Most cited article - PubMed ID 32732942
Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae
Matthiola incana, commonly known as stock and gillyflower, is a widely grown ornamental plant whose genome is significantly larger than that of other species in the mustard family. However, the evolutionary history behind such a large genome (~2 Gb) is still unknown. Here, we have succeeded in obtaining a high-quality chromosome-scale genome assembly of M. incana by integrating PacBio HiFi reads, Illumina short reads and Hi-C data. The resulting genome consists of seven pseudochromosomes with a length of 1965 Mb and 38 245 gene models. Phylogenetic analysis indicates that M. incana and other taxa of the supertribe Hesperodae represent an early-diverging lineage in the evolutionary history of the Brassicaceae. Through a comparative analysis, we revisited the ancestral Hesperodae karyotype (AHK, n = 7) and found several differences from the well-established ancestral crucifer karyotype (ACK, n = 8) model, including extensive inter- and intra-chromosomal rearrangements. Our results suggest that the primary reason for genome obesity in M. incana is the massive expansion of long terminal repeat retrotransposons (LTR-RTs), particularly from the Angela, Athila and Retand families. CHG methylation modification is obviously reduced in the regions where the highest density of Copia-type LTR-RTs and the lowest density of Gypsy-type LTR-RTs overlap, corresponding to the putative centromeres. Based on insertion times and methylation profiling, recently inserted LTR-RTs were found to have a significantly different methylation pattern compared to older ones.
- Keywords
- Cruciferae, Hesperodae, Lineage III, genome assembly, genome obesity, retrotransposons,
- MeSH
- Brassicaceae * genetics MeSH
- Chromosomes, Plant genetics MeSH
- Phylogeny MeSH
- Genome, Plant * genetics MeSH
- Karyotype MeSH
- Evolution, Molecular * MeSH
- Retroelements * genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Retroelements * MeSH
Model species continue to underpin groundbreaking plant science research. At the same time, the phylogenetic resolution of the land plant tree of life continues to improve. The intersection of these 2 research paths creates a unique opportunity to further extend the usefulness of model species across larger taxonomic groups. Here we promote the utility of the Arabidopsis thaliana model species, especially the ability to connect its genetic and functional resources, to species across the entire Brassicales order. We focus on the utility of using genomics and phylogenomics to bridge the evolution and diversification of several traits across the Brassicales to the resources in Arabidopsis, thereby extending scope from a model species by establishing a "model clade." These Brassicales-wide traits are discussed in the context of both the model species Arabidopsis and the family Brassicaceae. We promote the utility of such a "model clade" and make suggestions for building global networks to support future studies in the model order Brassicales.
Telomere repeat binding proteins (TRBs) belong to a family of proteins possessing a Myb-like domain which binds to telomeric repeats. Three members of this family (TRB1, TRB2, TRB3) from Arabidopsis thaliana have already been described as associated with terminal telomeric repeats (telomeres) or short interstitial telomeric repeats in gene promoters (telo-boxes). They are also known to interact with several protein complexes: telomerase, Polycomb repressive complex 2 (PRC2) E(z) subunits and the PEAT complex (PWOs-EPCRs-ARIDs-TRBs). Here we characterize two novel members of the TRB family (TRB4 and TRB5). Our wide phylogenetic analyses have shown that TRB proteins evolved in the plant kingdom after the transition to a terrestrial habitat in Streptophyta, and consequently TRBs diversified in seed plants. TRB4-5 share common TRB motifs while differing in several others and seem to have an earlier phylogenetic origin than TRB1-3. Their common Myb-like domains bind long arrays of telomeric repeats in vitro, and we have determined the minimal recognition motif of all TRBs as one telo-box. Our data indicate that despite the distinct localization patterns of TRB1-3 and TRB4-5 in situ, all members of TRB family mutually interact and also bind to telomerase/PRC2/PEAT complexes. Additionally, we have detected novel interactions between TRB4-5 and EMF2 and VRN2, which are Su(z)12 subunits of PRC2.
- Keywords
- PEAT, PRC2, TERT, TRB, Telomere repeat binding, Telomeric,
- MeSH
- Arabidopsis * genetics metabolism MeSH
- Phylogeny MeSH
- Arabidopsis Proteins * genetics metabolism MeSH
- Telomere-Binding Proteins genetics metabolism MeSH
- Soil MeSH
- Telomerase * genetics metabolism MeSH
- Telomere genetics metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Arabidopsis Proteins * MeSH
- Telomere-Binding Proteins MeSH
- Soil MeSH
- Telomerase * MeSH
Based on recent achievements in phylogenetic studies of the Brassicaceae, a novel infrafamilial classification is proposed that includes major improvements at the subfamilial and supertribal levels. Herein, the family is subdivided into two subfamilies, Aethionemoideae (subfam. nov.) and Brassicoideae. The Brassicoideae, with 57 of the 58 tribes of Brassicaceae, are further partitioned into five supertribes, including the previously recognized Brassicodae and the newly established Arabodae, Camelinodae, Heliophilodae, and Hesperodae. Additional tribus-level contributions include descriptions of the newly recognized Arabidopsideae, Asperuginoideae, Hemilophieae, Schrenkielleae, and resurrection of the Chamireae and Subularieae. Further detailed comments on 17 tribes in need of clarifications are provided.
- Keywords
- classification, subfamily, supertribe, taxonomy, tribe,
- Publication type
- Journal Article MeSH
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
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.
Molecular responses of plants to natural phytotoxins comprise more general and compound-specific mechanisms. How phytotoxic chalcones and other flavonoids inhibit seedling growth was widely studied, but how they interfere with seed germination is largely unknown. The dihydrochalcone and putative allelochemical myrigalone A (MyA) inhibits seed germination and seedling growth. Transcriptome (RNAseq) and hormone analyses of Lepidium sativum seed responses to MyA were compared to other bioactive and inactive compounds. MyA treatment of imbibed seeds triggered the phased induction of a detoxification programme, altered gibberellin, cis-(+)-12-oxophytodienoic acid and jasmonate metabolism, and affected the expression of hormone transporter genes. The MyA-mediated inhibition involved interference with the antioxidant system, oxidative signalling, aquaporins and water uptake, but not uncoupling of oxidative phosphorylation or p-hydroxyphenylpyruvate dioxygenase expression/activity. MyA specifically affected the expression of auxin-related signalling genes, and various transporter genes, including for auxin transport (PIN7, ABCG37, ABCG4, WAT1). Responses to auxin-specific inhibitors further supported the conclusion that MyA interferes with auxin homeostasis during seed germination. Comparative analysis of MyA and other phytotoxins revealed differences in the specific regulatory mechanisms and auxin transporter genes targeted to interfere with auxin homestasis. We conclude that MyA exerts its phytotoxic activity by multiple auxin-dependent and independent molecular mechanisms.
- Keywords
- ATP-binding cassette (ABC) transporter, PIN auxin efflux carrier, WRKY transcription factors, allelochemical and allelopathy, aquaporin-mediated water transport, auxin transport and homeostasis, cis-(+)-12-oxophytodienoic acid (OPDA) reductase, gibberellin metabolism, phytotoxin detoxification programme, seed germination,
- MeSH
- Chalcones MeSH
- Homeostasis MeSH
- Hormones metabolism MeSH
- Germination * genetics MeSH
- Indoleacetic Acids metabolism MeSH
- Lepidium sativum * metabolism MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Growth Regulators metabolism pharmacology MeSH
- Seeds genetics MeSH
- Seedlings metabolism MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chalcones MeSH
- Hormones MeSH
- Indoleacetic Acids MeSH
- myrigalone A MeSH Browser
- Plant Growth Regulators MeSH
The Balkan Peninsula played an important role in the evolution of many Mediterranean plants and served as a major source for post-Pleistocene colonisation of central and northern Europe. Its complex geo-climatic history and environmental heterogeneity significantly influenced spatiotemporal diversification and resulted in intricate phylogeographic patterns. To explore the evolutionary dynamics and phylogeographic patterns within the widespread eastern Mediterranean and central European species Aurinia saxatilis, we used a combination of phylogenomic (restriction-site associated DNA sequencing, RADseq) and phylogenetic (sequences of the plastid marker ndhF) data as well as species distribution models generated for the present and the Last Glacial Maximum (LGM). The inferred phylogenies retrieved three main geographically distinct lineages. The southern lineage is restricted to the eastern Mediterranean, where it is distributed throughout the Aegean area, the southern Balkan Peninsula, and the southern Apennine Peninsula, and corresponds to the species main distribution area during the LGM. The eastern lineage extends from the eastern Balkan Peninsula over the Carpathians to central Europe, while the central lineage occupies the central Balkan Peninsula. Molecular dating places the divergence among all the three lineages to the early to middle Pleistocene, indicating their long-term independent evolutionary trajectories. Our data revealed an early divergence and stable in situ persistence of the southernmost, eastern Mediterranean lineage, whereas the mainland, south-east European lineages experienced more complex and turbulent evolutionary dynamics triggered by Pleistocene climatic oscillations. Our data also support the existence of multiple glacial refugia in southeast Europe and highlight the central Balkan Peninsula not only as a cradle of lineage diversifications but also as a source of lineage dispersal. Finally, the extant genetic variation within A. saxatilis is congruent with the taxonomic separation of peripatric A. saxatilis subsp. saxatilis and A. saxatilis subsp. orientalis, whereas the taxonomic status of A. saxatilis subsp. megalocarpa remains doubtful.
- Keywords
- Aurinia saxatilis, RAD sequencing, demographic modelling, glacial refugia, ndhF, species distribution modelling,
- Publication type
- Journal Article MeSH
Deserts exert strong selection pressures on plants, but the underlying genomic drivers of ecological adaptation and subsequent speciation remain largely unknown. Here, we generated de novo genome assemblies and conducted population genomic analyses of the psammophytic genus Pugionium (Brassicaceae). Our results indicated that this bispecific genus had undergone an allopolyploid event, and the two parental genomes were derived from two ancestral lineages with different chromosome numbers and structures. The postpolyploid expansion of gene families related to abiotic stress responses and lignin biosynthesis facilitated environmental adaptations of the genus to desert habitats. Population genomic analyses of both species further revealed their recent divergence with continuous gene flow, and the most divergent regions were found to be centered on three highly structurally reshuffled chromosomes. Genes under selection in these regions, which were mainly located in one of the two subgenomes, contributed greatly to the interspecific divergence in microhabitat adaptation.
- Keywords
- chromosomal structural variation, desert plants, microhabitat divergence, polyploidization,
- MeSH
- Brassicaceae classification genetics physiology MeSH
- Ecosystem * MeSH
- Phylogeny MeSH
- Adaptation, Physiological genetics MeSH
- Genome, Plant * MeSH
- Polyploidy MeSH
- Genetic Speciation * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't 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
