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Nature Communications Jul 2023Polyploidization can provide a wealth of genetic variation for adaptive evolution and speciation, but understanding the mechanisms of subgenome evolution as well as its...
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., FMO, 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.
Topics: Armoracia; Genome, Plant; Plant Breeding; Genomics; Polyploidy; Evolution, Molecular
PubMed: 37491530
DOI: 10.1038/s41467-023-39800-y -
Annual Review of Plant Biology Jun 2021Most land plants are now known to be ancient polyploids that have rediploidized. Diploidization involves many changes in genome organization that ultimately restore... (Review)
Review
Most land plants are now known to be ancient polyploids that have rediploidized. Diploidization involves many changes in genome organization that ultimately restore bivalent chromosome pairing and disomic inheritance, and resolve dosage and other issues caused by genome duplication. In this review, we discuss the nature of polyploidy and its impact on chromosome pairing behavior. We also provide an overview of two major and largely independent processes of diploidization: cytological diploidization and genic diploidization/fractionation. Finally, we compare variation in gene fractionation across land plants and highlight the differences in diploidization between plants and animals. Altogether, we demonstrate recent advancements in our understanding of variation in the patterns and processes of diploidization in land plants and provide a road map for future research to unlock the mysteries of diploidization and eukaryotic genome evolution.
Topics: Animals; Embryophyta; Evolution, Molecular; Genome, Plant; Plants; Polyploidy
PubMed: 33684297
DOI: 10.1146/annurev-arplant-050718-100344 -
Plant Physiology Nov 2022Cucurbitales are an important order of flowering plants known for encompassing edible plants of economic and medicinal value and numerous ornamental plants of...
Cucurbitales are an important order of flowering plants known for encompassing edible plants of economic and medicinal value and numerous ornamental plants of horticultural value. By reanalyzing the genomes of two representative families (Cucurbitaceae and Begoniaceae) in Cucurbitales, we found that the previously identified Cucurbitaceae common paleotetraploidization that occurred shortly after the core-eudicot-common hexaploidization event is shared by Cucurbitales, including Begoniaceae. We built a multigenome alignment framework for Cucurbitales by identifying orthologs and paralogs and systematically redating key evolutionary events in Cucurbitales. Notably, characterizing the gene retention levels and genomic fractionation patterns between subgenomes generated from different polyploidizations in Cucurbitales suggested the autopolyploid nature of the Begoniaceae common tetraploidization and the allopolyploid nature of the Cucurbitales common tetraploidization and the Cucurbita-specific tetraploidization. Moreover, we constructed the ancestral Cucurbitales karyotype comprising 17 proto-chromosomes, confirming that the most recent common ancestor of Cucurbitaceae contained 15 proto-chromosomes and rejecting the previous hypothesis for an ancestral Cucurbitaceae karyotype with 12 proto-chromosomes. In addition, we found that the polyploidization and tandem duplication events promoted the expansion of gene families involved in the cucurbitacin biosynthesis pathway; however, gene loss and chromosomal rearrangements likely limited the expansion of these gene families.
Topics: Genome, Plant; Evolution, Molecular; Phylogeny; Magnoliopsida; Cucurbitaceae; Polyploidy
PubMed: 36053177
DOI: 10.1093/plphys/kiac410 -
Current Opinion in Plant Biology Apr 2015Polyploidy or whole-genome duplication occurs in some animals and many flowering plants, including many important crops such as wheat, cotton and oilseed rape. The... (Review)
Review
Polyploidy or whole-genome duplication occurs in some animals and many flowering plants, including many important crops such as wheat, cotton and oilseed rape. The prevalence of polyploidy in the plant kingdom suggests it as an important evolutionary feature for plant speciation and crop domestication. Studies of natural and synthetic polyploids have revealed rapid and dynamic changes in genomic structure and gene expression after polyploid formation. Growing evidence suggests that epigenetic modifications can alter homoeologous gene expression and reprogram gene expression networks, which allows polyploids to establish new cytotypes, grow vigorously and promote adaptation in local environments. Sequence and gene expression changes in polyploids have been well documented and reviewed elsewhere. This review is focused on developmental regulation and epigenetic changes including DNA methylation and histone modifications in polyploids.
Topics: DNA Methylation; Epigenesis, Genetic; Histones; Plant Development; Plant Proteins; Plants; Polyploidy
PubMed: 25765928
DOI: 10.1016/j.pbi.2015.02.007 -
Genetics Aug 2023Polyploidy is an important generator of evolutionary novelty across diverse groups in the Tree of Life, including many crops. However, the impact of whole-genome...
Polyploidy is an important generator of evolutionary novelty across diverse groups in the Tree of Life, including many crops. However, the impact of whole-genome duplication depends on the mode of formation: doubling within a single lineage (autopolyploidy) versus doubling after hybridization between two different lineages (allopolyploidy). Researchers have historically treated these two scenarios as completely separate cases based on patterns of chromosome pairing, but these cases represent ideals on a continuum of chromosomal interactions among duplicated genomes. Understanding the history of polyploid species thus demands quantitative inferences of demographic history and rates of exchange between subgenomes. To meet this need, we developed diffusion models for genetic variation in polyploids with subgenomes that cannot be bioinformatically separated and with potentially variable inheritance patterns, implementing them in the dadi software. We validated our models using forward SLiM simulations and found that our inference approach is able to accurately infer evolutionary parameters (timing, bottleneck size) involved with the formation of auto- and allotetraploids, as well as exchange rates in segmental allotetraploids. We then applied our models to empirical data for allotetraploid shepherd's purse (Capsella bursa-pastoris), finding evidence for allelic exchange between the subgenomes. Taken together, our model provides a foundation for demographic modeling in polyploids using diffusion equations, which will help increase our understanding of the impact of demography and selection in polyploid lineages.
Topics: Polyploidy; Biological Evolution; Hybridization, Genetic; Capsella; Demography
PubMed: 37279657
DOI: 10.1093/genetics/iyad107 -
The New Phytologist Apr 2021Rare yet accumulating evidence in both plants and animals shows that whole genome duplication (WGD, leading to polyploidy) can break down reproductive barriers,... (Review)
Review
Rare yet accumulating evidence in both plants and animals shows that whole genome duplication (WGD, leading to polyploidy) can break down reproductive barriers, facilitating gene flow between otherwise isolated species. Recent population genomic studies in wild, outcrossing Arabidopsis arenosa and Arabidopsis lyrata indicate that this WGD-potentiated gene flow can be adaptive and highly specific in response to particular environmental and intracellular challenges. The mechanistic basis of WGD-mediated easing of species barrier strength seems to primarily lie in the relative dosage of each parental genome in the endosperm. While generalisations about polyploids can be fraught, this evidence indicates that the breakdown of these barriers, combined with diploid to polyploid gene flow and gene flow between polyploids, allows some polyploids to act as adaptable 'allelic sponges', enjoying increased potential to respond to challenging environments.
Topics: Animals; Arabidopsis; Diploidy; Gene Flow; Genome, Plant; Polyploidy
PubMed: 33454987
DOI: 10.1111/nph.17204 -
Planta Feb 2016This article provides an up-to-date review concerning from basic issues of polyploidy to aspects regarding the relevance and role of both natural and artificial... (Review)
Review
This article provides an up-to-date review concerning from basic issues of polyploidy to aspects regarding the relevance and role of both natural and artificial polyploids in plant breeding programs. Polyploidy is a major force in the evolution of both wild and cultivated plants. Polyploid organisms often exhibit increased vigor and, in some cases, outperform their diploid relatives in several aspects. This remarkable superiority of polyploids has been the target of many plant breeders in the last century, who have induced polyploidy and/or used natural polyploids in many ways to obtain increasingly improved plant cultivars. Some of the most important consequences of polyploidy for plant breeding are the increment in plant organs ("gigas" effect), buffering of deleterious mutations, increased heterozygosity, and heterosis (hybrid vigor). Regarding such features as tools, cultivars have been generated with higher yield levels, improving the product quality and increasing the tolerance to both biotic and abiotic stresses. In some cases, when the crossing between two species is not possible because of differences in ploidy level, polyploids can be used as a bridge for gene transferring between them. In addition, polyploidy often results in reduced fertility due to meiotic errors, allowing the production of seedless varieties. On the other hand, the genome doubling in a newly formed sterile hybrid allows the restoration of its fertility. Based on these aspects, the present review initially concerns the origin, frequency and classification of the polyploids, progressing to show the revolution promoted by the discovery of natural polyploids and polyploidization induction in the breeding program status of distinct crops.
Topics: Fertility; Genome, Plant; Hybrid Vigor; Plant Breeding; Plants; Polyploidy
PubMed: 26715561
DOI: 10.1007/s00425-015-2450-x -
Current Opinion in Plant Biology Oct 2022The prevalence of polyploidy in wild and crop species has stimulated debate over its evolutionary advantages and disadvantages. Previous studies have focused on changes... (Review)
Review
The prevalence of polyploidy in wild and crop species has stimulated debate over its evolutionary advantages and disadvantages. Previous studies have focused on changes occurring at the polyploidization events, including genome-wide changes termed "genome shock," as well as ancient polyploidy. Recent bioinformatics advances and empirical studies of Arabidopsis and wheat relatives are filling a research gap: the functional evolutionary study of polyploid species using RNA-seq, DNA polymorphism, and epigenomics. Polyploid species can become generalists in natura through environmental robustness by inheriting and merging parental stress responses. Their evolvability is enhanced by mutational robustness working on inherited standing variation. The identification of key genes responsible for gradual adaptive evolution will encourage synthetic biological approaches to transfer polyploid advantages to other species.
Topics: Arabidopsis; Evolution, Molecular; Genome, Plant; Polyploidy; Triticum
PubMed: 36063635
DOI: 10.1016/j.pbi.2022.102292 -
Tree Physiology Oct 2022The apple rootstock Malus prunifolia (Willd.) Borkh. is widely used for apple production. Because polyploid plants are often more tolerant to abiotic stress than...
The apple rootstock Malus prunifolia (Willd.) Borkh. is widely used for apple production. Because polyploid plants are often more tolerant to abiotic stress than diploids, we wondered whether polyploidy induction in M. prunifolia might improve its stress tolerance, particularly to high salinity. We used a combination of colchicine and dimethyl sulfoxide (DMSO) to induce chromosome doubling in M. prunifolia and identified the resulting polyploids by stomatal observations and flow cytometry. We found the best way to induce polyploidy in M. prunifolia was to use 2% DMSO and 0.05% colchicine for 2 days for leaves or 0.02% colchicine for stem segments. The results of hydroponic salt treatment showed that polyploid plants were more salt tolerant and had greater photosynthetic efficiency, thicker leaf epidermis and palisade tissues, and shorter but denser root systems than diploids. During salt stress, the polyploid leaves and roots accumulated less Na+, showed upregulated expression of three salt overly sensitive (SOS) pathway genes, and produced fewer reactive oxygen species. The polyploid plants also had considerably higher ABA and jasmonic acid levels than diploid plants under salt stress. Under normal growth conditions, gibberellins (GAs) levels were much lower in polyploid leaves than in diploid leaves; however, after salt treatment, polyploid leaves showed upregulation of essential GAs synthesis genes. In summary, we developed a system for the induction of polyploidy in M. prunifolia and response to salt stress of the resulting polyploids, as reflected in leaf and root morphology, changes in Na+ accumulation, antioxidant capacity and plant hormone levels.
Topics: Antioxidants; Colchicine; Dimethyl Sulfoxide; Gibberellins; Malus; Plant Growth Regulators; Plant Leaves; Plant Roots; Polyploidy; Reactive Oxygen Species; Salt Tolerance
PubMed: 35532080
DOI: 10.1093/treephys/tpac053 -
Trends in Ecology & Evolution May 2024Cold temperatures have been posited as a key driver of polyploidy (possession of multiple chromosome sets). However, high temperatures associated with fire, and the...
Cold temperatures have been posited as a key driver of polyploidy (possession of multiple chromosome sets). However, high temperatures associated with fire, and the indirect impact of post-fire environments in polypoid formation and establishment deserve more attention for a comprehensive understanding of polyploid ecology, evolution, and current distributions.
Topics: Biological Evolution; Cold Temperature; Fires; Polyploidy
PubMed: 38521739
DOI: 10.1016/j.tree.2024.02.007