Polyploidy and subsequent post-polyploid diploidization (PPD) are key drivers of plant genome evolution, yet their contributions to evolutionary success remain debated. Here, we analyze the Malvaceae family as an exemplary system for elucidating the evolutionary role of polyploidy and PPD in angiosperms, leveraging 11 high-quality chromosome-scale genomes from all nine subfamilies, including newly sequenced, near telomere-to-telomere assemblies from four of these subfamilies. Our findings reveal a complex reticulate paleoallopolyploidy history early in the diversification of the Malvadendrina clade, characterized by multiple rounds of species radiation punctuated by ancient allotetraploidization (Mal-β) and allodecaploidization (Mal-α) events around the Cretaceous-Paleogene (K-Pg) boundary. We further reconstruct the evolutionary dynamics of PPD and find a strong correlation between dysploidy rate and taxonomic richness of the paleopolyploid subfamilies (R2 ≥ 0.90, P < 1e-4), supporting the "polyploidy for survival and PPD for success" hypothesis. Overall, our study provides a comprehensive reconstruction of the evolutionary history of the Malvaceae and underscores the crucial role of polyploidy-dysploidy waves in shaping plant biodiversity.
Sexual reproduction relies on meiotic chromosome pairing to form bivalents, a process that is complicated in polyploids owing to the presence of multiple subgenomes1. Uneven ploidy mostly results in sterility due to unbalanced chromosome pairing and segregation during meiosis. However, pentaploid dogroses (Rosa sect. Caninae; 2n = 5x = 35) achieve stable sexual reproduction through a unique mechanism: 14 chromosomes form bivalents and are transmitted biparentally, while the remaining 21 chromosomes are maternally inherited as univalents2,3. Despite being studied for over a century, the role of centromeres in this process has remained unclear. Here we analyse haplotype-resolved chromosome-level genome assemblies for three pentaploid dogroses. Subgenome phasing revealed a bivalent-forming subgenome with two highly homozygous chromosome sets and three divergent subgenomes lacking homologous partners, therefore explaining their meiotic behaviour. Comparative analyses of chromosome synteny, phylogenetic relationships and centromere composition indicate that the subgenomes originated from two divergent clades of the genus Rosa. Pollen genome analysis shows that subgenomes from different evolutionary origins form bivalents, supporting multiple origins of dogroses and highlighting variation in subgenome contributions. We reveal that bivalent-forming centromeres are enriched with ATHILA retrotransposons, contrasting with larger tandem-repeat-based centromeres mainly found in univalents. This centromere structural bimodality possibly contributes to univalent drive during female meiosis. Our findings provide insights into the unique reproductive strategies of dogroses, advancing our understanding of genome evolution, centromere diversity and meiotic mechanisms in organisms with asymmetrical inheritance systems.
- MeSH
- Centromere * genetics metabolism MeSH
- Chromosomes, Plant genetics MeSH
- Phylogeny MeSH
- Genome, Plant genetics MeSH
- Haplotypes genetics MeSH
- Meiosis * genetics MeSH
- Polyploidy * MeSH
- Pollen genetics cytology MeSH
- Retroelements genetics MeSH
- Synteny genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Retroelements MeSH
Aquatic plants are generally attributed to have larger ranges than their terrestrial counterparts, but this knowledge is often hindered by insufficient exploration of their diversity. To fill this gap, we investigated the taxonomically extremely challenging aquatic plant group Ranunculus sect. Batrachium in south-western Europe, which is an important glacial refugium, using flow cytometry, chromosome counting and DNA sequencing (ITS nuclear region and two non-coding plastid regions). In a dataset comprising 587 individuals from 117 localities, we detected 36 cytotypes across seven ploidy levels, which included a considerable proportion of previously unrecognized diversity consisting of three high ploidies (7x, 10x, 12x), seven cryptic species, two additional unclassifiable biotypes and nine hybrids. Two thirds of the taxa are polyploid, with many species presumed to be of allopolyploid origin. We discovered a remarkably close relationship between the local cytotype of R. peltatus s.l. and the morphologically distinct, widespread and ecologically specialized species R. fluitans; the latter might have evolved as a result of rapid adaptation to newly colonized river habitats in the early postglacial period. Undeniably, diversity within this group is still incompletely understood and is far more complex than current taxonomic concepts suggest.
- Keywords
- Chromosome number, Cryptic variation, Genome size, Hybridization, Molecular identification, Polyploidy,
- MeSH
- Biodiversity * MeSH
- Biological Evolution * MeSH
- DNA, Plant genetics MeSH
- Phylogeny MeSH
- Genetic Variation MeSH
- Evolution, Molecular MeSH
- Ploidies MeSH
- Polyploidy MeSH
- Ranunculus * genetics classification MeSH
- Sequence Analysis, DNA MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
- Names of Substances
- DNA, Plant MeSH
The genus Chenopodium L. is characterized by its wide geographic distribution and ecological adaptability. Species such as quinoa (Chenopodium quinoa Willd.) have served as domesticated staple crops for centuries. Wild Chenopodium species exhibit diverse niche adaptations and are important genetic reservoirs for beneficial agronomic traits, including disease resistance and climate hardiness. To harness the potential of the wild taxa for crop improvement, we developed a Chenopodium pangenome through the assembly and comparative analyses of 12 Chenopodium species that encompass the eight known genome types (A-H). Six of the species are new chromosome-scale assemblies, and many are polyploids; thus, a total of 20 genomes were included in the pangenome analyses. We show that the genomes vary dramatically in size with the D genome being the smallest (∼370 Mb) and the B genome being the largest (∼700 Mb) and that genome size was correlated with independent expansions of the Copia and Gypsy LTR retrotransposon families, suggesting that transposable elements have played a critical role in the evolution of the Chenopodium genomes. We annotated a total of 33,457 pan-Chenopodium gene families, of which ∼65% were classified as shell (2% private). Phylogenetic analysis clarified the evolutionary relationships among the genome lineages, notably resolving the taxonomic placement of the F genome while highlighting the uniqueness of the A genome in the Western Hemisphere. These genomic resources are particularly important for understanding the secondary and tertiary gene pools available for the improvement of the domesticated chenopods while furthering our understanding of the evolution and complexity within the genus.
- MeSH
- Chenopodium * genetics MeSH
- Genome Size MeSH
- Phylogeny MeSH
- Genome, Plant * MeSH
- Terminal Repeat Sequences * genetics MeSH
- Evolution, Molecular * MeSH
- Retroelements MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Retroelements MeSH
BACKGROUND/OBJECTIVES: Arachnids are a megadiverse arthropod group. The present study investigated the chromosomes of pedipalpid tetrapulmonates (orders Amblypygi, Thelyphonida, Schizomida) and two arachnid orders of uncertain phylogenetic placement, Ricinulei and Solifugae, to reconstruct their karyotype evolution. Except for amblypygids, the cytogenetics of these arachnid orders was almost unknown prior to the present study. METHODS: Chromosomes were investigated using methods of standard (Giemsa-stained preparations, banding techniques) and molecular cytogenetics (fluorescence in situ hybridization, comparative genomic hybridization). RESULTS AND CONCLUSIONS: New data for 38 species, combined with previously published data, suggest that ancestral arachnids possessed low to moderate 2n (22-40), monocentric chromosomes, one nucleolus organizer region (NOR), low levels of heterochromatin and recombinations, and no or homomorphic sex chromosomes. Karyotypes of Pedipalpi and Solifugae diversified via centric fusions, pericentric inversions, and changes in the pattern of NORs and, in solifuges, also through tandem fusions. Some solifuges display an enormous amount of constitutive heterochromatin and high NOR number. It is hypothesized that the common ancestor of amblypygids, thelyphonids, and spiders exhibited a homomorphic XY system, and that telomeric heterochromatin and NORs were involved in the evolution of amblypygid sex chromosomes. The new findings support the Cephalosomata clade (acariforms, palpigrades, and solifuges). Hypotheses concerning the origin of acariform holocentric chromosomes are presented. Unlike current phylogenetic hypotheses, the results suggest a sister relationship between Schizomida and a clade comprising other tetrapulmonates as well as a polyploidization in the common ancestor of the clade comprising Araneae, Amblypygi, and Thelyphonida.
- Keywords
- Ricinulei, heterochromatin, holocentric, nucleolus organizer region, polyploidy, sex chromosome, solifuge, somatic pairing, spider, telomere,
- MeSH
- Phylogeny MeSH
- In Situ Hybridization, Fluorescence MeSH
- Karyotype * MeSH
- Karyotyping MeSH
- Evolution, Molecular * MeSH
- Arachnida * genetics classification MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Numerous plant species are expanding their native ranges due to anthropogenic environmental change. Because cytotypes of polyploid complexes often show similar morphologies, there may be unnoticed range expansions (i.e. cryptic invasions) of one cytotype into regions where only the other cytotype is native. We critically revised herbarium specimens of diploid and tetraploid Centaurea stoebe, collected across Europe between 1790 and 2023. Based on their distribution in natural and relict habitats and phylogeographic data, we estimated the native ranges of both cytotypes. Diploids are native across their entire European range, whereas tetraploids are native only to South-Eastern Europe and have recently expanded their range toward Central Europe. The proportion of tetraploids has exponentially increased over time in their expanded but not in their native range. This cryptic invasion predominantly occurred in ruderal habitats and enlarged the climatic niche of tetraploids toward a more oceanic climate. We conclude that spatio-temporally explicit assessments of range shifts, habitat preferences and niche evolution can improve our understanding of cryptic invasions. We also emphasize the value of herbarium specimens for accurate estimation of species´ native ranges, with fundamental implications for the design of research studies and the assessment of biodiversity trends.
- Keywords
- Centaurea stoebe (spotted knapweed), climatic niche, colonization ability, cryptic invasion, herbarium specimens, polyploidy, range expansion, ruderal habitats,
- MeSH
- Centaurea * genetics physiology MeSH
- Diploidy MeSH
- Ecosystem MeSH
- Phylogeography MeSH
- Polyploidy * MeSH
- Introduced Species * MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
BACKGROUND: Genome size is influenced by natural selection and genetic drift acting on variations from polyploidy and repetitive DNA sequences. We hypothesized that centromere drive, where centromeres compete for inclusion in the functional gamete during meiosis, may also affect genome and chromosome size. This competition occurs in asymmetric meiosis, where only one of the four meiotic products becomes a gamete. If centromere drive influences chromosome size evolution, it may also impact post-polyploid diploidization, where a polyploid genome is restructured to function more like a diploid through chromosomal rearrangements, including fusions. We tested if plant lineages with asymmetric meiosis exhibit faster chromosome size evolution compared to those with only symmetric meiosis, which lack centromere drive as all four meiotic products become gametes. We also examined if positive selection on centromeric histone H3 (CENH3), a protein that can suppress centromere drive, is more frequent in these asymmetric lineages. METHODS: We analysed plant groups with different meiotic modes: asymmetric in gymnosperms and angiosperms, and symmetric in bryophytes, lycophytes and ferns. We selected species based on available CENH3 gene sequences and chromosome size data. Using Ornstein-Uhlenbeck evolutionary models and phylogenetic regressions, we assessed the rates of chromosome size evolution and the frequency of positive selection on CENH3 in these clades. RESULTS: Our analyses showed that clades with asymmetric meiosis have a higher frequency of positive selection on CENH3 and increased rates of chromosome size evolution compared to symmetric clades. CONCLUSIONS: Our findings support the hypothesis that centromere drive accelerates chromosome and genome size evolution, potentially also influencing the process of post-polyploid diploidization. We propose a model which in a single framework helps explain the stability of chromosome size in symmetric lineages (bryophytes, lycophytes and ferns) and its variability in asymmetric lineages (gymnosperms and angiosperms), providing a foundation for future research in plant genome evolution.
- Keywords
- Angiosperms, CENH3, asymmetric and symmetric meiosis, bryophytes, centromere drive, chromosome size, ferns, genome size, gymnosperms, lycophytes, post-polyploid diploidization,
- MeSH
- Biological Evolution MeSH
- Centromere * genetics MeSH
- Chromosomes, Plant * genetics MeSH
- Cycadopsida genetics MeSH
- Genome Size * MeSH
- Phylogeny MeSH
- Genome, Plant * genetics MeSH
- Histones genetics metabolism MeSH
- Ferns genetics physiology MeSH
- Magnoliopsida genetics MeSH
- Meiosis * genetics MeSH
- Evolution, Molecular * MeSH
- Polyploidy MeSH
- Plants genetics MeSH
- Selection, Genetic MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Histones MeSH
BACKGROUND: The genus Allium is known for its high chromosomal variability, but most chromosome counts are based on a few individuals and genome size (GS) reports are limited in certain taxonomic groups. This is evident in the Allium sect. Codonoprasum, a species-rich (> 150 species) and taxonomically complex section with weak morphological differences between taxa, the presence of polyploidy and frequent misidentification of taxa. Consequently, a significant proportion of older karyological reports may be unreliable and GS data are lacking for the majority of species within the section. This study, using chromosome counting and flow cytometry (FCM), provides the first comprehensive and detailed insight into variation in chromosome number, polyploid frequency and distribution, and GS in section members, marking a step towards understanding the unresolved diversification and evolution of this group. RESULTS: We analysed 1578 individuals from 316 populations of 25 taxa and reported DNA ploidy levels and their GS, with calibration from chromosome counts in 22 taxa. Five taxa had multiple ploidy levels. First estimates of GS were obtained for 16 taxa. A comprehensive review of chromosome number and DNA-ploidy levels in 129 taxa of the section revealed that all taxa have x = 8, except A. rupestre with two polyploid series (x = 8, descending dysploidy x = 7), unique for this section. Diploid taxa dominated (72.1%), while di- & polyploid (12.4%) and exclusively polyploid (15.5%) taxa were less common. Ploidy diversity showed that diploid taxa dominated in the eastern Mediterranean and decreased towards the west and north, whereas only polyploid cytotypes of di- & polyploid taxa or exclusively polyploid taxa dominated in northern and northwestern Europe. A 4.1-fold variation in GS was observed across 33 taxa analysed so far (2C = 22.3-92.1 pg), mainly due to polyploidy, with GS downsizing observed in taxa with multiple ploidy levels. Intra-sectional GS variation suggests evolutionary relationships, and intraspecific GS variation within some taxa may indicate taxonomic heterogeneity and/or historical migration patterns. CONCLUSIONS: Our study showed advantages of FCM as an effective tool for detecting ploidy levels and determining GS within the section. GS could be an additional character in understanding evolution and phylogenetic relationships within the section.
- Keywords
- Chromosome number, Cytogeography, DNA ploidy level, Flow cytometry, Genome size, Polyploidy,
- Publication type
- Journal Article MeSH
Plant species diversity may be considerably underestimated, especially in evolutionarily complex genera and in diversity hotspots that have enabled long-term species persistence and diversification, such as the Balkan Peninsula. Here, we address the topic of underexplored plant diversity and underlying evolutionary and biogeographic processes by investigating the hygrophytic mountain species complex of Cardamine acris s.l. distributed in the Balkans (three subspecies within C. acris) and northwestern Anatolia (C. anatolica). We performed a series of phylogenetic and phylogeographic analyses based on restriction-site associated DNA sequencing (RADseq) and target enrichment (Hyb-Seq) data in combination with habitat suitability modelling. We found C. anatolica as a clade nested within the Balkan C. acris, probably resulting from a founder event, and uncovered three allopatric cryptic lineages within C. acris subsp. acris, allowing us to recognise a total of six entities in this complex. We observed the deepest genetic split within C. acris subsp. acris in the western Balkans, which was at odds with taxonomy and showed no distribution gap. We inferred vicariance as the most likely process for population divergence in the Balkans, accompanied by gene flow between the recognised entities, which was consistent with the modelled habitat suitability dynamics. Furthermore, we discovered several polyploid populations in C. acris, representing both pure intra- and inter-lineage hybrid polyploids, but detected only minor traces of hybridization with related congeners. Overall, our results illustrate that diverse evolutionary processes may influence the history of mountain plant species in the Balkan Peninsula, including vicariance, reticulation, polyploidization and cryptic diversification.
- Keywords
- Hyb‐Seq, RAD sequencing, habitat suitability modelling, phylogeography, polyploidy, vicariance,
- MeSH
- Cardamine * genetics classification MeSH
- DNA, Plant genetics MeSH
- Ecosystem MeSH
- Phylogeny * MeSH
- Phylogeography * MeSH
- Genetic Variation MeSH
- Genome, Plant MeSH
- Genetics, Population MeSH
- Sequence Analysis, DNA MeSH
- Gene Flow MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Balkan Peninsula MeSH
- Turkey MeSH
- Names of Substances
- DNA, Plant MeSH
BACKGROUND: Polyploidisation often results in genome rearrangements that may involve changes in both the single-copy sequences and the repetitive genome fraction. In this study, we performed a comprehensive comparative analysis of repetitive DNA, with a particular focus on ribosomal DNA (rDNA), in Brachypodium hybridum (2n = 4x = 30, subgenome composition DDSS), an allotetraploid resulting from a natural cross between two diploid species that resemble the modern B. distachyon (2n = 10; DD) and B. stacei (2n = 20; SS). Taking advantage of the recurrent origin of B. hybridum, we investigated two genotypes, Bhyb26 and ABR113, differing markedly in their evolutionary age (1.4 and 0.14 Mya, respectively) and which resulted from opposite cross directions. To identify the origin of rDNA loci we employed cytogenetic and molecular methods (FISH, gCAPS and Southern hybridisation), phylogenetic and genomic approaches. RESULTS: Unlike the general maintenance of doubled gene dosage in B. hybridum, the rRNA genes showed a remarkable tendency towards diploidisation at both locus and unit levels. While the partial elimination of 35S rDNA units occurred in the younger ABR113 lineage, unidirectional elimination of the entire locus was observed in the older Bhyb26 lineage. Additionally, a novel 5S rDNA family was amplified in Bhyb26 replacing the parental units. The 35S and 5S rDNA units were preferentially eliminated from the S- and D-subgenome, respectively. Thus, in the more ancient B. hybridum lineage, Bhyb26, 5S and 35S rRNA genes are likely expressed from different subgenomes, highlighting the complexity of polyploid regulatory networks. CONCLUSION: Comparative analyses between two B. hybridum lineages of distinct evolutionary ages revealed that although the recent lineage ABR113 exhibited an additive pattern of rDNA loci distribution, the ancient lineage Bhyb26 demonstrated a pronounced tendency toward diploidisation manifested by the reduction in the number of both 35S and 5S loci. In conclusion, the age of the allopolyploid appears to be a decisive factor in rDNA turnover in B. hybridum.
- Keywords
- Brachypodium hybridum, 35S rDNA IGS, FISH, 5S rDNA NTS, nrITS, rDNA loci,
- MeSH
- Brachypodium * genetics MeSH
- Phylogeny * MeSH
- Genetic Variation MeSH
- Genome, Plant MeSH
- Genes, rRNA genetics MeSH
- Evolution, Molecular * MeSH
- Polyploidy * MeSH
- DNA, Ribosomal genetics MeSH
- RNA, Ribosomal genetics MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Ribosomal MeSH
- RNA, Ribosomal MeSH
