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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 -
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 Journal of Pathology Oct 2023Therapeutic resistance is a notable cause of death in patients with ovarian carcinoma. Polyploid giant cancer cells (PGCCs), commonly arising in tumor tissues following...
Therapeutic resistance is a notable cause of death in patients with ovarian carcinoma. Polyploid giant cancer cells (PGCCs), commonly arising in tumor tissues following chemotherapy, have recently been considered to contribute to drug resistance. As a type III deacetylase, Sirtuin1 (SIRT1) plays essential roles in the cell cycle, cellular senescence, and drug resistance. Accumulating evidence has suggested that alteration in its subcellular localization via nucleocytoplasmic shuttling is a critical process influencing the functions of SIRT1. However, the roles of SIRT1 subcellular localization in PGCC formation and subsequent senescence escape remain unclear. In this study, we compared the differences in the polyploid cell population and senescence state of PGCCs following paclitaxel treatment between tumor cells overexpressing wild-type SIRT1 (WT SIRT1) and those expressing nuclear localization sequence (NLS)-mutated SIRT1 (SIRT1 ). We investigated the involvement of cytoplasmic SIRT1 in biological processes and signaling pathways, including the cell cycle and cellular senescence, in ovarian carcinoma cells' response to paclitaxel treatment. We found that the SIRT1 tumor cell population contained more polyploid cells and fewer senescent PGCCs than the SIRT1-overexpressing tumor cell population. Comparative proteomic analyses using co-immunoprecipitation (Co-IP) combined with liquid chromatography-mass spectrometry (LC-MS)/MS showed the differences in the differentially expressed proteins related to PGCC formation, cell growth, and death, including CDK1 and CDK2, between SIRT1 and SIRT1 cells or PGCCs. Our results suggested that ovarian carcinoma cells utilize polyploidy formation as a survival mechanism during exposure to paclitaxel-based treatment via the effect of cytoplasmic SIRT1 on PGCC formation and survival, thereby boosting paclitaxel resistance. © 2023 The Pathological Society of Great Britain and Ireland.
Topics: Female; Humans; Paclitaxel; Sirtuin 1; Proteomics; Cell Line, Tumor; Ovarian Neoplasms; Carcinoma, Ovarian Epithelial; Polyploidy
PubMed: 37565313
DOI: 10.1002/path.6167 -
Frontiers in Plant Science 2023
PubMed: 38146271
DOI: 10.3389/fpls.2023.1340455 -
Emerging Topics in Life Sciences Dec 2023Biocultural diversity is the ever-evolving and irreplaceable sum total of all living organisms inhabiting the Earth. It plays a significant role in sustainable...
Biocultural diversity is the ever-evolving and irreplaceable sum total of all living organisms inhabiting the Earth. It plays a significant role in sustainable productivity and ecosystem services that benefit humanity and is closely allied with human cultural diversity. Despite its essentiality, biodiversity is seriously threatened by the insatiable and inequitable human exploitation of the Earth's resources. One of the benefits of biodiversity is its utilization in crop improvement, including cropping improvement (agronomic cultivation practices) and genetic improvement (plant breeding). Crop improvement has tended to decrease agricultural biodiversity since the origins of agriculture, but awareness of this situation can reverse this negative trend. Cropping improvement can strive to use more diverse cultivars and a broader complement of crops on farms and in landscapes. It can also focus on underutilized crops, including legumes. Genetic improvement can access a broader range of biodiversity sources and, with the assistance of modern breeding tools like genomics, can facilitate the introduction of additional characteristics that improve yield, mitigate environmental stresses, and restore, at least partially, lost crop biodiversity. The current legal framework covering biodiversity includes national intellectual property and international treaty instruments, which have tended to limit access and innovation to biodiversity. A global system of access and benefit sharing, encompassing digital sequence information, would benefit humanity but remains an elusive goal. The Kunming-Montréal Global Biodiversity Framework sets forth an ambitious set of targets and goals to be accomplished by 2030 and 2050, respectively, to protect and restore biocultural diversity, including agrobiodiversity.
PubMed: 38084755
DOI: 10.1042/ETLS20230067 -
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 -
Cell Reports Dec 2023The carcinogenesis and progression of hepatocellular carcinoma (HCC) are closely related to viral infection and intestinal bacteria. However, little is known about...
The carcinogenesis and progression of hepatocellular carcinoma (HCC) are closely related to viral infection and intestinal bacteria. However, little is known about bacteria within the HCC tumor microenvironment. Here, we showed that intratumoral Mycoplasma hyorhinis (M. hyorhinis) promoted the initiation and progression of HCC by enhancing nuclear ploidy. We quantified M. hyorhinis in clinical tissue specimens of HCC and observed that patients with high M. hyorhinis load had poor prognosis. We found that gastrointestinal M. hyorhinis can retrogradely infect the liver through the oral-duodenal-hepatopancreatic ampulla route. We further found that the increases in mononuclear polyploidy and cancer stemness resulted from mitochondrial fission caused by intracellular M. hyorhinis. Mechanistically, M. hyorhinis infection promoted the decay of mitochondrial fusion protein (MFN) 1 mRNA in an m6A-dependent manner. Our findings indicated that M. hyorhinis infection promoted pathological polyploidization and suggested that Mycoplasma clearance with antibiotics or regulating mitochondrial dynamics might have the potential for HCC therapy.
Topics: Humans; Mycoplasma; Carcinoma, Hepatocellular; Liver Neoplasms; Mycoplasma hyorhinis; Mycoplasma Infections; Tumor Microenvironment
PubMed: 38088929
DOI: 10.1016/j.celrep.2023.113563 -
Cells Aug 2023Salinity stress affects plant growth and development by causing osmotic stress and nutrient imbalances through excess Na, K, and Cl ion accumulations that induce toxic... (Review)
Review
Salinity stress affects plant growth and development by causing osmotic stress and nutrient imbalances through excess Na, K, and Cl ion accumulations that induce toxic effects during germination, seedling development, vegetative growth, flowering, and fruit set. However, the effects of salt stress on growth and development processes, especially in polyploidized leguminous plants, remain unexplored and scantly reported compared to their diploid counterparts. This paper discusses the physiological and molecular response of legumes towards salinity stress-based osmotic and ionic imbalances in plant cells. A multigenic response involving various compatible solutes, osmolytes, ROS, polyamines, and antioxidant activity, together with genes encoding proteins involved in the signal transduction, regulation, and response mechanisms to this stress, were identified and discussed. This discussion reaffirms polyploidization as the driving force in plant evolution and adaptation to environmental stress constraints such as drought, feverish temperatures, and, in particular, salt stress. As a result, thorough physiological and molecular elucidation of the role of gene duplication through induced autopolyploidization and possible mechanisms regulating salinity stress tolerance in grain legumes must be further studied.
Topics: Fabaceae; Mutagens; Salt Tolerance; Salt Stress; Crops, Agricultural
PubMed: 37626892
DOI: 10.3390/cells12162082 -
International Journal of Molecular... Jul 2023Endoreplication-a process that is common in plants and also accompanies changes in the development of animal organisms-has been seen from a new perspective in recent... (Review)
Review
Endoreplication-a process that is common in plants and also accompanies changes in the development of animal organisms-has been seen from a new perspective in recent years. In the paper, we not only shed light on this view, but we would also like to promote an understanding of the application potential of this phenomenon in plant cultivation. Endoreplication is a pathway for cell development, slightly different from the classical somatic cell cycle, which ends with mitosis. Since many rounds of DNA synthesis take place within its course, endoreplication is a kind of evolutionary compensation for the relatively small amount of genetic material that plants possess. It allows for its multiplication and active use through transcription and translation. The presence of endoreplication in plants has many positive consequences. In this case, repeatedly produced copies of genes, through the corresponding transcripts, help the plant acquire the favorable properties for which proteins are responsible directly or indirectly. These include features that are desirable in terms of cultivation and marketing: a greater saturation of fruit and flower colors, a stronger aroma, a sweeter fruit taste, an accumulation of nutrients, an increased resistance to biotic and abiotic stress, superior tolerance to adverse environmental conditions, and faster organ growth (and consequently the faster growth of the whole plant and its biomass). The two last features are related to the nuclear-cytoplasmic ratio-the greater the content of DNA in the nucleus, the higher the volume of cytoplasm, and thus the larger the cell size. Endoreplication not only allows cells to reach larger sizes but also to save the materials used to build organelles, which are then passed on to daughter cells after division, thus ending the classic cell cycle. However, the content of genetic material in the cell nucleus determines the number of corresponding organelles. The article also draws attention to the potential practical applications of the phenomenon and the factors currently limiting its use.
Topics: Animals; Endoreduplication; DNA Replication; Cell Cycle; Mitosis; DNA; Plants
PubMed: 37511616
DOI: 10.3390/ijms241411859 -
Journal of Hepatology Apr 2024Polyploidy in hepatocytes has been proposed as a genetic mechanism to buffer against transcriptional dysregulation. Here, we aim to demonstrate the role of polyploidy in...
BACKGROUND & AIMS
Polyploidy in hepatocytes has been proposed as a genetic mechanism to buffer against transcriptional dysregulation. Here, we aim to demonstrate the role of polyploidy in modulating gene regulatory networks in hepatocytes during ageing.
METHODS
We performed single-nucleus RNA sequencing in hepatocyte nuclei of different ploidy levels isolated from young and old wild-type mice. Changes in the gene expression and regulatory network were compared to three independent strains that were haploinsufficient for HNF4A, CEBPA or CTCF, representing non-deleterious perturbations. Phenotypic characteristics of the liver section were additionally evaluated histologically, whereas the genomic allele composition of hepatocytes was analysed by BaseScope.
RESULTS
We observed that ageing in wild-type mice results in nuclei polyploidy and a marked increase in steatosis. Haploinsufficiency of liver-specific master regulators (HFN4A or CEBPA) results in the enrichment of hepatocytes with tetraploid nuclei at a young age, affecting the genomic regulatory network, and dramatically suppressing ageing-related steatosis tissue wide. Notably, these phenotypes are not the result of subtle disruption to liver-specific transcriptional networks, since haploinsufficiency in the CTCF insulator protein resulted in the same phenotype. Further quantification of genotypes of tetraploid hepatocytes in young and old HFN4A-haploinsufficient mice revealed that during ageing, tetraploid hepatocytes lead to the selection of wild-type alleles, restoring non-deleterious genetic perturbations.
CONCLUSIONS
Our results suggest a model whereby polyploidisation leads to fundamentally different cell states. Polyploid conversion enables pleiotropic buffering against age-related decline via non-random allelic segregation to restore a wild-type genome.
IMPACT AND IMPLICATIONS
The functional role of hepatocyte polyploidisation during ageing is poorly understood. Using single-nucleus RNA sequencing and BaseScope approaches, we have studied ploidy dynamics during ageing in murine livers with non-deleterious genetic perturbations. We have identified that hepatocytes present different cellular states and the ability to buffer ageing-associated dysfunctions. Tetraploid nuclei exhibit robust transcriptional networks and are better adapted to genomically overcome perturbations. Novel therapeutic interventions aimed at attenuating age-related changes in tissue function could be exploited by manipulation of ploidy dynamics during chronic liver conditions.
PubMed: 38583492
DOI: 10.1016/j.jhep.2024.03.043