Nejvíce citovaný článek - PubMed ID 29024107
Multispeed genome diploidization and diversification after an ancient allopolyploidization
The majority of cultivated bananas originated from inter- and intra(sub)specific crosses between two wild diploid species, Musa acuminata and Musa balbisiana. Hybridization and polyploidization events during the evolution of bananas led to the formation of clonally propagated cultivars characterized by a high level of genome heterozygosity and reduced fertility. The combination of low fertility in edible clones and differences in the chromosome structure among M. acuminata subspecies greatly hampers the breeding of improved banana cultivars. Using comparative oligo-painting, we investigated large chromosomal rearrangements in a set of wild M. acuminata subspecies and cultivars that originated from natural and human-made crosses. Additionally, we analyzed the chromosome structure of F1 progeny that resulted from crosses between Mchare bananas and the wild M. acuminata 'Calcutta 4' genotype. Analysis of chromosome structure within M. acuminata revealed the presence of a large number of chromosomal rearrangements showing a correlation with banana speciation. Chromosome painting of F1 hybrids was complemented by Illumina resequencing to identify the contribution of parental subgenomes to the diploid hybrid clones. The balanced presence of both parental genomes was revealed in all F1 hybrids, with the exception of one clone, which contained only Mchare-specific SNPs and thus most probably originated from an unreduced diploid gamete of Mchare.
- Klíčová slova
- F1 hybrids, Musa acuminata, chromosome translocation, comparative cytogenetics, oligo painting FISH,
- Publikační typ
- časopisecké články 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.
- Klíčová slova
- Arabidopsis-related model systems, Brassicaceae, Cruciferae, Hyb-Seq, chromosome painting, diploidization, polyploidy, whole-genome duplication (WGD),
- Publikační typ
- časopisecké články MeSH
BACKGROUND AND AIMS: Reproductive isolation and local establishment are necessary for plant speciation. Polyploidy, the possession of more than two complete chromosome sets, creates a strong postzygotic reproductive barrier between diploid and tetraploid cytotypes. However, this barrier weakens between polyploids (e.g. tetraploids and hexaploids). Reproductive isolation may be enhanced by cytotype morphological and environmental differentiation. Moreover, morphological adaptations to local conditions contribute to plant establishment. However, the relative contributions of ploidy level and the environment to morphology have generally been neglected. Thus, the extent of morphological variation driven by ploidy level and the environment was modelled for diploid, tetraploid and hexaploid cytotypes of Campanula rotundifolia agg. Cytotype distribution was updated, and morphological and environmental differentiation was tested in the presence and absence of natural contact zones. METHODS: Cytotype distribution was assessed from 231 localities in Central Europe, including 48 localities with known chromosome counts, using flow cytometry. Differentiation in environmental niche and morphology was tested for cytotype pairs using discriminant analyses. A structural equation model was used to explore the synergies between cytotype, environment and morphology. KEY RESULTS: Tremendous discrepancies were revealed between the reported and detected cytotype distribution. Neither mixed-ploidy populations nor interploidy hybrids were detected in the contact zones. Diploids had the broadest environmental niche, while hexaploids had the smallest and specialized niche. Hexaploids and spatially isolated cytotype pairs differed morphologically, including allopatric tetraploids. While leaf and shoot morphology were influenced by environmental conditions and polyploidy, flower morphology depended exclusively on the cytotype. CONCLUSIONS: Reproductive isolation mechanisms vary between cytotypes. While diploids and polyploids are isolated postzygotically, the environmental niche shift is essential between higher polyploids. The impact of polyploidy and the environment on plant morphology implies the adaptive potential of polyploids, while the exclusive relationship between flower morphology and cytotype highlights the role of polyploidy in reproductive isolation.
- Klíčová slova
- Campanula rotundifolia agg, allopatry, contact zone, cytotype distribution, diploid, environmental niche shift, hexaploid, morphological differentiation, parapatry, polyploidy, reproductive isolation, tetraploid,
- MeSH
- Campanulaceae * MeSH
- diploidie MeSH
- ploidie MeSH
- polyploidie MeSH
- tetraploidie * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Angiosperm genome evolution was marked by many clade-specific whole-genome duplication events. The Microlepidieae is one of the monophyletic clades in the mustard family (Brassicaceae) formed after an ancient allotetraploidization. Postpolyploid cladogenesis has resulted in the extant c. 17 genera and 60 species endemic to Australia and New Zealand (10 species). As postpolyploid genome diploidization is a trial-and-error process under natural selection, it may proceed with different intensity and be associated with speciation events. In Microlepidieae, different extents of homoeologous recombination between the two parental subgenomes generated clades marked by slow ("cold") versus fast ("hot") genome diploidization. To gain a deeper understanding of postpolyploid genome evolution in Microlepidieae, we analyzed phylogenetic relationships in this tribe using complete chloroplast sequences, entire 35S rDNA units, and abundant repetitive sequences. The four recovered intra-tribal clades mirror the varied diploidization of Microlepidieae genomes, suggesting that the intrinsic genomic features underlying the extent of diploidization are shared among genera and species within one clade. Nevertheless, even congeneric species may exert considerable morphological disparity (e.g. in fruit shape), whereas some species within different clades experience extensive morphological convergence despite the different pace of their genome diploidization. We showed that faster genome diploidization is positively associated with mean morphological disparity and evolution of chloroplast genes (plastid-nuclear genome coevolution). Higher speciation rates in perennials than in annual species were observed. Altogether, our results confirm the potential of Microlepidieae as a promising subject for the analysis of postpolyploid genome diploidization in Brassicaceae.
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
- genomika MeSH
- karyotyp MeSH
- meióza MeSH
- molekulární evoluce * MeSH
- polyploidie * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy 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.
- Klíčová slova
- chromosome rearrangements, diploidization, dysploidy, hybridization, phylogenetics, polyploidy, reticulate evolution, whole-genome duplication,
- MeSH
- biologická evoluce * MeSH
- Brassicaceae genetika MeSH
- chromozomy rostlin * MeSH
- duplikace genu MeSH
- genom rostlinný * MeSH
- hybridizace genetická MeSH
- polyploidie * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem 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.
- Klíčová slova
- chromosome numbers, cytogenomics, dysploidy, genome evolution, phylogenetic models, polyploidy,
- MeSH
- chromozomy rostlin * MeSH
- genom rostlinný MeSH
- genomika MeSH
- malování chromozomů MeSH
- modely genetické * MeSH
- molekulární evoluce * MeSH
- polyploidie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Angiosperms have become the dominant terrestrial plant group by diversifying for ~145 million years into a broad range of environments. During the course of evolution, numerous morphological innovations arose, often preceded by whole genome duplications (WGD). The mustard family (Brassicaceae), a successful angiosperm clade with ~4000 species, has been diversifying into many evolutionary lineages for more than 30 million years. Here we develop a species inventory, analyze morphological variation, and present a maternal, plastome-based genus-level phylogeny. We show that increased morphological disparity, despite an apparent absence of clade-specific morphological innovations, is found in tribes with WGDs or diversification rate shifts. Both are important processes in Brassicaceae, resulting in an overall high net diversification rate. Character states show frequent and independent gain and loss, and form varying combinations. Therefore, Brassicaceae pave the way to concepts of phylogenetic genome-wide association studies to analyze the evolution of morphological form and function.
The mustard family (Brassicaceae) comprises several dozen monophyletic clades usually ranked as tribes. The tribe Boechereae plays a prominent role in plant research due to the incidence of apomixis and its close relationship to Arabidopsis. This tribe, largely confined to western North America, harbors nine genera and c. 130 species, with >90% of species belonging to the genus Boechera. Hundreds of apomictic diploid and triploid Boechera hybrids have spurred interest in this genus, but the remaining Boechereae genomes remain virtually unstudied. Here we report on comparative genome structure of six genera (Borodinia, Cusickiella, Phoenicaulis, Polyctenium, Nevada, and Sandbergia) and three Boechera species as revealed by comparative chromosome painting (CCP). All analyzed taxa shared the same seven-chromosome genome structure. Comparisons with the sister Halimolobeae tribe (n = 8) showed that the ancestral Boechereae genome (n = 7) was derived from an older n = 8 genome by descending dysploidy followed by the divergence of extant Boechereae taxa. As tribal divergence post-dated the origin of four tribe-specific chromosomes, it is proposed that these chromosomal rearrangements were a key evolutionary innovation underlaying the origin and diversification of the Boechereae in North America. Although most Boechereae genera exhibit genomic conservatism, intra-tribal cladogenesis has occasionally been accompanied by chromosomal rearrangements (particularly inversions). Recently, apomixis was reported in the Boechereae genera Borodinia and Phoenicaulis. Here, we report sexual reproduction in diploid Nevada, diploid Sandbergia, and tetraploid Cusickiella and aposporous apomixis in tetraploids of Polyctenium and Sandbergia. In sum, apomixis is now known to occur in five of the nine Boechereae genera.
- Klíčová slova
- Cruciferae, North America, apomixis, apospory, autopolyploidy, descending dysploidy, karyotype evolution, speciation,
- Publikační typ
- časopisecké články 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 genetika MeSH
- Brassicaceae klasifikace genetika MeSH
- chromothripsis * MeSH
- chromozomy rostlin MeSH
- diploidie * MeSH
- fylogeneze MeSH
- genom rostlinný * MeSH
- hybridizace genetická MeSH
- molekulární evoluce * MeSH
- polyploidie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
