Polyploidization: Consequences of genome doubling on the evolutionary potential of populations
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
PubMed
35862788
DOI
10.1002/ajb2.16029
Knihovny.cz E-zdroje
- Klíčová slova
- evolvability, extinction, genetic variation, mating system, whole-genome duplication,
- MeSH
- biologická evoluce * MeSH
- diploidie MeSH
- genom rostlinný MeSH
- polyploidie * MeSH
- rostliny genetika MeSH
- Publikační typ
- časopisecké články MeSH
Whole-genome duplication is common in plants and is considered to have a broad range of effects on individuals' phenotypes and genomes and to be an important driver of plant adaptation and speciation. Despite their increased capacity to cope with challenging environments, polyploid lineages are generally as prone to extinction, and sometimes more prone, than their diploid progenitors. Although several explanations have been proposed to explain the short- and long-term disadvantages of polyploidy on the survival probability of populations, the consequences of whole-genome doubling on the heritable variance remain poorly studied. Whole-genome doubling can have major effects not only on the genetics, but also on the ecology and life history of the populations. Modifications of other properties of populations can reverse the effects of polyploidization per se on heritable variance. In this synthesis, I summarize the empirical and theoretical knowledge about the multifarious consequences of genome doubling on the heritable variance of quantitative traits and on the evolutionary potential of polyploid populations compared to their diploid progenitors. I propose several ways to decipher the consequences of whole-genome doubling on survival probability and to study the further consequences of shifting the ecological niche and life-history traits of a population. I also highlight some practical considerations for comparing the heritable variance of a trait among different cytotypes. Such investigations appear to be timely and necessary to understand more about the paradoxical aspects of polyploidization and to understand the evolutionary potential of polyploid lineages in a global warming context.
Zobrazit více v PubMed
Abu Awad, D., and D. Roze. 2018. Effects of partial selfing on the equilibrium genetic variance, mutation load, and inbreeding depression under stabilizing selection. Evolution 72: 751-769.
Amoros, W., E. Salas, V. Hualla, G. Burgos, B. De Boeck, R. Eyzaguirre, T. zum Felde, and M. Bonierbale. 2020. Heritability and genetic gains for iron and zinc concentration in diploid potato. Crop Science 60: 1884-1896.
Arnold, B. J., B. Lahner, J. M. DaCosta, C. M. Weisman, J. D. Hollister, D. E. Salt, K. Bomblies, and L. Yant. 2016. Borrowed alleles and convergence in serpentine adaptation. Proceedings of the National Academy of Sciences, USA 113: 8320-8325.
Arrigo, N., and M. S. Barker. 2012. Rarely successful polyploids and their legacy in plant genomes. Current Opinion in Plant Biology 15: 140-146.
Baduel, P., S. Bray, M. Vallejo-Marin, F. Kolář, and L. Yant. 2018. The “polyploid hop”: shifting challenges and opportunities over the evolutionary lifespan of genome duplications. Frontiers in Ecology and Evolution 6: 117.
Barringer, B. C. 2007. Polyploidy and self-fertilization in flowering plants. American Journal of Botany 94: 1527-1533.
Bingham, E. T., R. W. Groose, D. R. Woodfield, and K. K. Kidwell. 1994. Complementary gene interactions in alfalfa are greater in autotetraploids than diploids. Crop Science 34: 823-829.
Bomblies, K. 2020. When everything changes at once: finding a new normal after genome duplication. Proceedings of the Royal Society, B, Biological Sciences 287: 20202154.
Brochmann, C., A. K. Brysting, I. G. Alsos, L. Borgen, H. H. Grundt, A.-C. Scheen, and R. Elven. 2004. Polyploidy in arctic plants. Biological Journal of the Linnean Society 82: 521-536.
Bürger, R., G. P. Wagner, and F. Stettinger. 1989. How much heritable variation can be maintained in finite populations by mutation-selection balance? Evolution 43: 1748-1766.
Burgess, K. S., J. R. Etterson, and L. F. Galloway. 2007. Artificial selection shifts flowering phenology and other correlated traits in an autotetraploid herb. Heredity 99: 641-648.
Carter, A. J., J. Hermisson, and T. F. Hansen. 2005. The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theoretical Population Biology 68: 179-196.
Chao, D.-Y., B. Dilkes, H. Luo, A. Douglas, E. Yakubova, B. Lahner, and D. E. Salt. 2013. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341: 658-659.
Charlesworth, D., and B. Charlesworth. 1995. Quantitative genetics in plants: the effect of the breeding system on genetic variability. Evolution 49: 911-920.
Clo, J. 2022. The evolution of the additive variance of a trait under stabilizing selection after autopolyploidization. Journal of Evolutionary Biology 35: 891−897.
Clo, J., L. Gay, and J. Ronfort. 2019. How does selfing affect the genetic variance of quantitative traits? An updated meta-analysis on empirical results in angiosperm species. Evolution 73: 1578-1590.
Clo, J., and F. Kolář. 2021. Short- and long-term consequences of genome doubling: a meta-analysis. American Journal of Botany 108: 2315-2322.
Clo, J., and Ø. H. Opedal. 2021. Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species. Evolution 75: 1920-1935.
Clo, J., N. Padilla-García, and F. Kolář. 2022. Polyploidization as an opportunistic mutation: the role of unreduced gametes formation and genetic drift in polyploid establishment. Journal of Evolutionary Biology, in press. https://doi.org/10.1111/jeb.14055
Clo, J., J. Ronfort, and L. Gay. 2021. Fitness consequences of hybridization in a predominantly selfing species: insights into the role of dominance and epistatic incompatibilities. Heredity 127: 393-400.
Comai, L. 2005. The advantages and disadvantages of being polyploid. Nature Reviews Genetics 6: 836-846.
de Nettancourt, D. 1977. Incompatibility in angiosperms. Springer-Verlag, Berlin, Germany.
Doyle, J. J., and J. E. Coate. 2019. Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. International Journal of Plant Sciences 180: 1-52.
Dubcovsky, J., and J. Dvorak. 2007. Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316: 1862-1866.
Etterson, J. R., S. R. Keller, and L. F. Galloway. 2007. Epistatic and cytonuclear interactions govern outbreeding depression in the autotetraploid Campanulastrum americanum. Evolution 61: 2671-2683.
Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Longman Group, Harlow, UK.
Fawcett, J. A., S. Maere, and Y. Van de Peer. 2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proceedings of the National Academy of Sciences, USA 106: 5737-5742.
Fowler, N. L., and D. A. Levin. 1984. Ecological constraints on the establishment of a novel polyploid in competition with its diploid progenitor. American Naturalist 124: 703-711.
Geber, M. A., and L. R. Griffen. 2003. Inheritance and natural selection on functional traits. International Journal of Plant Sciences 164: S21-S42.
Gemble, S., R. Wardenaar, K. Keuper, N. Srivastava, M. Nano, A.-S. Macé, A. E. Tijhuis, et al. 2022. Genetic instability from a single S phase after whole-genome duplication. Nature 604: 146-151.
Glennon, K. L., M. E. Ritchie, and K. A. Segraves. 2014. Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecology Letters 17: 574-582.
Gregory, T. R., and B. K. Mable. 2005. Polyploidy in animals. In T. R. Gregory [ed.], The evolution of the genome, 427-517. Elsevier, Burlington, MA, USA.
Griswold, C. K., and M. W. Williamson. 2017. A two-locus model of selection in autotetraploids: chromosomal gametic disequilibrium and selection for an adaptive epistatic gene combination. Heredity 119: 314-327.
Haldane, J. B. S. 1927. A mathematical theory of natural and artificial selection, part V: selection and mutation. Mathematical Proceedings of the Cambridge Philosophical Society 23: 838-844.
Hannweg, K., W. Steyn, and I. Bertling. 2016. In vitro-induced tetraploids of Plectranthus esculentus are nematode-tolerant and have enhanced nutritional value. Euphytica 207: 343-351.
Hansen, T. F., C. Pélabon, and D. Houle. 2011. Heritability is not evolvability. Evolutionary Biology 38: 258-277.
Hardie, D. C., and J. A. Hutchings. 2010. Evolutionary ecology at the extremes of species' ranges. Environmental Reviews 18: 1-20.
Hegarty, M., J. Coate, S. Sherman-Broyles, R. Abbott, S. Hiscock, and J. Doyle. 2013. Lessons from natural and artificial polyploids in higher plants. Cytogenetic and Genome Research 140: 204-225.
Hias, N., A. Svara, and J. W. Keulemans. 2018. Effect of polyploidisation on the response of apple (Malus × domestica Borkh.) to Venturia inaequalis infection. European Journal of Plant Pathology 151: 515-526.
Husband, B. C., B. Ozimec, S. L. Martin, and L. Pollock. 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. International Journal of Plant Sciences 169: 195-206.
Johansen-Morris, A. D., and R. G. Latta. 2006. Fitness consequences of hybridization between ecotypes of Avena barbata: hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60: 1585-1595.
Kempthorne, O. 1955. The correlation between relatives in a simple autotetraploid population. Genetics 40: 168.
Kolář, F., M. Čertner, J. Suda, P. Schönswetter, and B. C. Husband. 2017. Mixed-ploidy species: progress and opportunities in polyploid research. Trends in Plant Science 22: 1041-1055.
Lande, R. 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314-334.
Lande, R., and E. Porcher. 2015. Maintenance of quantitative genetic variance under partial self-fertilization, with implications for evolution of selfing. Genetics 200: 891-906.
Layman, N. C., and J. W. Busch. 2018. Bottlenecks and inbreeding depression in autotetraploids. Evolution 72: 2025-2037.
Le Rouzic, A. 2014. Estimating directional epistasis. Frontiers in Genetics 5: 198.
Leebens-Mack, J. H., M. S. Barker, E. J. Carpenter, M. K. Deyholos, M. A. Gitzendanner, S. W. Graham, I. Grosse, et al. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574: 679-685.
Levin, D. A. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35-43.
Levin, D. A. 2019. Why polyploid exceptionalism is not accompanied by reduced extinction rates. Plant Systematics and Evolution 305: 1-11.
Levin, D. A., and D. E. Soltis. 2018. Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude. Current Opinion in Plant Biology 42: 1-7.
Lynch, M., and W. Gabriel. 1983. Phenotypic evolution and parthenogenesis. American Naturalist 122: 745-764.
Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA, USA.
Marburger, S., P. Monnahan, P. J. Seear, S. H. Martin, J. Koch, P. Paajanen, M. Bohutínská, et al. 2019. Interspecific introgression mediates adaptation to whole genome duplication. Nature Communications 10: 1-11.
Martin, S. L., and B. C. Husband. 2012. Whole genome duplication affects evolvability of flowering time in an autotetraploid plant. PLoS One 7: e44784.
Martínez-Padilla, J., A. Estrada, R. Early, and F. García-González. 2017. Evolvability meets biogeography: evolutionary potential decreases at high and low environmental favourability. Proceedings of the Royal Society, B, Biological Sciences 284: 20170516.
Mayrose, I., S. H. Zhan, C. J. Rothfels, N. Arrigo, M. S. Barker, L. H. Rieseberg, and S. P. Otto. 2015. Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis et al. (2014). New Phytologist 206: 27-35.
Mayrose, I., S. H. Zhan, C. J. Rothfels, K. Magnuson-Ford, M. S. Barker, L. H. Rieseberg, and S. P. Otto. 2011. " Recently formed polyploid plants diversify at lower rates." Science 333: 1257.
Mittelbach, G. G., D. W. Schemske, H. V. Cornell, A. P. Allen, J. M. Brown, M. B. Bush, S. P. Harrison, et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters 10: 315-331.
Monnahan, P. J., and J. K. Kelly. 2015. Epistasis is a major determinant of the additive genetic variance in Mimulus guttatus. PLoS Genetics 11: e1005201.
Mostafaee, N., and C. K. Griswold. 2019. Two-locus local adaptation by additive or epistatic gene combinations in autotetraploids versus diploids. Journal of Heredity 110: 866-879.
Neiman, M., and T. A. Linksvayer. 2006. The conversion of variance and the evolutionary potential of restricted recombination. Heredity 96: 111-121.
Novikova, P. Y., I. G. Brennan, W. Booker, M. Mahony, P. Doughty, A. R. Lemmon, E. Moriarty Lemmon, et al. 2020. Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus. PLoS Genetics 16: e1008769.
Oakley, C. G., J. A. Agren, and D. W. Schemske. 2015. Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana. Heredity 115: 73-82.
O'Neil, P. 1997. Natural selection on genetically correlated phenological characters in Lythrum salicaria L. (Lythraceae). Evolution 51: 267-274.
Opedal, Ø. H., G. H. Bolstad, T. F. Hansen, W. S. Armbruster, and C. Pélabon. 2017. The evolvability of herkogamy: quantifying the evolutionary potential of a composite trait. Evolution 71: 1572-1586.
Ortiz, R., and A. M. Golmirzaie. 2003. Genetic parameters for agronomic characteristics. II. Intermediate and advanced stages in a true potato seed breeding population. Hereditas 139: 217-222.
Otto, S. P. 2007. The evolutionary consequences of polyploidy. Cell 131: 452-462.
Otto, S. P., and J. Whitton. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437.
Pandit, M. K., M. J. Pocock, and W. E. Kunin. 2011. Ploidy influences rarity and invasiveness in plants. Journal of Ecology 99: 1108-1115.
Pélabon, C., C. H. Hilde, S. Einum, and M. Gamelon. 2020. On the use of the coefficient of variation to quantify and compare trait variation. Evolution letters 4: 180-188.
Pennington, L. K., R. A. Slatyer, D. V. Ruiz-Ramos, S. D. Veloz, and J. P. Sexton. 2021. How is adaptive potential distributed within species ranges? Evolution 75: 2152-2166.
Pironon, S., G. Papuga, J. Villellas, A. L. Angert, M. B. García, and J. D. Thompson. 2017. Geographic variation in genetic and demographic performance: new insights from an old biogeographical paradigm. Biological Reviews 92: 1877-1909.
Porturas, L. D., T. J. Anneberg, A. E. Curé, S. Wang, D. M. Althoff, and K. A. Segraves. 2019. A meta-analysis of whole genome duplication and the effects on flowering traits in plants. American journal of botany 106: 469-476.
Pujol, B., and J. R. Pannell. 2008. " Reduced responses to selection after species range expansion." Science 321: 96.
Ramsey, J., and D. W. Schemske. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467-501.
Rausch, J. H., and M. T. Morgan. 2005. The effect of self-fertilization, inbreeding depression, and population size on autopolyploid establishment. Evolution 59: 1867-1875.
Rice, A., P. Šmarda, M. Novosolov, M. Drori, L. Glick, N. Sabath, S. Meiri, et al. 2019. The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265-273.
Robertson, K., E. E. Goldberg, and B. Igić. 2011. Comparative evidence for the correlated evolution of polyploidy and self-compatibility in Solanaceae. Evolution 65: 139-155.
Rojas-Andrés, B. M., N. Padilla-García, M. de Pedro, N. López-González, L. Delgado, D. C. Albach, M. Castro, et al. 2020. Environmental differences are correlated with the distribution pattern of cytotypes in Veronica subsection Pentasepalae at a broad scale. Annals of Botany 125: 471-484.
Ronfort, J. 1999. The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genetics Research 74: 31-42.
Rowe, D. E. 1982. Effect of gametic disequilibrium on selection in an autotetraploid population. Theoretical and Applied Genetics 64: 69-74.
Rowe, D. E., and R. R. Hill. 1984. Effect of gametic disequilibrium on means and on genetic variances of autotetraploid synthetic varieties. Theoretical and Applied Genetics 68: 69-74.
Ruiz, M., A. Quiñones, M.-R. Martínez-Cuenca, P. Aleza, R. Morillon, L. Navarro, E. Primo-Millo, and B. Martínez-Alcántara. 2016. Tetraploidy enhances the ability to exclude chloride from leaves in carrizo citrange seedlings. Journal of Plant Physiology 205: 1-10.
Schmickl, R., and L. Yant. 2021. Adaptive introgression: how polyploidy reshapes gene flow landscapes. New Phytologist 230: 457-461.
Sexton, J. P., P. J. McIntyre, A. L. Angert, and K. J. Rice. 2009. Evolution and ecology of species range limits. Annual Review of Ecology, Evolution, and Systematics 40: 415-436.
Slater, A. T., G. M. Wilson, N. O. Cogan, J. W. Forster, and B. J. Hayes. 2014. Improving the analysis of low heritability complex traits for enhanced genetic gain in potato. Theoretical and Applied Genetics 127: 809-820.
Soltis, D. E., M. C. Segovia-Salcedo, I. Jordon-Thaden, L. Majure, N. M. Miles, E. V. Mavrodiev, W. Mei, et al. 2014a. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytologist 202: 1105-1117.
Soltis, D. E., C. J. Visger, and P. S. Soltis. 2014b. The polyploidy revolution then… and now: Stebbins revisited. American Journal of Botany 101: 1057-1078.
Soltis, P. S., X. Liu, D. B. Marchant, C. J. Visger, and D. E. Soltis. 2014c. Polyploidy and novelty: Gottlieb's legacy. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 369: 20130351.
Stebbins, G. L. 1971. Processes of organic evolution. Prentice-Hall, Englewood Cliffs, NJ, USA.
Tate, J. A., V. V. Symonds, A. N. Doust, R. J. Buggs, E. Mavrodiev, L. C. Majure, P. S. Soltis, and D. E. Soltis. 2009. Synthetic polyploids of Tragopogon miscellus and T. mirus (Asteraceae): 60 years after Ownbey's discovery. American Journal of Botany 96: 979-988.
Te Beest, M., J. J. Le Roux, D. M. Richardson, A. K. Brysting, J. Suda, M. Kubešová, and P. Pyšek. 2012. The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109: 19-45.
Vamosi, J. C., S. J. Goring, B. F. Kennedy, R. J. Mayberry, C. M. Moray, L. A. Neame, N. D. Tunbridge, and E. Elle. 2007. Pollination, floral display, and the ecological correlates of polyploidy. Functional Ecosystems and Communities 1: 1-9.
Van de Peer, Y., T.-L. Ashman, P. S. Soltis, and D. E. Soltis. 2021. Polyploidy: an evolutionary and ecological force in stressful times. Plant Cell 33: 11-26.
Van de Peer, Y., E. Mizrachi, and K. Marchal. 2017. The evolutionary significance of polyploidy. Nature Reviews Genetics 18: 411.
Van Drunen, W. E., and B. C. Husband. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytologist 224: 1266-1277.
Vanneste, K., G. Baele, S. Maere, and Y. Van de Peer. 2014a. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Research 24: 1334-1347.
Vanneste, K., S. Maere, and Y. Van de Peer. 2014b. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philosophical Transactions of the Royal Society, B, Biological Sciences 369: 20130353.
Walsh, B. 2005. The struggle to exploit non-additive variation. Australian Journal of Agricultural Research 56: 873-881.
Walsh, B., and M. Lynch. 2018. Evolution and selection of quantitative traits. Oxford University Press, Oxford, UK.
Wang, W., Y. He, Z. Cao, and Z. Deng. 2018. Induction of tetraploids in impatiens (Impatiens walleriana) and characterization of their changes in morphology and resistance to downy mildew. HortScience 53: 925-931.
Wolak, M. E., and L. F. Keller. 2014. Dominance genetic variance and inbreeding in natural populations. In A. Charmantier, D. Garant, and L. E. B. Kruuk [eds.], Quantitative genetics in the wild, 104-127. Oxford Scholarship Online. Oxford University Press, Oxford, UK.
Wood, J. L., M. C. Yates, and D. J. Fraser. 2016. Are heritability and selection related to population size in nature? Meta-analysis and conservation implications. Evolutionary Applications 9: 640-657.
Wright, S. 1938. The distribution of gene frequencies in populations of polyploids. Proceedings of the National Academy of Sciences, USA 24: 372.
Xue, L., H. Dai, and J. Lei. 2015. Creating high polyploidy pink-flowered strawberries with improved cold tolerance. Euphytica 206: 417-426.