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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 -
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 -
Biology Letters Dec 2022Whole-genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects, the resulting morphological and fitness consequences and how they... (Meta-Analysis)
Meta-Analysis
Whole-genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects, the resulting morphological and fitness consequences and how they affect the survival of polyploid lineages are intensively studied. Another important factor may also determine the probability of establishment and success of polyploid lineages: inbreeding depression. Inbreeding depression is expected to play an important role in the establishment of neopolyploid lineages, their capacity to colonize new environments, and in the simultaneous evolution of ploidy and other life-history traits such as self-fertilization. Both theoretically and empirically, there is no consensus on the consequences of polyploidy on inbreeding depression. In this meta-analysis, we investigated the effect of polyploidy on the evolution of inbreeding depression, by performing a meta-analysis within angiosperm species. The main results of our study are that the consequences of polyploidy on inbreeding depression are complex and depend on the time since polyploidization. We found that young polyploid lineages have a much lower amount of inbreeding depression than their diploid relatives and their established counterparts. Natural polyploid lineages are intermediate and have a higher amount of inbreeding depression than synthetic neopolyploids, and a smaller amount than diploids, suggesting that the negative effect of polyploidy on inbreeding depression decreases with time since polyploidization.
Topics: Inbreeding Depression; Polyploidy; Diploidy; Inbreeding; Magnoliopsida
PubMed: 36514955
DOI: 10.1098/rsbl.2022.0477 -
Genes Jan 2024Cells with an abnormal number of chromosomes have been found in more than 90% of solid tumors, and among these, polyploidy accounts for about 40%. Polyploidized cells... (Review)
Review
Cells with an abnormal number of chromosomes have been found in more than 90% of solid tumors, and among these, polyploidy accounts for about 40%. Polyploidized cells most often have duplicate centrosomes as well as genomes, and thus their mitosis tends to promote merotelic spindle attachments and chromosomal instability, which produces a variety of aneuploid daughter cells. Polyploid cells have been found highly resistant to various stress and anticancer therapies, such as radiation and mitogenic inhibitors. In other words, common cancer therapies kill proliferative diploid cells, which make up the majority of cancer tissues, while polyploid cells, which lurk in smaller numbers, may survive. The surviving polyploid cells, prompted by acute environmental changes, begin to mitose with chromosomal instability, leading to an explosion of genetic heterogeneity and a concomitant cell competition and adaptive evolution. The result is a recurrence of the cancer during which the tenacious cells that survived treatment express malignant traits. Although the presence of polyploid cells in cancer tissues has been observed for more than 150 years, the function and exact role of these cells in cancer progression has remained elusive. For this reason, there is currently no effective therapeutic treatment directed against polyploid cells. This is due in part to the lack of suitable experimental models, but recently several models have become available to study polyploid cells in vivo. We propose that the experimental models in , for which genetic techniques are highly developed, could be very useful in deciphering mechanisms of polyploidy and its role in cancer progression.
Topics: Animals; Drosophila; Neoplasms; Polyploidy; Centrosome; Chromosomal Instability
PubMed: 38254985
DOI: 10.3390/genes15010096 -
Seminars in Cancer Biology Jun 2022Therapeutic resistance represents a major cause of death for most lethal cancers. However, the underlying mechanisms of such resistance have remained unclear. The... (Review)
Review
Therapeutic resistance represents a major cause of death for most lethal cancers. However, the underlying mechanisms of such resistance have remained unclear. The polyploid cells are due to an increase in DNA content, commonly associated with cell enlargement. In human, they play a variety of roles in physiology and pathologic conditions and perform the specialized functions during development, inflammation, and cancer. Recent work shows that cancer cells can be induced into polyploid giant cancer cells (PGCCs) that leads to reprogramming of surviving cancer cells to acquire resistance. In this article, we will review the polyploidy involved in development and inflammation, and the process of PGCCs formation and propagation that benefits to cell survival. We will discuss the potential opportunities in fighting resistant cancers. The increased knowledge of PGCCs will offer a completely new paradigm to explore the therapeutic intervention for lethal cancers.
Topics: Giant Cells; Humans; Inflammation; Neoplasms; Polyploidy
PubMed: 33839294
DOI: 10.1016/j.semcancer.2021.04.005 -
Development (Cambridge, England) Jun 2023The placenta is essential for reproductive success. The murine placenta includes polyploid giant cells that are crucial for its function. Polyploidy occurs broadly in...
The placenta is essential for reproductive success. The murine placenta includes polyploid giant cells that are crucial for its function. Polyploidy occurs broadly in nature but its regulators and significance in the placenta are unknown. We have discovered that many murine placental cell types are polyploid and have identified factors that license polyploidy using single-cell RNA sequencing. Myc is a key regulator of polyploidy and placental development, and is required for multiple rounds of DNA replication, likely via endocycles, in trophoblast giant cells. Furthermore, MYC supports the expression of DNA replication and nucleotide biosynthesis genes along with ribosomal RNA. Increased DNA damage and senescence occur in trophoblast giant cells without Myc, accompanied by senescence in the neighboring maternal decidua. These data reveal Myc is essential for polyploidy to support normal placental development, thereby preventing premature senescence. Our study, combined with available literature, suggests that Myc is an evolutionarily conserved regulator of polyploidy.
Topics: Animals; Female; Mice; Pregnancy; Placenta; Placentation; Polyploidy; Trophoblasts
PubMed: 37278344
DOI: 10.1242/dev.201581 -
The Plant Journal : For Cell and... Aug 2022Polyploidy is a major force shaping eukaryote evolution but poses challenges for meiotic chromosome segregation. As a result, first-generation polyploids often suffer...
Polyploidy is a major force shaping eukaryote evolution but poses challenges for meiotic chromosome segregation. As a result, first-generation polyploids often suffer from more meiotic errors and lower fertility than established wild polyploid populations. How established polyploids adapt their meiotic behaviour to ensure genome stability and accurate chromosome segregation remains an active research question. We present here a cytological description of meiosis in the model allopolyploid species Arabidopsis suecica (2n = 4x = 26). In large part meiosis in A. suecica is diploid-like, with normal synaptic progression and no evidence of synaptic partner exchanges. Some abnormalities were seen at low frequency, including univalents at metaphase I, anaphase bridges and aneuploidy at metaphase II; however, we saw no evidence of crossover formation occurring between non-homologous chromosomes. The crossover number in A. suecica is similar to the combined number reported from its diploid parents Arabidopsis thaliana (2n = 2x = 10) and Arabidopsis arenosa (2n = 2x = 16), with an average of approximately 1.75 crossovers per chromosome pair. This contrasts with naturally evolved autotetraploid A. arenosa, where accurate chromosome segregation is achieved by restricting crossovers to approximately 1 per chromosome pair. Although an autotetraploid donor is hypothesized to have contributed the A. arenosa subgenome to A. suecica, A. suecica harbours diploid A. arenosa variants of key meiotic genes. These multiple lines of evidence suggest that meiosis in the recently evolved allopolyploid A. suecica is essentially diploid like, with meiotic adaptation following a very different trajectory to that described for autotetraploid A. arenosa.
Topics: Arabidopsis; Diploidy; Genome, Plant; Meiosis; Polyploidy
PubMed: 35759495
DOI: 10.1111/tpj.15879 -
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 -
Trends in Parasitology Nov 2016While some amoebae reproduce sexually, many amoebae (e.g., Acanthamoeba, Naegleria) reproduce asexually and therefore, according to popular doctrine, are likely to have... (Review)
Review
While some amoebae reproduce sexually, many amoebae (e.g., Acanthamoeba, Naegleria) reproduce asexually and therefore, according to popular doctrine, are likely to have been genetically disadvantaged as a consequence. In the absence of sex, mutations are proposed to accumulate by a mechanism known as Muller's ratchet. I hypothesise that amoebae can escape the ravages of accumulated mutation by virtue of their being polyploid. The polyploid state reduces spontaneous mutation accumulation by gene conversion, the freshly mutated copy being corrected by the presence of the many other wild-type copies. In this manner these amoebae reap the benefits of an asexual reproductive existence: principally, that it is rapid and convenient. Evidence for this mechanism comes from polyploid plants, bacteria, and archaea.
Topics: Amoeba; Gene Conversion; Mutation; Polyploidy; Reproduction, Asexual
PubMed: 27599632
DOI: 10.1016/j.pt.2016.08.006 -
The American Naturalist Aug 2022AbstractDetermining how and how often asexual lineages emerge within sexual species is central to our understanding of sex-asex transitions and the long-term maintenance...
AbstractDetermining how and how often asexual lineages emerge within sexual species is central to our understanding of sex-asex transitions and the long-term maintenance of sex. Asexuality can arise "by transmission" from an existing asexual lineage to a new one through different types of crosses. The occurrence of these crosses, cryptic sex, variations in ploidy, and recombination within asexuals greatly complicates the study of sex-asex transitions, as they preclude the use of standard phylogenetic methods and genetic distance metrics. In this study we show how to overcome these challenges by developing new approaches to investigate the origin of the various asexual lineages of the brine shrimp . We use a large sample of asexuals, including all known polyploids, and their sexual relatives. We combine flow cytometry with mitochondrial and nuclear DNA data. We develop new genetic distance measures and methods to compare various scenarios describing the origin of the different lineages. We find that all diploid and polyploid likely arose within the past 80,000 years through successive and nested hybridization events that involved backcrosses with different sexual species. All have the same common ancestor and therefore likely carry the same asexuality gene(s) and reproduce by automixis. These findings radically change our view of sex-asex transitions in this group and show the importance of considering scenarios of asexuality by transmission. The methods developed are applicable to many other asexual taxa.
Topics: Animals; Artemia; Parthenogenesis; Phylogeny; Polyploidy; Reproduction, Asexual
PubMed: 35905400
DOI: 10.1086/720268