Most cited article - PubMed ID 31451448
Origin and Evolution of Diploid and Allopolyploid Camelina Genomes Were Accompanied by Chromosome Shattering
Boechera falcata (Turcz.) Al-Shehbaz, previously known as Arabis turczaninowii Ledeb., is a herbaceous perennial of the East Siberian, boreal-steppe ecotype. It is the sole species of the diverse genus Boechera found on the Eurasian continent, with all other species endemic to North America and Greenland. Likely migrating from North America to Eastern Siberia via the Bering Land Bridge during the Pleistocene glaciation, B. falcata presents a unique case for genomic study. The genus Boechera is notable for its many allodiploid and triploid apomicts, which have arisen through complex hybridization of sexual species and ecotypes. To date, only the genomes of 2 American Boechera species, B. stricta and B. retrofracta, have been sequenced and analyzed. In this study, we sequenced, assembled to the chromosome level, and analyzed the highly homozygous 189.36 Mb genome of B. falcata (2n = 14). Molecular phylogenetic analysis of nuclear and organelle genomes revealed a high degree of relatedness to North American relatives. Cytogenetic analysis identified all 22 genomic blocks of crucifers, showing that 5 of the 7 B. falcata chromosomes are collinear with their ancestral counterparts, while 2 have undergone inversions. Allelic analysis of the apomixis marker APOLLO gene revealed that B. falcata contains only sex alleles. The availability of the B. falcata genome will advance studies of the evolution and phylogeny of Brassicaceae species and the mechanisms of apomixis, providing a crucial resource for future research in plant genetics and breeding.
- Keywords
- Boechera falcata, Brassicaceae, chloroplast genome, chromosome rearrangements, chromosome-level genome assembly and annotation, comparative chromosome painting, genome structure, molecular phylogeny,
- MeSH
- Brassicaceae * genetics classification MeSH
- Chromosomes, Plant genetics MeSH
- Phylogeny * MeSH
- Genome, Plant * MeSH
- Genomics * methods MeSH
- Publication type
- Journal Article MeSH
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.
Y chromosomes are thought to undergo progressive degeneration due to stepwise loss of recombination and subsequent reduction in selection efficiency. However, the timescales and evolutionary forces driving degeneration remain unclear. To investigate the evolution of sex chromosomes on multiple timescales, we generated a high-quality phased genome assembly of the massive older (<10 MYA) and neo (<200,000 yr) sex chromosomes in the XYY cytotype of the dioecious plant Rumex hastatulus and a hermaphroditic outgroup Rumex salicifolius. Our assemblies, supported by fluorescence in situ hybridization, confirmed that the neo-sex chromosomes were formed by two key events: an X-autosome fusion and a reciprocal translocation between the homologous autosome and the Y chromosome. The enormous sex-linked regions of the X (296 Mb) and two Y chromosomes (503 Mb) both evolved from large repeat-rich genomic regions with low recombination; however, the complete loss of recombination on the Y still led to over 30% gene loss and major rearrangements. In the older sex-linked region, there has been a significant increase in transposable element abundance, even into and near genes. In the neo-sex-linked regions, we observed evidence of extensive rearrangements without gene degeneration and loss. Overall, we inferred significant degeneration during the first 10 million years of Y chromosome evolution but not on very short timescales. Our results indicate that even when sex chromosomes emerge from repetitive regions of already-low recombination, the complete loss of recombination on the Y chromosome still leads to a substantial increase in repetitive element content and gene degeneration.
- Keywords
- genomics, plants, sex chromosomes, transposable elements,
- MeSH
- Chromosomes, Plant * MeSH
- Genome, Plant * MeSH
- In Situ Hybridization, Fluorescence MeSH
- Evolution, Molecular * MeSH
- Sex Chromosomes genetics MeSH
- Recombination, Genetic MeSH
- Rumex * genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The establishment of Arabidopsis as the most important plant model has also brought other crucifer species into the spotlight of comparative research. While the genus Capsella has become a prominent crucifer model system, its closest relative has been overlooked. The unispecific genus Catolobus is native to temperate Eurasian woodlands, from eastern Europe to the Russian Far East. Here, we analyzed chromosome number, genome structure, intraspecific genetic variation, and habitat suitability of Catolobus pendulus throughout its range. Unexpectedly, all analyzed populations were hypotetraploid (2n = 30, ~330 Mb). Comparative cytogenomic analysis revealed that the Catolobus genome arose by a whole-genome duplication in a diploid genome resembling Ancestral Crucifer Karyotype (ACK, n = 8). In contrast to the much younger Capsella allotetraploid genomes, the presumably autotetraploid Catolobus genome (2n = 32) arose early after the Catolobus/Capsella divergence. Since its origin, the tetraploid Catolobus genome has undergone chromosomal rediploidization, including a reduction in chromosome number from 2n = 32 to 2n = 30. Diploidization occurred through end-to-end chromosome fusion and other chromosomal rearrangements affecting a total of six of 16 ancestral chromosomes. The hypotetraploid Catolobus cytotype expanded toward its present range, accompanied by some longitudinal genetic differentiation. The sister relationship between Catolobus and Capsella allows comparative studies of tetraploid genomes of contrasting ages and different degrees of genome diploidization.
- Keywords
- Arabidopsis-related model systems, Brassicaceae, Cruciferae, Hyb-Seq, chromosome painting, diploidization, polyploidy, whole-genome duplication (WGD),
- Publication type
- Journal Article MeSH
The evolution of eukaryotic genomes is accompanied by fluctuations in chromosome number, reflecting cycles of chromosome number increase (polyploidy and centric fissions) and decrease (chromosome fusions). Although all chromosome fusions result from DNA recombination between two or more nonhomologous chromosomes, several mechanisms of descending dysploidy are exploited by eukaryotes to reduce their chromosome number. Genome sequencing and comparative genomics have accelerated the identification of inter-genome chromosome collinearity and gross chromosomal rearrangements and have shown that end-to-end chromosome fusions (EEFs) and nested chromosome fusions (NCFs) may have played a more important role in the evolution of eukaryotic karyotypes than previously thought. The present review aims to summarize the limited knowledge on the origin, frequency, and evolutionary implications of EEF and NCF events in eukaryotes and especially in land plants. The interactions between nonhomologous chromosomes in interphase nuclei and chromosome (mis)pairing during meiosis are examined for their potential importance in the origin of EEFs and NCFs. The remaining open questions that need to be addressed are discussed.
- MeSH
- Genomics MeSH
- Karyotype MeSH
- Meiosis MeSH
- Evolution, Molecular * MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
The genus Camelina (Brassicaceae) comprises 7-8 diploid, tetraploid, and hexaploid species. Of particular agricultural interest is the biofuel crop, C. sativa (gold-of-pleasure or false flax), an allohexaploid domesticated from the widespread weed, C. microcarpa. Recent cytogenetics and genomics work has uncovered the identity of the parental diploid species involved in ancient polyploidization events in Camelina. However, little is known about the maternal subgenome ancestry of contemporary polyploid species. To determine the diploid maternal contributors of polyploid Camelina lineages, we sequenced and assembled 84 Camelina chloroplast genomes for phylogenetic analysis. Divergence time estimation was used to infer the timing of polyploidization events. Chromosome counts were also determined for 82 individuals to assess ploidy and cytotypic variation. Chloroplast genomes showed minimal divergence across the genus, with no observed gene-loss or structural variation. Phylogenetic analyses revealed C. hispida as a maternal diploid parent to the allotetraploid Camelina rumelica, and C. neglecta as the closest extant diploid contributor to the allohexaploids C. microcarpa and C. sativa. The tetraploid C. rumelica appears to have evolved through multiple independent hybridization events. Divergence times for polyploid lineages closely related to C. sativa were all inferred to be very recent, at only ~65 thousand years ago. Chromosome counts confirm that there are two distinct cytotypes within C. microcarpa (2n = 38 and 2n = 40). Based on these findings and other recent research, we propose a model of Camelina subgenome relationships representing our current understanding of the hybridization and polyploidization history of this recently-diverged genus.
- Publication type
- Journal Article MeSH
Pervasive hybridization and whole-genome duplications (WGDs) influenced genome evolution in several eukaryotic lineages. Although frequent and recurrent hybridizations may result in reticulate phylogenies, the evolutionary events underlying these reticulations, including detailed structure of the ancestral diploid and polyploid genomes, were only rarely reconstructed. Here, we elucidate the complex genomic history of a monophyletic clade from the mustard family (Brassicaceae), showing contentious relationships to the early-diverging clades of this model plant family. Genome evolution in the crucifer tribe Biscutelleae (∼60 species, 5 genera) was dominated by pervasive hybridizations and subsequent genome duplications. Diversification of an ancestral diploid genome into several divergent but crossable genomes was followed by hybridizations between these genomes. Whereas a single genus (Megadenia) remained diploid, the four remaining genera originated by allopolyploidy (Biscutella, Lunaria, Ricotia) or autopolyploidy (Heldreichia). The contentious relationships among the Biscutelleae genera, and between the tribe and other early diverged crucifer lineages, are best explained by close genomic relatedness among the recurrently hybridizing ancestral genomes. By using complementary cytogenomics and phylogenomics approaches, we demonstrate that the origin of a monophyletic plant clade can be more complex than a parsimonious assumption of a single WGD spurring postpolyploid cladogenesis. Instead, recurrent hybridization among the same and/or closely related parental genomes may phylogenetically interlink diploid and polyploid genomes despite the incidence of multiple independent WGDs. Our results provide new insights into evolution of early-diverging Brassicaceae lineages and elucidate challenges in resolving the contentious relationships within and between land plant lineages with pervasive hybridization and WGDs.
- Keywords
- chromosome rearrangements, diploidization, dysploidy, hybridization, phylogenetics, polyploidy, reticulate evolution, whole-genome duplication,
- MeSH
- Biological Evolution * MeSH
- Brassicaceae genetics MeSH
- Chromosomes, Plant * MeSH
- Gene Duplication MeSH
- Genome, Plant * MeSH
- Hybridization, Genetic MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Chromosome numbers have been widely used to describe the most fundamental genomic attribute of an organism or a lineage. Although providing strong phylogenetic signal, chromosome numbers vary remarkably among eukaryotes at all levels of taxonomic resolution. Changes in chromosome numbers regularly serve as indication of major genomic events, most notably polyploidy and dysploidy. Here, we review recent advancements in our ability to make inferences regarding historical events that led to alterations in the number of chromosomes of a lineage. We first describe the mechanistic processes underlying changes in chromosome numbers, focusing on structural chromosomal rearrangements. Then, we focus on experimental procedures, encompassing comparative cytogenomics and genomics approaches, and on computational methodologies that are based on explicit models of chromosome-number evolution. Together, these tools offer valuable predictions regarding historical events that have changed chromosome numbers and genome structures, as well as their phylogenetic and temporal placements.
- Keywords
- chromosome numbers, cytogenomics, dysploidy, genome evolution, phylogenetic models, polyploidy,
- MeSH
- Chromosomes, Plant * MeSH
- Genome, Plant MeSH
- Genomics MeSH
- Chromosome Painting MeSH
- Models, Genetic * MeSH
- Evolution, Molecular * MeSH
- Polyploidy MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The tribe Aethionemeae is sister to all other crucifers, making it a crucial group for unraveling genome evolution and phylogenetic relationships within the crown group Brassicaceae. In this study, we extend the analysis of Brassicaceae genomic blocks (GBs) to Aethionema whereby we identified unique block boundaries shared only with the tribe Arabideae. This was achieved using bioinformatic methods to analyze synteny between the recently updated genome sequence of Aethionema arabicum and other high-quality Brassicaceae genome sequences. We show that compared to the largely conserved genomic structure of most non-polyploid Brassicaceae lineages, GBs are highly rearranged in Aethionema. Furthermore, we detected similarities between the genomes of Aethionema and Arabis alpina, in which also a high number of genomic rearrangements compared to those of other Brassicaceae was found. These similarities suggest that tribe Arabideae, a clade showing conflicting phylogenetic position between studies, may have diverged before diversification of the other major lineages, and highlight the potential of synteny information for phylogenetic inference.
- Keywords
- Aethionema, Arabideae, Brassicaceae, comparative genomics, genomic blocks, synteny,
- Publication type
- Journal Article MeSH
Centromere position may change despite conserved chromosomal collinearity. Centromere repositioning and evolutionary new centromeres (ENCs) were frequently encountered during vertebrate genome evolution but only rarely observed in plants. The largest crucifer tribe, Arabideae (∼550 species; Brassicaceae, the mustard family), diversified into several well-defined subclades in the virtual absence of chromosome number variation. Bacterial artificial chromosome-based comparative chromosome painting uncovered a constancy of genome structures among 10 analyzed genomes representing seven Arabideae subclades classified as four genera: Arabis, Aubrieta, Draba, and Pseudoturritis Interestingly, the intra-tribal diversification was marked by a high frequency of ENCs on five of the eight homoeologous chromosomes in the crown-group genera, but not in the most ancestral Pseudoturritis genome. From the 32 documented ENCs, at least 26 originated independently, including 4 ENCs recurrently formed at the same position in not closely related species. While chromosomal localization of ENCs does not reflect the phylogenetic position of the Arabideae subclades, centromere seeding was usually confined to long chromosome arms, transforming acrocentric chromosomes to (sub)metacentric chromosomes. Centromere repositioning is proposed as the key mechanism differentiating overall conserved homoeologous chromosomes across the crown-group Arabideae subclades. The evolutionary significance of centromere repositioning is discussed in the context of possible adaptive effects on recombination and epigenetic regulation of gene expression.
