Most cited article - PubMed ID 24400905
The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure
The ancestral crucifer karyotype and 22 conserved genomic blocks (CGBs) facilitate phylogenomic analyses in the Brassicaceae. Chromosomal rearrangements reshuffled CGBs of ancestral chromosomes during karyotype evolution. Here, we identify eight protochromosomes representing the common ancestral karyotype (ACBK) of the two Brassicoideae supertribes: Camelinodae (Lineage I) and Brassicodae (Lineage II). The characterization of multiple cascading fusion events allows us to infer evolutionary relationships based on these events. In the Camelinodae, the ACBK first evolved into the AKI genome, which remained conserved in the Cardamineae, whereas it was altered to tAKI by a reciprocal translocation that preceded the diversification of most Camelinodae tribes. The identified fusion breakpoints largely overlap with CGB boundaries, suggesting that CGBs are mainly disrupted by chromosome fusions. Our results demonstrate the stable inheritance of chromosome fusions and their importance for reconstructing evolutionary relationships. The chromosomal breakpoint approach provides a basis for ancestral state reconstruction based on chromosome-level genome assemblies.
Polyploidization can provide a wealth of genetic variation for adaptive evolution and speciation, but understanding the mechanisms of subgenome evolution as well as its dynamics and ultimate consequences remains elusive. Here, we report the telomere-to-telomere (T2T) gap-free reference genome of allotetraploid horseradish (Armoracia rusticana) sequenced using a comprehensive strategy. The (epi)genomic architecture and 3D chromatin structure of the A and B subgenomes differ significantly, suggesting that both the dynamics of the dominant long terminal repeat retrotransposons and DNA methylation have played critical roles in subgenome diversification. Investigation of the genetic basis of biosynthesis of glucosinolates (GSLs) and horseradish peroxidases reveals both the important role of polyploidization and subgenome differentiation in shaping the key traits. Continuous duplication and divergence of essential genes of GSL biosynthesis (e.g., FMOGS-OX, IGMT, and GH1 gene family) contribute to the broad GSL profile in horseradish. Overall, the T2T assembly of the allotetraploid horseradish genome expands our understanding of polyploid genome evolution and provides a fundamental genetic resource for breeding and genetic improvement of horseradish.
BACKGROUND AND AIMS: Sexual reproduction is known to drive plant diversification and adaptation. Here we investigate the evolutionary history and spatiotemporal origin of a dodecaploid (2n = 12x = 96) Eurasian deciduous woodland species, Cardamine bulbifera, which reproduces and spreads via vegetative bulb-like structures only. The species has been among the most successful range-expanding understorey woodland plants in Europe, which raises the question of the genetic architecture of its gene pool, since its hexaploid (2n = 6x = 48) but putatively outcrossing closest relative, C. quinquefolia, displays a smaller distribution range in Eastern Europe towards the Caucasus region. Cardamine bulbifera belongs to a small monophyletic clade of four species comprising also C. abchasica (2n = 2x = 16) and C. bipinnata (unknown ploidy) from the Caucasus region. METHODS: We sequenced the genomes of the two polyploids and their two putative ancestors using Illumina short-read sequencing technology (×7-8 coverage). Covering the entire distribution range, genomic data were generated for 67 samples of the two polyploids (51 samples of C. bulbifera, 16 samples of C. quinquefolia) and 6 samples of the putative diploid taxa (4 samples of C. abchasica, 2 samples of C. bipinnata) to unravel the evolutionary origin of the polyploid taxa using phylogenetic reconstructions of biparentally and maternally inherited genetic sequence data. Ploidy levels of C. bulbifera and C. quinquefolia were analysed by comparative chromosome painting. We used genetic assignment analysis (STRUCTURE) and approximate Bayesian computation (ABC) modelling to test whether C. bulbifera represents genetically differentiated lineages and addressed the hypothesis of its hybrid origin. Comparative ecological modelling was applied to unravel possible niche differentiation among the two polyploid species. KEY RESULTS: Cardamine bulbifera was shown to be a non-hybridogenous, auto-dodecaploid taxon of early Pleistocene origin, but with a history of past gene flow with its hexaploid sister species C. quinquefolia, likely during the last glacial maximum in shared refuge areas in Eastern Europe towards Western Turkey and the Crimean Peninsula region. The diploid Caucasian endemic C. abchasica is considered an ancestral species, which also provides evidence for the origin of the species complex in the Caucasus region. Cardamine bulbifera successfully expanded its distribution range postglacially towards Central and Western Europe accompanied by a transition to exclusively vegetative propagation. CONCLUSIONS: A transition to vegetative propagation in C. bulbifera is hypothesized as the major innovation to rapidly expand its distribution range following postglacially progressing woodland vegetation throughout Europe. Preceding and introgressive gene flow from its sister species C. quinquefolia in the joint refuge area is documented. This transition and ecological differentiation may have been triggered by preceding introgressive gene flow from its sister species in the joint East European refuge areas.
- Keywords
- Cardamine bulbifera, chromosome painting, clonal reproduction, demographic history, ecological modelling, evolutionary history, genomics, polyploidy, postglacial expansion, reproductive shift,
- MeSH
- Bayes Theorem MeSH
- Cardamine * genetics MeSH
- Phylogeny MeSH
- Polyploidy MeSH
- Reproduction MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Despite the essential requirement of telomeric DNA for genome stability, the length of telomere tracts between species substantially differs, raising the question of the minimal length of telomeric DNA necessary for proper function. Here, we address this question using a hypomorphic allele of the telomerase catalytic subunit, TERT. We show that although this construct partially restored telomerase activity to a tert mutant, telomeres continued to shorten over several generations, ultimately stabilizing at a bimodal size distribution. Telomeres on two chromosome arms were maintained at a length of 1 kb, while the remaining telomeres were maintained at 400 bp. The longest telomeres identified in this background were also significantly longer in wild-type populations, suggesting cis-acting elements on these arms either promote telomerase processivity or recruitment. Genetically disrupting telomerase processivity in this background resulted in immediate lethality. Thus, telomeres of 400 bp are both necessary and sufficient for Arabidopsis viability. As this length is the estimated minimal length for t-loop formation, our data suggest that telomeres long enough to form a t-loop constitute the minimal functional length.
- Keywords
- genome stability, subtelomere, t-loop, telomerase, telomeres,
- MeSH
- Arabidopsis MeSH
- Telomere Homeostasis * MeSH
- Mutation MeSH
- Arabidopsis Proteins genetics metabolism MeSH
- Telomerase genetics metabolism MeSH
- Telomere genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, N.I.H., Extramural MeSH
- Names of Substances
- Arabidopsis Proteins MeSH
- Telomerase MeSH
- TERT protein, Arabidopsis MeSH Browser
Whole genome duplication (WGD) can promote adaptation but is disruptive to conserved processes, especially meiosis. Studies in Arabidopsis arenosa revealed a coordinated evolutionary response to WGD involving interacting proteins controlling meiotic crossovers, which are minimized in an autotetraploid (within-species polyploid) to avoid missegregation. Here, we test whether this surprising flexibility of a conserved essential process, meiosis, is recapitulated in an independent WGD system, Cardamine amara, 17 My diverged from A. arenosa. We assess meiotic stability and perform population-based scans for positive selection, contrasting the genomic response to WGD in C. amara with that of A. arenosa. We found in C. amara the strongest selection signals at genes with predicted functions thought important to adaptation to WGD: meiosis, chromosome remodeling, cell cycle, and ion transport. However, genomic responses to WGD in the two species differ: minimal ortholog-level convergence emerged, with none of the meiosis genes found in A. arenosa exhibiting strong signal in C. amara. This is consistent with our observations of lower meiotic stability and occasional clonal spreading in diploid C. amara, suggesting that nascent C. amara autotetraploid lineages were preadapted by their diploid lifestyle to survive while enduring reduced meiotic fidelity. However, in contrast to a lack of ortholog convergence, we see process-level and network convergence in DNA management, chromosome organization, stress signaling, and ion homeostasis processes. This gives the first insight into the salient adaptations required to meet the challenges of a WGD state and shows that autopolyploids can utilize multiple evolutionary trajectories to adapt to WGD.
Mountains of the Balkan Peninsula are significant biodiversity hotspots with great species richness and a large proportion of narrow endemics. Processes that have driven the evolution of the rich Balkan mountain flora, however, are still insufficiently explored and understood. Here we focus on a group of Cardamine (Brassicaceae) perennials growing in wet, mainly mountainous habitats. It comprises several Mediterranean endemics, including those restricted to the Balkan Peninsula. We used target enrichment with genome skimming (Hyb-Seq) to infer their phylogenetic relationships, and, along with genomic in situ hybridization (GISH), to resolve the origin of tetraploid Cardamine barbaraeoides endemic to the Southern Pindos Mts. (Greece). We also explored the challenges of phylogenomic analyses of polyploid species and developed a new approach of allele sorting into homeologs that allows identifying subgenomes inherited from different progenitors. We obtained a robust phylogenetic reconstruction for diploids based on 1,168 low-copy nuclear genes, which suggested both allopatric and ecological speciation events. In addition, cases of plastid-nuclear discordance, in agreement with divergent nuclear ribosomal DNA (nrDNA) copy variants in some species, indicated traces of interspecific gene flow. Our results also support biogeographic links between the Balkan and Anatolian-Caucasus regions and illustrate the contribution of the latter region to high Balkan biodiversity. An allopolyploid origin was inferred for C. barbaraeoides, which highlights the role of mountains in the Balkan Peninsula both as refugia and melting pots favoring species contacts and polyploid evolution in response to Pleistocene climate-induced range dynamics. Overall, our study demonstrates the importance of a thorough phylogenomic approach when studying the evolution of recently diverged species complexes affected by reticulation events at both diploid and polyploid levels. We emphasize the significance of retrieving allelic and homeologous variation from nuclear genes, as well as multiple nrDNA copy variants from genome skim data.
- Keywords
- Balkan endemism, Hyb-Seq, Pindhos Mts., allopolyploidy, genomic in situ hybridization, nrDNA, read-backed phasing, target enrichment,
- Publication type
- Journal Article MeSH
INTRODUCTION: Ribosomal DNA (rDNA) loci have been widely used for identification of allopolyploids and hybrids, although few of these studies employed high-throughput sequencing data. Here we use graph clustering implemented in the RepeatExplorer (RE) pipeline to analyze homoeologous 5S rDNA arrays at the genomic level searching for hybridogenic origin of species. Data were obtained from more than 80 plant species, including several well-defined allopolyploids and homoploid hybrids of different evolutionary ages and from widely dispersed taxonomic groups. RESULTS: (i) Diploids show simple circular-shaped graphs of their 5S rDNA clusters. In contrast, most allopolyploids and other interspecific hybrids exhibit more complex graphs composed of two or more interconnected loops representing intergenic spacers (IGS). (ii) There was a relationship between graph complexity and locus numbers. (iii) The sequences and lengths of the 5S rDNA units reconstituted in silico from k-mers were congruent with those experimentally determined. (iv) Three-genomic comparative cluster analysis of reads from allopolyploids and progenitor diploids allowed identification of homoeologous 5S rRNA gene families even in relatively ancient (c. 1 Myr) Gossypium and Brachypodium allopolyploids which already exhibit uniparental partial loss of rDNA repeats. (v) Finally, species harboring introgressed genomes exhibit exceptionally complex graph structures. CONCLUSION: We found that the cluster graph shapes and graph parameters (k-mer coverage scores and connected component index) well-reflect the organization and intragenomic homogeneity of 5S rDNA repeats. We propose that the analysis of 5S rDNA cluster graphs computed by the RE pipeline together with the cytogenetic analysis might be a reliable approach for the determination of the hybrid or allopolyploid plant species parentage and may also be useful for detecting historical introgression events.
- Keywords
- 5S rRNA genes, allopolyploidy, evolution, graph structure clustering, high-throughput sequencing, hybridization, repeatome,
- Publication type
- Journal Article MeSH
Oligo painting FISH was established to identify all chromosomes in banana (Musa spp.) and to anchor pseudomolecules of reference genome sequence of Musa acuminata spp. malaccensis "DH Pahang" to individual chromosomes in situ. A total of 19 chromosome/chromosome-arm specific oligo painting probes were developed and were shown to be suitable for molecular cytogenetic studies in genus Musa. For the first time, molecular karyotypes of diploid M. acuminata spp. malaccensis (A genome), M. balbisiana (B genome), and M. schizocarpa (S genome) from the Eumusa section of Musa, which contributed to the evolution of edible banana cultivars, were established. This was achieved after a combined use of oligo painting probes and a set of previously developed banana cytogenetic markers. The density of oligo painting probes was sufficient to study chromosomal rearrangements on mitotic as well as on meiotic pachytene chromosomes. This advance will enable comparative FISH mapping and identification of chromosomal translocations which accompanied genome evolution and speciation in the family Musaceae.
- Keywords
- Musa, banana, chromosome identification, fluorescence in situ hybridization, molecular karyotype, oligo painting FISH,
- Publication type
- Journal Article MeSH
Complexes of diploid and polyploid species have formed frequently during the evolution of land plants. In false flax (Camelina sativa), an important hexaploid oilseed crop closely related to Arabidopsis (Arabidopsis thaliana), the putative parental species as well as the origin of other Camelina species remained unknown. By using bacterial artificial chromosome-based chromosome painting, genomic in situ hybridization, and multi-gene phylogenetics, we aimed to elucidate the origin and evolution of the polyploid complex. Genomes of diploid camelinas (Camelina hispida, n = 7; Camelina laxa, n = 6; and Camelina neglecta, n = 6) originated from an ancestral n = 7 genome. The allotetraploid genome of Camelina rumelica (n = 13, N6H) arose from hybridization between diploids related to C. neglecta (n = 6, N6) and C. hispida (n = 7, H), and the N subgenome has undergone a substantial post-polyploid fractionation. The allohexaploid genomes of C. sativa and Camelina microcarpa (n = 20, N6N7H) originated through hybridization between an auto-allotetraploid C. neglecta-like genome (n = 13, N6N7) and C. hispida (n = 7, H), and the three subgenomes have remained stable overall since the genome merger. Remarkably, the ancestral and diploid Camelina genomes were shaped by complex chromosomal rearrangements, resembling those associated with human disorders and resulting in the origin of genome-specific shattered chromosomes.plantcell;31/11/2596/FX1F1fx1.
- MeSH
- Arabidopsis genetics MeSH
- Brassicaceae classification genetics MeSH
- Chromothripsis * MeSH
- Chromosomes, Plant MeSH
- Diploidy * MeSH
- Phylogeny MeSH
- Genome, Plant * MeSH
- Hybridization, Genetic MeSH
- Evolution, Molecular * MeSH
- Polyploidy MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
BACKGROUND AND AIMS: Cardamine occulta (Brassicaceae) is an octoploid weedy species (2n = 8x = 64) originated in Eastern Asia. It has been introduced to other continents including Europe and considered to be an invasive species. Despite its wide distribution, the polyploid origin of C. occulta remained unexplored. The feasibility of comparative chromosome painting (CCP) in crucifers allowed us to elucidate the origin and genome evolution in Cardamine species. We aimed to investigate the genome structure of C. occulta in comparison with its tetraploid (2n = 4x = 32, C. kokaiensis and C. scutata) and octoploid (2n = 8x = 64, C. dentipetala) relatives. METHODS: Genomic in situ hybridization (GISH) and large-scale CCP were applied to uncover the parental genomes and chromosome composition of the investigated Cardamine species. KEY RESULTS: All investigated species descended from a common ancestral Cardamine genome (n = 8), structurally resembling the Ancestral Crucifer Karyotype (n = 8), but differentiated by a translocation between chromosomes AK6 and AK8. Allotetraploid C. scutata originated by hybridization between two diploid species, C. parviflora and C. amara (2n = 2x = 16). By contrast, C. kokaiensis has an autotetraploid origin from a parental genome related to C. parviflora. Interestingly, octoploid C. occulta probably originated through hybridization between the tetraploids C. scutata and C. kokaiensis. The octoploid genome of C. dentipetala probably originated from C. scutata via autopolyploidization. Except for five species-specific centromere repositionings and one pericentric inversion post-dating the polyploidization events, the parental subgenomes remained stable in the tetra- and octoploids. CONCLUSIONS: Comparative genome structure, origin and evolutionary history was reconstructed in C. occulta and related species. For the first time, whole-genome cytogenomic maps were established for octoploid plants. Post-polyploid evolution in Asian Cardamine polyploids has not been associated with descending dysploidy and intergenomic rearrangements. The combination of different parental (sub)genomes adapted to distinct habitats provides an evolutionary advantage to newly formed polyploids by occupying new ecological niches.
- Keywords
- Allopolyploidy, Asian Cardamine, Brassicaceae, GISH (genomic in situ hybridization), autopolyploidy, centromere repositioning, chromosome rearrangements, comparative chromosome painting, diploidization, genome collinearity, hybridization, invasive species,
- MeSH
- Brassicaceae * MeSH
- Cardamine * MeSH
- Genome, Plant MeSH
- Humans MeSH
- Polyploidy MeSH
- Introduced Species MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Asia, Eastern MeSH
- Europe MeSH
