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

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.

Fast Diploidization in Close Mesopolyploid Relatives ofArabidopsis

“…The identification of the ACK as an ancestral karyotype of the closest relatives of the Australian Camelineae species further corroborate our conclusion that these allopolyploids originated from hybridization between taxa with ACK-derived complements. Although a recurrent origin of allopolyploid species was reported for Arabidopsis kamchatica (Shimizu-Inatsugi et al, 2009), Helianthus (Schwarzbach and Rieseberg, 2002), Tragopogon (Lim et al, 2008), Persicaria (Kim et al, 2008), and other genera, we are unable to find clear evidence for recurrent polyploid formation from our data. On the contrary, two paracentric inversions on one of the AK8-like homoeologs shared by five analyzed species (see Supplemental Figure 2 online) as well as the estimated large evolutionary distance between the parental genomes (;4 million years old at the time of the allopolyploidization; see Supplemental Figure 5 online) argue in favor of a single origin.…”

“…Both inter-and intragenomic translocations between nonhomoeologous chromosomes prevail in the three diploidized species. Similar large-scale chromosome reshuffling was reported, for example, in natural and synthetic polyploid B. napus (Parkin et al, 2005;Gaeta et al, 2007), Tragopogon allopolyploids (Lim et al, 2008), and in fertile Festulolium hybrids (Kopecký et al, 2008).…”

Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids

“…Ownbey (1950) observed multivalent formation in early generations of natural T. miscellus, and the patterns of isozyme variation in T. miscellus are consistent with homoeologous recombination (Soltis et al, 1995). More recently, Lim et al (2008) and Tate et al (in press) reported multivalent formation in both natural and synthetic Tragopogon allopolyploids, along with unisomy, trisomy and reciprocal translocations in natural Tragopogon allopolyploids. Thus, it seems that in T. miscellus homoeologue loss is an ongoing consequence of allopolyploidy, rather than an instantaneous event following allopolyploidisation.…”

Patterns of chromosomal variation in natural populations of the neoallotetraploid Tragopogon mirus (Asteraceae)

“…The existence of chromosomal variation in T. mirus was revealed in an earlier study, with six out of seven plants showing deviations 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(Chester et al, , 2013, we can now identify cytogenetic similarities and differences on a perchromosome basis.…”