage and contribute to evolutionary success of polyploids. Deletion and reactivation cycles may lead to bidirectional homogenisation of rRNA arrays in the long term.Heredity advance online publication, 24 December 2014; doi:10.1038/hdy.2014.111.
    Heredity 12/2014; 114(3). DOI:10.1038/hdy.2014.111 · 3.80 Impact Factor
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    • "from the expected parentally additive karyotype (Lim et al., 2008). By applying an updated methodology that allows all individual chromosomes to be identified (Chester et al., 2012, 2013), we can now identify cytogenetic similarities and differences on a perchromosome basis. "
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    ABSTRACT: Cytological studies have shown many newly formed allopolyploids (neoallopolyploids) exhibit chromosomal variation as a result of meiotic irregularities, but few naturally occurring neoallopolyploids have been examined. Little is known about how long chromosomal variation may persist and how it might influence the establishment and evolution of allopolyploids in nature. In this study we assess chromosomal composition in a natural neoallotetraploid, Tragopogon mirus, and compare it with T. miscellus, which is an allotetraploid of similar age (~40 generations old). We also assess whether parental gene losses in T. mirus correlate with entire or partial chromosome losses. Of 37 T. mirus individuals that were karyotyped, 23 (62%) were chromosomally additive of the parents, whereas the remaining 14 individuals (38%) had aneuploid compositions. The proportion of additive versus aneuploid individuals differed from that found previously in T. miscellus, in which aneuploidy was more common (69%; Fisher's exact test, P=0.0033). Deviations from parental chromosome additivity within T. mirus individuals also did not reach the levels observed in T. miscellus, but similar compensated changes were observed. The loss of T. dubius-derived genes in two T. mirus individuals did not correlate with any chromosomal changes, indicating a role for smaller-scale genetic alterations. Overall, these data for T. mirus provide a second example of prolonged chromosomal instability in natural neoallopolyploid populations.Heredity advance online publication, 5 November 2014; doi:10.1038/hdy.2014.101.
    Heredity 11/2014; 114(3). DOI:10.1038/hdy.2014.101 · 3.80 Impact Factor
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    • "Repeated patterns of homeolog loss and retention have been reported across multiple origins of both T. mirus and T. miscellus ( Tate et al., 2006 , 2009 ; Koh et al., 2010 ; Buggs et al., 2012 ). Furthermore, in T. miscellus , loci belonging to certain gene ontology (GO) categories were disproportionately more likely to be lost, and patterns of loss and retention after 40 generations in this young polyploid were similar to those discovered for much older (40 Myr) WGDs in Asteraceae ( Barker et al., 2008 ). Over longer evolutionary time, patterns of duplicate gene retention and loss appear to be related to gene function (e.g., Paterson et al., 2006 ; Barker et al., 2008 ; Severin et al., 2011 ; De Smet et al., 2013 ). "
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    ABSTRACT: Polyploidy has long been considered a major force in plant evolution. G. Ledyard Stebbins, Jr., an architect of the Modern Synthesis, elegantly addressed a broad range of topics, from genes to chromosomes to deep phylogeny, but some of his most lasting insights came in the study of polyploidy. Here, we review the immense impact of his work on polyploidy over more than 60 years, from his entrance into this fledgling field in the 1920s until the end of his career. Stebbins and his contemporaries developed a model of polyploid evolution that persisted for nearly half a century. As new perspectives emerged in the 1980s and new genetic tools for addressing key aspects of polyploidy have become available, a new paradigm of polyploidy has replaced much of the Stebbinsian framework. We review that paradigm shift and emphasize those areas in which the ideas of Stebbins continue to propel the field forward, as well as those areas in which the field was held back; we also note new directions that plant geneticists and evolutionists are now exploring in polyploidy research. Perhaps the most important conclusion from recent and ongoing studies of polyploidy is that, following Levin and others, polyploidy may propel a population into a new adaptive sphere given the myriad changes that accompany genome doubling.
    American Journal of Botany 07/2014; 101(7). DOI:10.3732/ajb.1400178 · 2.46 Impact Factor
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