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BMC Biology Nov 2020Wheat is a powerful genetic model for studying polyploid evolution and crop domestication. Hexaploid bread wheat was formed by two rounds of interspecific hybridization...
BACKGROUND
Wheat is a powerful genetic model for studying polyploid evolution and crop domestication. Hexaploid bread wheat was formed by two rounds of interspecific hybridization and polyploidization, processes which are often accompanied by genetic and epigenetic changes, including DNA methylation. However, the extent and effect of such changes during wheat evolution, particularly from tetraploid-to-hexaploid wheat, are currently elusive.
RESULTS
Here we report genome-wide DNA methylation landscapes in extracted tetraploid wheat (ETW, AABB), natural hexaploid wheat (NHW, AABBDD), resynthesized hexaploid wheat (RHW, AABBDD), natural tetraploid wheat (NTW, AABB), and diploid (DD). In the endosperm, levels of DNA methylation, especially in CHG (H=A, T, or C) context, were dramatically decreased in the ETW relative to natural hexaploid wheat; hypo-differentially methylated regions (DMRs) (850,832) were 24-fold more than hyper-DMRs (35,111). Interestingly, those demethylated regions in ETW were remethylated in the resynthesized hexaploid wheat after the addition of the D genome. In ETW, hypo-DMRs correlated with gene expression, and TEs were demethylated and activated, which could be silenced in the hexaploid wheat. In NHW, groups of TEs were dispersed in genic regions of three subgenomes, which may regulate the expression of TE-associated genes. Further, hypo-DMRs in ETW were associated with reduced H3K9me2 levels and increased expression of histone variant genes, suggesting concerted epigenetic changes after separation from the hexaploid.
CONCLUSION
Genome merger and separation provoke dynamic and reversible changes in chromatin and DNA methylation. These changes correlate with altered gene expression and TE activity, which may provide insights into polyploid genome and wheat evolution.
Topics: Biological Evolution; DNA Methylation; Domestication; Evolution, Molecular; Genome, Plant; Polyploidy; Triticum
PubMed: 33218336
DOI: 10.1186/s12915-020-00909-x -
International Journal of Molecular... 2012Polyploidy is a very common phenomenon in the plant kingdom, where even diploid species are often described as paleopolyploids. The polyploid condition may bring about... (Review)
Review
Polyploidy is a very common phenomenon in the plant kingdom, where even diploid species are often described as paleopolyploids. The polyploid condition may bring about several advantages compared to the diploid state. Polyploids often show phenotypes that are not present in their diploid progenitors or exceed the range of the contributing species. Some of these traits may play a role in heterosis or could favor adaptation to new ecological niches. Advances in genomics and sequencing technology may create unprecedented opportunities for discovering and monitoring the molecular effects of polyploidization. Through this review, we provide an overview of technologies and strategies that may allow an in-depth analysis of polyploid genomes. After introducing some basic aspects on the origin and genetics of polyploids, we highlight the main tools available for genome and gene expression analysis and summarize major findings. In the last part of this review, the implications of next generation sequencing are briefly discussed. The accumulation of knowledge on polyploid formation, maintenance, and divergence at whole-genome and subgenome levels will not only help plant biologists to understand how plants have evolved and diversified, but also assist plant breeders in designing new strategies for crop improvement.
Topics: Genome, Plant; Genomics; High-Throughput Nucleotide Sequencing; Phenotype; Plants; Polyploidy
PubMed: 22949863
DOI: 10.3390/ijms130810316 -
Molecular Plant Jul 2022Potato (Solanum tuberosum) is the most consumed non-cereal food crop. Most commercial potato cultivars are autotetraploids with highly heterozygous genomes, severely...
Potato (Solanum tuberosum) is the most consumed non-cereal food crop. Most commercial potato cultivars are autotetraploids with highly heterozygous genomes, severely hampering genetic analyses and improvement. By leveraging the state-of-the-art sequencing technologies and polyploid graph binning, we achieved a chromosome-scale, haplotype-resolved genome assembly of a cultivated potato, Cooperation-88 (C88). Intra-haplotype comparative analyses revealed extensive sequence and expression differences in this tetraploid genome. We identified haplotype-specific pericentromeres on chromosomes, suggesting a distinct evolutionary trajectory of potato homologous centromeres. Furthermore, we detected double reduction events that are unevenly distributed on haplotypes in 1021 of 1034 selfing progeny, a feature of autopolyploid inheritance. By distinguishing maternal and paternal haplotype sets in C88, we simulated the origin of heterosis in cultivated tetraploid with a survey of 3110 tetra-allelic loci with deleterious mutations, which were masked in the heterozygous condition by two parents. This study provides insights into the genomic architecture of autopolyploids and will guide their breeding.
Topics: Haplotypes; Plant Breeding; Polyploidy; Solanum tuberosum; Tetraploidy
PubMed: 35733345
DOI: 10.1016/j.molp.2022.06.009 -
American Journal of Botany Oct 2022It is well-known that whole genome duplication (WGD) has played a significant role in the evolution of plants. The best-known phenotypic effect of WGD is the gigas...
PREMISE
It is well-known that whole genome duplication (WGD) has played a significant role in the evolution of plants. The best-known phenotypic effect of WGD is the gigas effect, or the enlargement of polyploid plant traits. WGD is often linked with increased weediness, which could be a result of fitness advantages conferred by the gigas effect. As a result, the gigas effect could potentially explain polyploid persistence and abundance. We test whether a gigas effect is present in the polyploid-rich geophyte Oxalis, at both organ and cellular scales.
METHODS
We measured traits in conspecific diploid and polyploid accessions of 24 species across the genus. In addition, we measured the same and additional traits in 20 populations of the weedy and highly ploidy-variable species Oxalis purpurea L., including measures of clonality and selfing as a proxy for weediness. Ploidy level was determined using flow cytometry.
RESULTS
We found substantial variation and no consistent ploidy-related size difference, both between and within species, and across traits. Oxalis purpurea polyploids did, however, produce significantly more underground biomass and more bulbils than diploids, consistent with a potential role of WGD in the weediness of this species.
CONCLUSIONS
Our results suggest a more nuanced role for the gigas effect, at least in Oxalis. It may be temporary, short-lived, and inconsistently expressed and retained on evolutionary time scales, but in the short term can contribute to lineage success via increased vegetative reproduction.
Topics: Oxalidaceae; Polyploidy; Diploidy; Ploidies; Reproduction
PubMed: 36193941
DOI: 10.1002/ajb2.16077 -
The American Journal of Pathology Jun 2019The liver contains diploid and polyploid hepatocytes (tetraploid, octaploid, etc.), with polyploids comprising ≥90% of the hepatocyte population in adult mice....
The liver contains diploid and polyploid hepatocytes (tetraploid, octaploid, etc.), with polyploids comprising ≥90% of the hepatocyte population in adult mice. Polyploid hepatocytes form multipolar spindles in mitosis, which lead to chromosome gains/losses and random aneuploidy. The effect of aneuploidy on liver function is unclear, and the degree of liver aneuploidy is debated, with reports showing aneuploidy affects 5% to 60% of hepatocytes. To study relationships among liver polyploidy, aneuploidy, and adaptation, mice lacking E2f7 and E2f8 in the liver (LKO), which have a polyploidization defect, were used. Polyploids were reduced fourfold in LKO livers, and LKO hepatocytes remained predominantly diploid after extensive proliferation. Moreover, nearly all LKO hepatocytes were euploid compared with control hepatocytes, suggesting polyploid hepatocytes are required for production of aneuploid progeny. To determine whether reduced polyploidy impairs adaptation, LKO mice were bred onto a tyrosinemia background, a disease model whereby the liver can develop disease-resistant, regenerative nodules. Although tyrosinemic LKO mice were more susceptible to morbidities and death associated with tyrosinemia-induced liver failure, they developed regenerating nodules similar to control mice. Analyses revealed that nodules in the tyrosinemic livers were generated by aneuploidy and inactivating mutations. In summary, we identified new roles for polyploid hepatocytes and demonstrated that they are required for the formation of aneuploid progeny and can facilitate adaptation to chronic liver disease.
Topics: Adaptation, Physiological; Animals; E2F7 Transcription Factor; Gene Knockdown Techniques; Hepatocytes; Liver Regeneration; Lung Injury; Mice; Mice, Inbred NOD; Mice, Knockout; Polyploidy; Repressor Proteins
PubMed: 30928253
DOI: 10.1016/j.ajpath.2019.02.008 -
Hepatology (Baltimore, Md.) Mar 2019The liver contains a mixture of hepatocytes with diploid or polyploid (tetraploid, octaploid, etc.) nuclear content. Polyploid hepatocytes are commonly found in adult...
The liver contains a mixture of hepatocytes with diploid or polyploid (tetraploid, octaploid, etc.) nuclear content. Polyploid hepatocytes are commonly found in adult mammals, representing ~90% of the entire hepatic pool in rodents. The cellular and molecular mechanisms that regulate polyploidization have been well characterized; however, it is unclear whether diploid and polyploid hepatocytes function similarly in multiple contexts. Answering this question has been challenging because proliferating hepatocytes can increase or decrease ploidy, and animal models with healthy diploid-only livers have not been available. Mice lacking E2f7 and E2f8 in the liver (liver-specific E2f7/E2f8 knockout; LKO) were recently reported to have a polyploidization defect, but were otherwise healthy. Herein, livers from LKO mice were rigorously characterized, demonstrating a 20-fold increase in diploid hepatocytes and maintenance of the diploid state even after extensive proliferation. Livers from LKO mice maintained normal function, but became highly tumorigenic when challenged with tumor-promoting stimuli, suggesting that tumors in LKO mice were driven, at least in part, by diploid hepatocytes capable of rapid proliferation. Indeed, hepatocytes from LKO mice proliferate faster and out-compete control hepatocytes, especially in competitive repopulation studies. In addition, diploid or polyploid hepatocytes from wild-type (WT) mice were examined to eliminate potentially confounding effects associated with E2f7/E2f8 deficiency. WT diploid cells also showed a proliferative advantage, entering and progressing through the cell cycle faster than polyploid cells, both in vitro and during liver regeneration (LR). Diploid and polyploid hepatocytes responded similarly to hepatic mitogens, indicating that proliferation kinetics are unrelated to differential response to growth stimuli. Conclusion: Diploid hepatocytes proliferate faster than polyploids, suggesting that the polyploid state functions as a growth suppressor to restrict proliferation by the majority of hepatocytes.
Topics: Animals; Cell Proliferation; Female; Hepatocytes; Liver Regeneration; Male; Mice; Mice, Inbred C57BL; Polyploidy
PubMed: 30244478
DOI: 10.1002/hep.30286 -
BMC Biology Mar 2021Polyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages. However, how polyploid genomes adapt to the abrupt presence of two...
BACKGROUND
Polyploidy has played a prominent role in the evolution of plants and many other eukaryotic lineages. However, how polyploid genomes adapt to the abrupt presence of two or more sets of chromosomes via genome regulation remains poorly understood. Here, we analyzed genome-wide histone modification and gene expression profiles in relation to domestication and ploidy transition in the A and B subgenomes of polyploid wheat.
RESULTS
We found that epigenetic modification patterns by two typical euchromatin histone markers, H3K4me3 and H3K27me3, for the great majority of homoeologous triad genes in A and B subgenomes were highly conserved between wild and domesticated tetraploid wheats and remained stable in the process of ploidy transitions from hexaploid to extracted tetraploid and then back to resynthesized hexaploid. However, a subset of genes was differentially modified during tetraploid and hexaploid wheat domestication and in response to ploidy transitions, and these genes were enriched for particular gene ontology (GO) terms. The extracted tetraploid wheat manifested higher overall histone modification levels than its hexaploid donor, and which were reversible and restored to normal levels in the resynthesized hexaploid. Further, while H3K4me3 marks were distally distributed along each chromosome and significantly correlated with subgenome expression as expected, H3K27me3 marks showed only a weak distal bias and did not show a significant correlation with gene expression.
CONCLUSIONS
Our results reveal overall high stability of histone modification patterns in the A and B subgenomes of polyploid wheat during domestication and in the process of ploidy transitions. However, modification levels of a subset of functionally relevant genes in the A and B genomes were trans-regulated by the D genome in hexaploid wheat.
Topics: Domestication; Genome, Plant; Histone Code; Polyploidy; Triticum
PubMed: 33750361
DOI: 10.1186/s12915-021-00985-7 -
The New Phytologist May 2013In the plant kingdom, events of whole genome duplication or polyploidization are generally believed to occur via alterations of the sexual reproduction process. Thereby,... (Review)
Review
In the plant kingdom, events of whole genome duplication or polyploidization are generally believed to occur via alterations of the sexual reproduction process. Thereby, diploid pollen and eggs are formed that contain the somatic number of chromosomes rather than the gametophytic number. By participating in fertilization, these so-called 2n gametes generate polyploid offspring and therefore constitute the basis for the establishment of polyploidy in plants. In addition, diplogamete formation, through meiotic restitution, is an essential component of apomixis and also serves as an important mechanism for the restoration of F1 hybrid fertility. Characterization of the cytological mechanisms and molecular factors underlying 2n gamete formation is therefore not only relevant for basic plant biology and evolution, but may also provide valuable cues for agricultural and biotechnological applications (e.g. reverse breeding, clonal seeds). Recent data have provided novel insights into the process of 2n pollen and egg formation and have revealed multiple means to the same end. Here, we summarize the cytological mechanisms and molecular regulatory networks underlying 2n gamete formation, and outline important mitotic and meiotic processes involved in the ectopic induction of sexual polyploidization.
Topics: Biological Evolution; Genes, Plant; Genome, Plant; Germ Cells; Meiosis; Mitosis; Plant Cells; Plants; Pollen; Polyploidy
PubMed: 23421646
DOI: 10.1111/nph.12184 -
International Journal of Molecular... Mar 2022DNA replication during cell proliferation is 'vertical' copying, which reproduces an initial amount of genetic information. Polyploidy, which results from whole-genome... (Review)
Review
DNA replication during cell proliferation is 'vertical' copying, which reproduces an initial amount of genetic information. Polyploidy, which results from whole-genome duplication, is a fundamental complement to vertical copying. Both organismal and cell polyploidy can emerge via premature cell cycle exit or via cell-cell fusion, the latter giving rise to polyploid hybrid organisms and epigenetic hybrids of somatic cells. Polyploidy-related increase in biological plasticity, adaptation, and stress resistance manifests in evolution, development, regeneration, aging, oncogenesis, and cardiovascular diseases. Despite the prevalence in nature and importance for medicine, agri- and aquaculture, biological processes and epigenetic mechanisms underlying these fundamental features largely remain unknown. The evolutionarily conserved features of polyploidy include activation of transcription, response to stress, DNA damage and hypoxia, and induction of programs of morphogenesis, unicellularity, and longevity, suggesting that these common features confer adaptive plasticity, viability, and stress resistance to polyploid cells and organisms. By increasing cell viability, polyploidization can provide survival under stressful conditions where diploid cells cannot survive. However, in somatic cells it occurs at the expense of specific function, thus promoting developmental programming of adult cardiovascular diseases and increasing the risk of cancer. Notably, genes arising via evolutionary polyploidization are heavily involved in cancer and other diseases. Ploidy-related changes of gene expression presumably originate from chromatin modifications and the derepression of bivalent genes. The provided evidence elucidates the role of polyploidy in evolution, development, aging, and carcinogenesis, and may contribute to the development of new strategies for promoting regeneration and preventing cardiovascular diseases and cancer.
Topics: Adaptation, Physiological; Carcinogenesis; Cardiovascular Diseases; Diploidy; Humans; Neoplasms; Polyploidy
PubMed: 35408902
DOI: 10.3390/ijms23073542 -
The New Phytologist Apr 2010Polyploidization and recombination are two important processes driving evolution through the building and reshaping of genomes. Allopolyploids arise from hybridization... (Review)
Review
Polyploidization and recombination are two important processes driving evolution through the building and reshaping of genomes. Allopolyploids arise from hybridization and chromosome doubling among distinct, yet related species. Polyploids may display novel variation relative to their progenitors, and the sources of this variation lie not only in the acquisition of extra gene dosages, but also in the genomic changes that occur after divergent genomes unite. Genomic changes (deletions, duplications, and translocations) have been detected in both recently formed natural polyploids and resynthesized polyploids. In resynthesized Brassica napus allopolyploids, there is evidence that many genetic changes are the consequence of homoeologous recombination. Homoeologous recombination can generate novel gene combinations and phenotypes, but may also destabilize the karyotype and lead to aberrant meiotic behavior and reduced fertility. Thus, natural selection plays a role in the establishment and maintenance of fertile natural allopolyploids that have stabilized chromosome inheritance and a few advantageous chromosomal rearrangements. We discuss the evidence for genome rearrangements that result from homoeologous recombination in resynthesized B. napus and how these observations may inform phenomena such as chromosome replacement, aneuploidy, non-reciprocal translocations and gene conversion seen in other polyploids.
Topics: Brassica napus; Chromosome Pairing; Chromosome Segregation; Models, Genetic; Polyploidy; Recombination, Genetic
PubMed: 20002315
DOI: 10.1111/j.1469-8137.2009.03089.x