Inconsistent expression of the gigas effect in polyploid Oxalis
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
PubMed
36193941
DOI
10.1002/ajb2.16077
Knihovny.cz E-zdroje
- Klíčová slova
- Oxalidaceae, Oxalis, bulbils, gigas effect, polyploidy, weediness,
- MeSH
- diploidie MeSH
- Oxalidaceae * MeSH
- ploidie MeSH
- polyploidie MeSH
- rozmnožování MeSH
- Publikační typ
- časopisecké články MeSH
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.
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Adams, K. L., and J. F. Wendel. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135-141.
Ainouche, M. L., and E. Jenczewski. 2010. Focus on polyploidy. New Phytologist 186: 1-4.
Alexander, M. P. 1969. Differential staining of aborted and nonaborted pollen. Stain Technology 44: 117-122.
Alix, K., P. R. Gérard, T. Schwarzacher, and J. S. Heslop-Harrison. 2017. Polyploidy and interspecific hybridization: Partners for adaptation, speciation and evolution in plants. Annals of Botany 120: 183-194.
Arnold, B., S. Kim, and K. Bomblies. 2015. Single geographic origin of a widespread autotetraploid Arabidopsis arenosa lineage followed by interploidy admixture. Molecular Biology and Evolution 32: 1382-1395.
Arrigo, N., and M. Barker. 2012. Rarely successful polyploids and their legacy in plant genomes. Current Opinion in Plant Biology 15: 140-146.
Arvanitis, L., C. Wiklund, Z. Münzbergova, J. Dahlgren, and J. Ehrlén. 2010. Novel antagonistic interactions associated with plant polyploidization influence trait selection and habitat preference. Ecology Letters 13: 330-337.
Baack, E. 2005. To succeed globally, disperse locally: Effects of local pollen and seed dispersal on tetraploid establishment. Heredity 94: 538-546.
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: Art. 117.
Baker, R., Y. Yarkhunova, K. Vidal, B. Ewers, and C. Weinig. 2017. Polyploidy and the relationship between leaf structure and function: Implications for correlated evolution of anatomy, morphology, and physiology in Brassica. BMC Plant Biology 17: Article 3.
Balao, F., J. Herrera, and S. Talavera. 2011. Phenotypic consequences of polyploidy and genome size at the microevolutionary scale: A multivariate morphological approach. New Phytologist 192: 256-265.
Baniaga, A., H. Marx, N. Arrigo, and M. Barker. 2019. Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives. Ecology Letters 23: 68-78.
Barrett, S. C. H. 1992. Heterostylous genetic polymorphisms: Model systems for evolutionary analysis. In S. C. H. Barrett [ed.], Evolution and function of heterostyly, 1-29. Springer, Berlin, Germany.
Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274-284.
Barrett, S. C. H. 2019. ‘A most complex marriage arrangement’: Recent advances on heterostyly and unresolved questions. New Phytologist 224: 1051-1067.
Barringer, B. 2007. Polyploidy and self-fertilization in flowering plants. American Journal of Botany 94: 1527-1533.
Bates, D., M. Mächler, B. Bolker, and S. Walker. 2014. Fitting linear mixed-effects models using lme4. ArXiv. Website: https://doi.org/10.48550/arXiv.1406.5823 [Preprint].
Becker, F. W., K. C. Oberlander, P. Trávníček, and L. L. Dreyer. 2022. Inconsistent expression of the gigas effect in polyploid Oxalis. Zenodo. https://zenodo.org/record/7034366#.Y0wLo1LMKIY
Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, B, Methodological 57: 289-300.
Boalt, E., L. Arvanitis, K. Lehtilä, and J. Ehrlén. 2010. The association among herbivory tolerance, ploidy level, and herbivory pressure in cardamine pratensis. Evolutionary Ecology 24: 1101-1113.
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.
Butterfass, T. 1987. Cell volume ratios of natural and of induced tetraploid and diploid flowering plants. Cytologia 52: 309-316.
Carta, A., and L. Peruzzi. 2015. Testing the large genome constraint hypothesis: Plant traits, habitat and climate seasonality in Liliaceae. New Phytologist 210: 709-716.
Castro, S., M. Castro, V. Ferrero, J. Costa, D. Tavares, L. Navarro, and J. Loureiro. 2016. Invasion fosters change: Independent evolutionary shifts in reproductive traits after Oxalis pes-caprae L. introduction. Frontiers in Plant Science 7: 874.
Castro, S., V. Ferrero, J. Costa, A. Sousa, M. Castro, L. Navarro, and J. Loureiro. 2013. Reproductive strategy of the invasive Oxalis pes-caprae: Distribution patterns of floral morphs, ploidy levels and sexual reproduction. Biological Invasions 15: 1863-1875.
Castro, S., J. Loureiro, C. Santos, M. Ater, G. Ayensa, and L. Navarro. 2007. Distribution of flower morphs, ploidy level and sexual reproduction of the invasive weed Oxalis pes-caprae in the western area of the Mediterranean region. Annals of Botany 99: 507-517.
Čertner, M., E. Fenclová, P. Kúr, F. Kolář, P. Koutecký, A. Krahulcová, and J. Suda. 2017. Evolutionary dynamics of mixed-ploidy populations in an annual herb: Dispersal, local persistence and recurrent origins of polyploids. Annals of Botany 120: 303-315.
Chapman, M., and R. Abbott. 2009. Introgression of fitness genes across a ploidy barrier. New Phytologist 186: 63-71.
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., 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 35: 1099-1109.
Coate, J., A. Luciano, V. Seralathan, K. Minchew, T. Owens, and J. Doyle. 2012a. Anatomical, biochemical, and photosynthetic responses to recent allopolyploidy in Glycine dolichocarpa (Fabaceae). American Journal of Botany 99: 55-67.
Coate, J., A. Powell, T. Owens, and J. Doyle. 2012b. Transgressive physiological and transcriptomic responses to light stress in allopolyploid Glycine dolichocarpa (Leguminosae). Heredity 110: 160-170.
Coyne, J., and H. Orr. 2004. Speciation. Sinauer, Sunderland, Massachusetts, USA.
Cuevas, J., A. Marticorena, and L. Cavieres. 2004. New additions to the introduced flora of the Juan Fernández Islands: Origin, distribution, life history traits, and potential of invasion. Revista Chilena de Historia Natural 77: 523-538.
Cui, L., P. Wall, J. Leebens-Mack, B. Lindsay, D. Soltis, J. Doyle, and P. Soltis et al. 2006. Widespread genome duplications throughout the history of flowering plants. Genome Research 16: 738-749.
De Azkue, D. 2000. Chromosome diversity of South American Oxalis (Oxalidaceae). Botanical Journal of the Linnean Society, Linnean Society of London 132: 143-152.
Dolezel, E., E. Greilhuber, and J. Suda. 2007. Flow cytometry with plant cells: analysis of genes, chromosomes and genomes. Wiley, New York, New York, USA.
Doležel, J., M. Doleželová, and F. J. Novák. 1994. Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata and M. balbisiana). Biologia Plantarum 36: Article 351.
Duchoslav, M., L. Šafářová, and F. Krahulec. 2010. Complex distribution patterns, ecology and coexistence of ploidy levels of Allium oleraceum (Alliaceae) in the Czech Republic. Annals of Botany 105: 719-735.
Emshwiller, E. 2002. Ploidy levels among species in the ‘Oxalis tuberosa alliance’ as inferred by flow cytometry. Annals of Botany 89: 741-753.
Emshwiller, E., T. Theim, A. Grau, V. Nina, and F. Terrazas. 2009. Origins of domestication and polyploidy in oca (Oxalis tuberosa; Oxalidaceae). 3. AFLP data of oca and four wild, tuber-bearing taxa. American Journal of Botany 96: 1839-1848.
Felber, F. 1991. Establishment of a tetraploid cytotype in a diploid population: Effect of relative fitness of the cytotypes. Journal of Evolutionary Biology 4: 195-207.
Fowler, N., and D. Levin. 1984. Ecological constraints on the establishment of a novel polyploid in competition with its diploid progenitor. American Naturalist 124: 703-711.
Fowler, N., and D. Levin. 2016. Critical factors in the establishment of allopolyploids. American Journal of Botany 103: 1236-1251.
Gates, R. R. 1909. The stature and chromosomes of Oenothera gigas, De Vries. Zeitschrift für Induktive Abstammungs- und Vererbungslehre 3: 220.
Glennon, K., M. Ritchie, and K. Segraves. 2014. Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecology Letters 17: 574-582.
Harbert, R., A. Brown, and J. Doyle. 2014. Climate niche modelling in the perennial Glycine (Leguminosae) allopolyploid complex. American Journal of Botany 101: 710-721.
Haukka, A., L. Dreyer, and K. Esler. 2013. Effect of soil type and climatic conditions on the growth and flowering phenology of three Oxalis species in the Western Cape, South Africa. South African Journal of Botany 88: 152-163.
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.
Herben, T., J. Suda, J. Klimešová, S. Mihulka, P. Říha, and I. Šímová. 2012. Ecological effects of cell-level processes: Genome size, functional traits and regional abundance of herbaceous plant species. Annals of Botany 110: 1357-1367.
Hülber, K., M. Sonnleitner, J. Suda, J. Krejčíková, P. Schönswetter, G. Schneeweiss, and M. Winkler. 2015. Ecological differentiation, lack of hybrids involving diploids, and asymmetric gene flow between polyploids in narrow contact zones of Senecio carniolicus (syn. Jacobaea carniolica, Asteraceae). Ecology and Evolution 5: 1224-1234.
Husband, B., S. Baldwin, and H. Sabara. 2016. Direct vs. indirect effects of whole-genome duplication on prezygotic isolation in Chamerion angustifolium: Implications for rapid speciation. American Journal of Botany 103: 1259-1271.
Husband, B., B. Ozimec, S. Martin, and L. Pollock. 2008. Mating consequences of colyploid evolution in flowering plants: Current trends and insights from synthetic polyploids. International Journal of Plant Sciences 169: 195-206.
Husband, B., and H. Sabara. 2004. Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). New Phytologist 161: 703-713.
Jiao, Y., J. Leebens-Mack, S. Ayyampalayam, J. Bowers, M. McKain, J. McNeal, and M. Rolf et al. 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biology 13: Article R3.
Jiao, Y., N. Wickett, S. Ayyampalayam, A. Chanderbali, L. Landherr, P. Ralph, and L. Tomsho et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97-100.
Jooste, M., L. Dreyer, and K. Oberlander. 2016. The phylogenetic significance of leaf anatomical traits of southern African Oxalis. BMC Evolutionary Biology 16: 1-19.
Kao, R. 2007. Asexuality and the coexistence of cytotypes. New Phytologist 175: 764-772.
Knight, C., and J. Beaulieu. 2008. Genome size scaling through phenotype space. Annals of Botany 101: 759-766.
Knight, C., R. Clancy, L. Götzenberger, L. Dann, and J. Beaulieu. 2010. On the relationship between pollen size and genome size. Journal of Botany 2010: 1-7.
Knight, C., N. Molinari, and D. Petrov. 2005. The large genome constraint hypothesis: Evolution, ecology and phenotype. Annals of Botany 95: 177-190.
Krejčíková, J., R. Sudová, M. Lučanová, P. Trávníček, T. Urfus, P. Vít, and H. Weiss-Schneeweiss et al. 2013a. High ploidy diversity and distinct patterns of cytotype distribution in a widespread species of Oxalis in the Greater Cape Floristic Region. Annals of Botany 111: 641-649.
Krejčíková, J., R. Sudová, K. Oberlander, L. Dreyer, and J. Suda. 2012. Cytogeography of Oxalis pes-caprae in its native range: Where are the pentaploids? Biological Invasions 15: 1189-1194.
Krejčíková, J., R. Sudová, K. Oberlander, L. Dreyer, and J. Suda. 2013b. The spatio-ecological segregation of different cytotypes of Oxalis obtusa (Oxalidaceae) in contact zones. South African Journal of Botany 88: 62-68.
Kuznetsova, A., P. Brockhoff, and R. Christensen. 2017. lmerTest Package: Tests in linear mixed effects models. Journal of Statistical Software 82: 1-26.
Lavania, U. 2020. Plant speciation and polyploidy: In habitat divergence and environmental perspective. Nucleus 63: 1-5.
Levin, D. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35-43.
Levin, D. 1983. Polyploidy and novelty in flowering plants. American Naturalist 122: 1-25.
Levin, D. 2002. The role of chromosomal change in plant evolution. Oxford University Press, New York, New York, USA.
Levin, D. 2011. Polyploidy and ecological transfiguration in Achillea. Proceedings of the National Academy of Sciences, USA 108: 6697-6698.
Lockwood, J., P. Cassey, and T. Blackburn. 2009. The more you introduce the more you get: The role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15: 904-910.
Lourteig, A. 1974. Oxalidaceae extra-austroamericanae. I. Oxalis L. Sectio Thamnoxys Planchon. Phytologia 29: 449-471.
Lourteig, A. 2000. Oxalis L. subgéneros Monoxalis (Small) Lourt., Oxalis y Trifidus Lourt. Bradea 7: 201-371.
Luo, S., D. Zhang, and S. Renner. 2006. Oxalis debilis in China: Distribution of flower morphs, sterile pollen and polyploidy. Annals of Botany 98: 459-464.
Lutz, A. 1907. A preliminary note on the chromosomes of Oenothera lamarckiana and one of its mutants, O. gigas. Science 26: 151-152.
Manning, J., and P. Goldblatt. 2012. Plants of the greater cape floristic region. 1: The Core Cape flora. South African National Biodiversity Institute, Pretoria, South Africa.
Marchant, B., D. Soltis, and P. Soltis. 2016. Patterns of abiotic niche shifts in allopolyploids relative to their progenitors. New Phytologist 212: 708-718.
Martin, S., and B. Husband. 2009. Influence of phylogeny and ploidy on species ranges of North American angiosperms. Journal of Ecology 97: 913-922.
Martin, S., and B. Husband. 2013. Adaptation of diploid and tetraploid Chamerion angustifolium to elevation but not local environment. Evolution 67: 1780-1791.
Mayrose, I., S. Zhan, C. Rothfels, K. Magnuson-Ford, M. Barker, L. Rieseberg, and S. Otto. 2011. Recently formed polyploid plants diversify at lower rates. Science 333: 1257.
McIntyre, P. 2012. Polyploidy associated with altered and broader ecological niches in the Claytonia perfoliata (Portulacaceae) species complex. American Journal of Botany 99: 655-662.
Müntzing, A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21: 363-378.
Ning, G., X. Shi, H. Hu, Y. Yan, and M. Bao. 2009. Development of a range of polyploid lines in Petunia hybrida and the relationship of ploidy with the single-/double-flower trait. HortScience 44: 250-255.
Oberlander, K., L. Dreyer, P. Goldblatt, J. Suda, and H. Linder. 2016. Species-rich and polyploid-poor: Insights into the evolutionary role of whole-genome duplication from the Cape flora biodiversity hotspot. American Journal of Botany 103: 1336-1347.
Ornduff, R. 1972. The breakdown of trimorphic incompatibility in Oxalis section Corniculatae. Evolution 26: 52-65.
Oswald, B., and S. Nuismer. 2007. Neopolyploidy and pathogen resistance. Proceedings of the Royal Society, B, Biological Sciences 274: 2393-2397.
Oswald, B., and S. Nuismer. 2011. Neopolyploidy and diversification in Heuchera grossulariifolia. Evolution 65: 1667-1679.
Otto, S., and J. Whitton. 2000. Polyploid incidence and evolution. Annual Review of Genetics 34: 401-437.
Pandit, M., M. Pocock, and W. Kunin. 2011. Ploidy influences rarity and invasiveness in plants. Journal of Ecology 99: 1108-1115.
Pandit, M., H. Tan, and M. Bisht. 2006. Polyploidy in invasive plant species of Singapore. Botanical Journal of the Linnean Society, Linnean Society of London 151: 395-403.
Paynter, M. 1968. Review of “Towards a new relationship of man and nature in temperate lands”. Town Planning Review 39: 168-172.
Porturas, L., T. Anneberg, A. Curé, S. Wang, D. Althoff, and K. Segraves. 2019. A meta-analysis of whole genome duplication and the effects on flowering traits in plants. American Journal of Botany 106: 469-476.
R Core Team. 2021. Version 1.4.17. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Website: http://www.R-project.org
Ramsey, J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proceedings of the National Academy of Sciences, USA 108: 7096-7101.
Ramsey, J., and T. Ramsey. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society, B, Biological Sciences 369: 20130352.
Randall, R., and Cooperative Research Centre for Australian Weed Management. 2007. The introduced flora of Australia and its weed status. CRC for Australian Weed Management, Adelaide, Australia.
Randall, R [ed.]. 2017. A global compendium of weeds, 3rd ed. R. P. Randall, Perth, Australia.
Rice, A., P. Šmarda, M. Novosolov, M. Drori, L. Glick, N. Sabath, and S. Meiri et al. 2019. The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265-273.
Richards, A. 1997. Plant breeding systems, 2nd ed. Garland Science, New York, New York, USA.
Ross, L., P. Lambdon, and P. Hulme. 2008. Disentangling the roles of climate, propagule pressure and land use on the current and potential elevational distribution of the invasive weed Oxalis pes-caprae L. on Crete. Perspectives in Plant Ecology, Evolution and Systematics 10: 251-258.
Rozefelds, A., L. Cave, D. Morris, and A. Buchanan. 1999. The weed invasion in Tasmania since 1970. Australian Journal of Botany 47: 23-48.
Salter, T. 1944. The genus Oxalis in South Africa. Cape Times Ltd., Cape Town, South Africa.
Sanz-Elorza, M., E. Dana Sánchez, and E. Sobrino Vesperinas. 2004. Atlas de las plantas alóctonas invasoras en España. Ministerio de Medio Ambiente, Organismo Autónomo Parque Nacionales, Madrid, Spain.
Schneider, C., W. Rasband, and K. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.
Segraves, K. 2017. The effects of genome duplications in a community context. New Phytologist 215: 57-69.
Segraves, K., and J. Thompson. 1999. Plant polyploidy and pollination: Floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia. Evolution 53: 1114-1127.
Singmann, H., B. Bolker, J. Westfall, F. Aust, and M. Ben-Shachar. 2015. afex: Analysis of factorial experiments. R package version 0.13-145. Websites: https://afex.singmann.science/; https://github.com/singmann/afex/
Sliwinska, E., J. Loureiro, I. Leitch, P. Šmarda, J. Bainard, P. Bureš, and Z. Chumová et al. 2021. Application-based guidelines for best practices in plant flow cytometry. Cytometry Part A 101: 749-781.
Soltis, D. 1984. Autopolyploidy in Tolmiea menziesii (Saxifragaceae). American Journal of Botany 71: 1171-1174.
Soltis, D., V. Albert, J. Leebens-Mack, C. Bell, A. Paterson, C. Zheng, D. Sankoff et al. 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96: 336-348.
Soltis, P., D. Marchant, Y. Van de Peer, and D. Soltis. 2015. Polyploidy and genome evolution in plants. Current Opinion in Genetics & Development 35: 119-125.
Sonnleitner, M., R. Flatscher, P. Escobar García, J. Rauchová, J. Suda, G. Schneeweiss, K. Hülber, and P. Schönswetter. 2010. Distribution and habitat segregation on different spatial scales among diploid, tetraploid and hexaploid cytotypes of Senecio carniolicus (Asteraceae) in the Eastern Alps. Annals of Botany 106: 967-977.
Sora, D., P. Kron, and B. Husband. 2016. Genetic and environmental determinants of unreduced gamete production in Brassica napus, Sinapis arvensis and their hybrids. Heredity 117: 440-448.
Stebbins, G. L. 1950. Variation and evolution in plants. Columbia University Press, New York, New York, USA.
Stebbins, G. L. 1971. Chromosomal evolution in higher plants. Edward Arnold, London, UK.
Strong, D., and D. Ayres. 2013. Ecological and evolutionary misadventures of Spartina. Annual Review of Ecology, Evolution, and Systematics 44: 389-410.
Suda, J., and T. Herben. 2013. Ploidy frequencies in plants with ploidy heterogeneity: Fitting a general gametic model to empirical population data. Proceedings of the Royal Society, B, Biological Sciences 280: 20122387.
Tate, J., D. Soltis, and P. Soltis. 2005. Polyploidy in plants. In T. R. Gregory [ed.], The evolution of the genome, 371-426. Elsevier, Amsterdam, Netherlands.
Theodoridis, S., C. Randin, O. Broennimann, T. Patsiou, and E. Conti. 2013. Divergent and narrower climatic niches characterize polyploid species of European primroses in Primula sect. Aleuritia. Journal of Biogeography 40: 1278-1289.
Thissen, D., L. Steinberg, and D. Kuang. 2002. Quick and easy implementation of the Benjamini-Hochberg procedure for controlling the false positive rate in multiple comparisons. Journal of Educational and Behavioral Statistics 27: 77-83.
Thompson, J., and K. Merg. 2008. Evolution of polyploidy and the diversification of plant-pollinator interactions. Ecology 89: 2197-2206.
Thompson, J., S. Nuismer, and K. Merg. 2004. Plant polyploidy and the evolutionary ecology of plant/animal interactions. Biological Journal of the Linnean Society, Linnean Society of London 82: 511-519.
Trávníček, P., B. Kubátová, V. Čurn, J. Rauchová, E. Krajníková, J. Jersáková, and J. Suda. 2010. Remarkable coexistence of multiple cytotypes of the Gymnadenia conopsea aggregate (the fragrant orchid): Evidence from flow cytometry. Annals of Botany 107: 77-87.
Trojak-Goluch, A., and U. Skomra. 2013. Artificially induced polyploidization in Humulus lupulus L. and its effect on morphological and chemical traits. Breeding Science 63: 393-399.
Vaio, M., A. Gardner, P. Speranza, E. Emshwiller, and M. Guerra. 2016. Phylogenetic and cytogenetic relationships among species of Oxalis section Articulatae (Oxalidaceae). Plant Systematics and Evolution 302: 1253-1265.
Vamosi, J., S. Goring, B. Kennedy, R. Mayberry, C. Moray, L. Neame, N. 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. 2011. A mystery unveiled. Genome Biology 12: 113.
Van de Peer, Y., J. Fawcett, S. Proost, L. Sterck, and K. Vandepoele. 2009. The flowering world: A tale of duplications. Trends in Plant Science 14: 680-688.
Van Drunen, W., and J. Friedman. 2022. Autopolyploid establishment depends on life-history strategy and the mating outcomes of clonal architecture. Evolution 76: 1953-1970.
Van Drunen, W., and B. Husband. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytologist 224: 1266-1277.
Verdaguer, D., A. Sala, and M. Vilà. 2010. Effect of environmental factors and bulb mass on the invasive geophyte Oxalis pes-caprae development. Acta Oecologica 36: 92-99.
Veselý, P., P. Bureš, and P. Šmarda. 2013. Nutrient reserves may allow for genome size increase: Evidence from comparison of geophytes and their sister non-geophytic relatives. Annals of Botany 112: 1193-1200.
Veselý, P., P. Bureš, P. Šmarda, and T. Pavlíček. 2012. Genome size and DNA base composition of geophytes: The mirror of phenology and ecology? Annals of Botany 109: 65-75.
Viehmannová, I., E. Cusimamani, M. Bechyne, M. Vyvadilová, and M. Greplová. 2009. In vitro induction of polyploidy in yacon (Smallanthus sonchifolius). Plant Cell, Tissue and Organ Culture (PCTOC) 97: 21-25.
Vila, M., I. Bartomeus, I. Gimeno, A. Traveset, and E. Moragues. 2006. Demography of the invasive geophyte Oxalis pes-caprae across a mediterranean island. Annals of Botany 97: 1055-1062.
Wang, X., J. Morton, J. Pellicer, I. Leitch, and A. Leitch. 2021. Genome downsizing after polyploidy: Mechanisms, rates and selection pressures. Plant Journal 107: 1003-1015.
Wang, Z., M. Wang, L. Liu, and F. Meng. 2013. Physiological and proteomic responses of diploid and tetraploid black locust (Robinia pseudoacacia L.) subjected to salt stress. International Journal of Molecular Sciences 14: 20299-20325.
Warner, D., and G. Edwards. 1993. Effects of polyploidy on photosynthesis. Photosynthesis Research 35: 135-147.
Weiss-Schneeweiss, H., K. Emadzade, T. Jang, and G. Schneeweiss. 2013. Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenetic and Genome Research 140: 137-150.
Wickham, H. 2016. ggplot2: Elegant graphics for data analysis. Springer, New York, New York, USA.
Williams, V., L. Jones, and J. Tukey. 1999. Controlling error in multiple comparisons, with examples from state-to-state differences in educational achievement. Journal of Educational and Behavioral Statistics 24: 42-69.
Xiong, Z., R. Gaeta, and J. Pires. 2011. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proceedings of the National Academy of Sciences, USA 108: 7908-7913.