Complex patterns of ploidy in a holocentric plant clade (Schoenus, Cyperaceae) in the Cape biodiversity hotspot

. 2023 Feb 07 ; 131 (1) : 143-156.

Jazyk angličtina Země Anglie, Velká Británie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35226733

BACKGROUND AND AIMS: It is unclear how widespread polyploidy is throughout the largest holocentric plant family - the Cyperaceae. Because of the prevalence of chromosomal fusions and fissions, which affect chromosome number but not genome size, it can be impossible to distinguish if individual plants are polyploids in holocentric lineages based on chromosome count data alone. Furthermore, it is unclear how differences in genome size and ploidy levels relate to environmental correlates within holocentric lineages, such as the Cyperaceae. METHODS: We focus our analyses on tribe Schoeneae, and more specifically the southern African clade of Schoenus. We examine broad-scale patterns of genome size evolution in tribe Schoeneae and focus more intensely on determining the prevalence of polyploidy across the southern African Schoenus by inferring ploidy level with the program ChromEvol, as well as interpreting chromosome number and genome size data. We further investigate whether there are relationships between genome size/ploidy level and environmental variables across the nutrient-poor and summer-arid Cape biodiversity hotspot. KEY RESULTS: Our results show a large increase in genome size, but not chromosome number, within Schoenus compared to other species in tribe Schoeneae. Across Schoenus, there is a positive relationship between chromosome number and genome size, and our results suggest that polyploidy is a relatively common process throughout the southern African Schoenus. At the regional scale of the Cape, we show that polyploids are more often associated with drier locations that have more variation in precipitation between dry and wet months, but these results are sensitive to the classification of ploidy level. CONCLUSIONS: Polyploidy is relatively common in the southern African Schoenus, where a positive relationship is observed between chromosome number and genome size. Thus, there may be a high incidence of polyploidy in holocentric plants, whose cell division properties differ from monocentrics.

Zobrazit více v PubMed

Bales  AL, Hersch-Green EI. 2019. Effects of soil nitrogen on diploid advantage in fireweed, Chamerion angustifolium (Onagraceae). Ecology and Evolution 9: 1095–1109. PubMed PMC

Barlow  PW, Nevin D. 1976. Quantitative karyology of some species of Luzula. Plant Systematics and Evolution 125: 77–86.

Beaulieu  JM, Leitch IJ, Patel S, Pendharkar A, Knight CA. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist 179: 975–986. PubMed

te Beest  M, Le Roux JJ, Richardson DM, et al.  2012. The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109: 19–45. PubMed PMC

Bennett  MD. 1987. Variation in genomic form in plants and its ecological implications. New Phytologist 106: 177–200.

Benson  DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. 2010. GenBank. Nucleic Acids Research 38: D46–D51. PubMed PMC

Blakeslee  AF, Belling J, Farnham M. 1920. Chromosomal duplication and Mendelian phenomena in Datura mutants. Science 52: 388–390. PubMed

Blomberg  SP, Garland T, Ives AR. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745. PubMed

Bozek  M, Leitch AR, Leitch IJ, Záveská Drábková L, Kuta E. 2012. Chromosome and genome size variation in Luzula (Juncaceae), a genus with holocentric chromosomes. Botanical Journal of the Linnean Society 170: 529–541.

Burchardt  P, Buddenhagen CE, Gaeta ML, Souza MD, Marques A, Vanzela ALL. 2020. Holocentric karyotype evolution in Rhynchospora is marked by intense numerical, structural, and genome size changes. Frontiers in Plant Science 11: 1390. PubMed PMC

Bureš  P. 1998. A high polyploid Eleocharis uniglumis sl (Cyperaceae) from Central and Southeastern Europe. Folia Geobotanica 33: 429–439.

Bureš  P, Zedek F, Marková M. 2013. Holocentric chromosomes. In: Leitch IJ, ed. Plant genome diversity volume 2: physical structure, behaviour and evolution of plant genomes. Vienna: Springer-Verlag, 187–208.

Bureš  P, Zedek F. 2014. Holokinetic drive: centromere drive in chromosomes without centromeres. Evolution 68: 2412–2420. PubMed

Cacho  NI, McIntyre PJ, Kliebenstein DJ, Strauss SY. 2021. Genome size evolution is associated with climate seasonality and glucosinolates, but not life history, soil nutrients or range size, across a clade of mustards. Annals of Botany 127: 887–902. PubMed PMC

Castro-Jimenez  Y, Newton R, Price H, Halliwell R. 1989. Drought stress responses of Microseris species differing in nuclear DNA content. American Journal of Botany 76: 789–795.

Cavalier-Smith  T. 2005. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Annals of Botany 95: 147–175. PubMed PMC

Chapin  FS. 1980. The mineral-nutrition of wild plants. Annual Review of Ecology and Systematics 11: 233–260.

Chung  K, Hipp AL, Roalson EH. 2012. Chromosome number evolves independently of genome size in a clade with nonlocalized centromeres (Carex: Cyperaceae). Evolution; International Journal of Organic Evolution 66: 2708–2722. PubMed

Cramer  MD, Wootton LM, van Mazijk R, Verboom GA. 2019. New regionally modelled soil layers improve prediction of vegetation type relative to that based on global soil models. Diversity and Distributions 25: 1736–1750.

De Bodt  S, Maere S, Van de Peer Y. 2005. Genome duplication and the origin of angiosperms. Trends in Ecology & Evolution 20: 591–597. PubMed

Dodsworth  S, Chase MW, Leitch AR. 2016. Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Botanical Journal of the Linnean Society 180: 1–5.

Elliott  TL, Barrett RL, Muasya AM. 2019. A taxonomic revision of Schoenus cuspidatus and allies (Cyperaceae, tribe Schoeneae)—Part 1. South African Journal of Botany 121: 519–535.

Elliott  TL, Euston-Brown DIW, Muasya AM. 2020. Schoenus inconspicuus (Cyperaceae, tribe Schoeneae): a new species from Southern Africa. Phytotaxa 440: 239–244.

Elliott  TL, Muasya AM. 2017. Taxonomic realignment in the southern African Tetraria (Cyperaceae, tribe Schoeneae; Schoenus clade). South African Journal of Botany 112: 354–360.

Elliott  TL, Muasya AM. 2018. A taxonomic revision of Schoenus compar - Schoenus pictus and allies (Cyperaceae, tribe Schoeneae) with three new species described from South Africa. South African Journal of Botany 114: 303–315.

Elliott  TL, Muasya AM. 2019. Three new species and a new combination among Southern African Schoenus (Cyperaceae, tribe Schoeneae). Phytotaxa 401: 267–275.

Elliott  TL, Muasya AM. 2020a. A taxonomic revision of Schoenus cuspidatus and allies (Cyperaceae, tribe Schoeneae)—Part 2. South African Journal of Botany 130: 327–347.

Elliott  TL, Muasya AM. 2020b. A taxonomic revision of the Epischoenus group of Schoenus (Cyperaceae, tribe Schoeneae). South African Journal of Botany 135: 296–316.

Elliott  TL, van Mazijk R, Barrett RL, et al.  2021. Global dispersal and diversification of the genus Schoenus (Cyperaceae) from the Western Australian biodiversity hotspot. Journal of Systematics and Evolution 59: 791–808.

Freckleton  R, Harvey P, Pagel M. 2002. Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist 160: 712–726. PubMed

Galbraith  DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E. 1983. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220: 1049–1051. PubMed

Gelman  A, Rubin DB. 1992. Inference from iterative simulation using multiple sequences. Statistical Science 7: 457–472.

Glick  L, Mayrose I. 2014. ChromEvol: assessing the pattern of chromosome number evolution and the inference of polyploidy along a phylogeny. Molecular Biology and Evolution 31: 1914–1922. PubMed

Global Carex Group. 2021. A framework infrageneric classification of Carex (Cyperaceae) and its organizing principles. Journal of Systematics and Evolution 59: 726–762.

Greilhuber  J, Dolezel J, Lysak MA, Bennett M. 2005. The origin, evolution and proposed stabilization of the terms ‘Genome Size’ and ‘C-Value’ to describe nuclear DNA contents. Annals of Botany 95: 255–260. PubMed PMC

Guignard  MS, Nichols RA, Knell RJ, et al.  2016. Genome size and ploidy influence angiosperm species’ biomass under nitrogen and phosphorus limitation. New Phytologist 210: 1195–1206. PubMed PMC

Hadfield  JD. 2010. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. Journal of Statistical Software 33: 1–22. PubMed PMC

Håkansson  A. 1954. Meiosis and pollen mitosis in x-rayed and untreated spikelets of Eleocharis palustris. Hereditas 40: 325–345.

Harms  LJ. 1968. Cytotaxonomic studies in Eleocharis subser. Palustres: central United States taxa. American Journal of Botany 55: 966–974.

Hengl  T, Mendes de Jesus J, Heuvelink GB, et al.  2017. SoilGrids250m: Global gridded soil information based on machine learning. PLoS One 12: e0169748. PubMed PMC

Hijmans  RJ. 2020. Geographic data analysis and modeling [R package raster version 3.4-5]. https://cran.r-project.org/web/packages/raster/index.html.

Hipp  AL. 2007. Nonuniform processes of chromosome evolution in sedges (Carex: Cyperaceae). Evolution; International Journal of Organic Evolution 61: 2175–2194. PubMed

Hipp  AL, Rothrock PE, Roalson EH. 2009. The evolution of chromosome arrangements in Carex (Cyperaceae). The Botanical Review 75: 96–109.

Hodgson  J, Sharafi M, Jalili A, et al.  2010. Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Annals of Botany 105: 573–584. PubMed PMC

Hopper  SD. 2009. OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322: 49–86.

Husband  BC, Baldwin SJ, Suda J. 2013. The incidence of polyploidy in natural plant populations: major patterns and evolutionary processes. In: Leitch IJ, ed. Plant genome diversity volume 2: physical structure, behaviour and evolution of plant genomes. Vienna: Springer-Verlag, 255–276.

International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. Nature 436: 793–800. PubMed

Jiao  Y, Wickett NJ, Ayyampalayam S, et al.  2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473: 97–100. PubMed

Johnen  L, de Souza TB, Rocha DM, et al.  2020. Allopolyploidy and genomic differentiation in holocentric species of the Eleocharis montana complex (Cyperaceae). Plant Systematics and Evolution 306: 1–17.

Karger  DN, Conrad O, Böhner J, et al.  2017. Climatologies at high resolution for the earth’s land surface areas. Scientific Data 4: 170122. PubMed PMC

Katoh  K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. PubMed PMC

Kaur  N, Datson PM, Murray BG. 2012. Genome size and chromosome number in the New Zealand species of Schoenus (Cyperaceae). Botanical Journal of the Linnean Society 169: 555–564.

Knight  CA, Molinari NA, Petrov DA. 2005. The large genome constraint hypothesis: evolution, ecology and phenotype. Annals of Botany 95: 177–190. PubMed PMC

Kolodin  P, Cempírková H, Bureš P, et al.  2018. Holocentric chromosomes may be an apomorphy of Droseraceae. Plant Systematics and Evolution 304: 1289–1296.

Landis  JB, Soltis DE, Li Z, et al.  2018. Impact of whole-genome duplication events on diversification rates in angiosperms. American Journal of Botany 105: 348–363. PubMed

Larridon  I, Spalink D, Jiménez-Mejías P, et al.  2021.  b. The evolutionary history of sedges (Cyperaceae) in Madagascar. Journal of Biogeography 48: 917–932.

Larridon  I, Zuntini AR, Léveillé-Bourret E, et al.  2021.  a. A new classification of Cyperaceae (Poales) supported by phylogenomic data. Journal of Systematics and Evolution 59: 852–895.

Larsson  A. 2014. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30: 3276–3278. PubMed PMC

Leitch  A, Leitch I. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481–483. PubMed

Levin  DA. 1983. Polyploidy and novelty in flowering plants. The American Naturalist 122: 1–25.

Levin  DA. 2002. The role of chromosomal change in plant evolution. Oxford: Oxford University Press.

Levyns  MR. 1950. Tetraria Beauv. In: Adamson RS, Salter TM, eds. Flora of the Cape Peninsula. Cape Town: Juta, 121–128.

Linder  HP. 2005. Evolution of diversity: the Cape flora. Trends in Plant Science 10: 536–541. PubMed

Linder  HP, Verboom GA. 2015. The evolution of regional species richness: the history of the Southern African flora. Annual Review of Ecology, Evolution, and Systematics 46: 393–412.

Lipnerová  I, Bureš P, Horová L, Šmarda P. 2013. Evolution of genome size in Carex (Cyperaceae) in relation to chromosome number and genomic base composition. Annals of Botany 111: 79–94. PubMed PMC

Lwin  AK, Bertolini E, Pè ME, Zuccolo A. 2017. Genomic skimming for identification of medium/highly abundant transposable elements in Arundo donax and Arundo plinii. Molecular Genetics and Genomics 292: 157–171. PubMed

Lysák  MA, Schubert I. 2013. Mechanisms of chromosome rearrangements. In: Leitch IJ, ed. Plant genome diversity volume 2: physical structure, behaviour and evolution of plant genomes. Vienna: Springer-Verlag, 137–147.

Manning  J, Goldblatt P. 2012. Plants of the greater cape floristic region. 1: the Core Cape flora. Pretoria: South African National Biodiversity Institute.

Márquez-Corro  JI, Martín-Bravo S, Spalink D, Luceño M, Escudero M. 2019. Inferring hypothesis-based transitions in clade-specific models of chromosome number evolution in sedges (Cyperaceae). Molecular Phylogenetics and Evolution 135: 203–209. PubMed

Matzke  M, Scheid OM, Matzke A. 1999. Rapid structural and epigenetic changes in polyploid and aneuploid genomes. Bioessays 21: 761–767. PubMed

Mowforth  M, Grime J. 1989. Intra-population variation in nuclear DNA amount, cell size and growth rate in Poa annua L. Functional Ecology 3: 289–295.

Neumann  P, Oliveira L, Čížková J, et al.  2021. Impact of parasitic lifestyle and different types of centromere organization on chromosome and genome evolution in the plant genus Cuscuta. New Phytologist 229: 2365–2377. PubMed

Nordenskiöld  H. 1961. Tetrad analysis and the course of meiosis in three hybrids of Luzula campestris. Hereditas 47: 203–238.

Orme  D, Freckleton R, Thomas G, et al.  2013. Caper: comparative analysis of phylogenetics and evolution in R.https://cran.r-project.org/web/packages/caper/vignettes/caper.pdf.

Otto  F, Oldiges H, Göhde W, Jain V. 1981. Flow cytometric measurement of nuclear DNA content variations as a potential in vivo mutagenicity test. Cytometry: The Journal of the International Society for Analytical Cytology 2: 189–191. PubMed

Paradis  E, Claude J, Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. PubMed

Parisod  C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytologist 186: 5–17. PubMed

Pellicer  J, Hidalgo O, Dodsworth S, Leitch IJ. 2018. Genome size diversity and its impact on the evolution of land plants. Genes 9: 88. PubMed PMC

Potts  A, Rebelo T, Barrett R, Stirton C. 2018. Hybrid Cape and Kwong. South African Journal of Botany 118: 284–352.

R Core Team.  2020. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

Ramsey  J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589–639.

Revell  LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223.

Rice  A, Mayrose I. 2021. Model adequacy tests for probabilistic models of chromosome-number evolution. New Phytologist 229: 3602–3613. PubMed

Rice  A, Šmarda P, Novosolov M, et al.  2019. The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265–273. PubMed

Roalson  EH. 2008. A synopsis of chromosome number variation in the Cyperaceae. The Botanical Review 74: 209–393.

Schrader  F. 1935. Notes on the mitotic behavior of long chromosomes. Cytologia 6: 422–430.

da Silva  CRM, de Souza TB, Trevisan R, et al.  2017. Genome differentiation, natural hybridisation and taxonomic relationships among Eleocharis viridans, E. niederleinii and E. ramboana (Cyperaceae). Australian Systematic Botany 30: 183–195.

da Silva  CRM, Trevisan R, González-Elizondo MS, Ferreira JM, Vanzela ALL. 2010. Karyotypic diversification and its contribution to the taxonomy of Eleocharis (Cyperaceae) from Brazil. Australian Journal of Botany 58: 49–60.

Šmarda  P, Bureš P, Horová L, et al.  2014. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proceedings of the National Academy of Sciences 111: E4096–E4102. PubMed PMC

Šmarda  P, Bureš P, Horová L, Foggi B, Rossi G. 2008. Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction. Annals of Botany 101: 421–433. PubMed PMC

Smith  SA, O’Meara BC. 2012. treePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28: 2689–2690. PubMed

Soltis  DE, Soltis PS, Schemske DW, et al.  2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56: 13–30.

Soltis  DE, Soltis PS. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348–352. PubMed

de Souza  TB, Chaluvadi SR, Johnen L, et al.  2018. Analysis of retrotransposon abundance, diversity and distribution in holocentric Eleocharis (Cyperaceae) genomes. Annals of Botany 122: 279–290. PubMed PMC

Spalink  D, Drew BT, Pace MC, et al.  2016. Evolution of geographical place and niche space: patterns of diversification in the North American sedge (Cyperaceae) flora. Molecular Phylogenetics and Evolution 95: 183–195. PubMed

Stamatakis  A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313. PubMed PMC

Stock  W, Lewis O. 1984. Uptake and assimilation of nitrate and ammonium by an evergreen fynbos shrub species Protea repens L. (Proteaceae). New Phytologist 97: 261–268.

Stock  W, Lewis O. 1986. Soil nitrogen and the role of fire as a mineralizing agent in a South African coastal fynbos ecosystem. Journal of Ecology 74: 317–328.

Temsch  EM, Koutecký P, Urfus T, Šmarda P, Doležel J. 2021. Reference standards for flow cytometric estimation of absolute nuclear DNA content in plants. Cytometry. Part A. 10.1002/cyto.a.24495. PubMed DOI PMC

Van de Peer  Y, Fawcett JA, Proost S, Sterck L, Vandepoele K. 2009. The flowering world: a tale of duplications. Trends in Plant Science 14: 680–688. PubMed

Veleba  A, Šmarda P, Zedek F, Horová L, Šmerda J, Bureš P. 2017. Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae). Annals of Botany 119: 409–416. PubMed PMC

Verboom  GA. 2006. A phylogeny of the schoenoid sedges (Cyperaceae: Schoeneae) based on plastid DNA sequences, with special reference to the genera found in Africa. Molecular Phylogenetics and Evolution 38: 79–89. PubMed

Veselý  P, Bureš P, Šmarda P, Pavlíček T. 2012. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany 109: 65–75. PubMed PMC

Viljoen  J-A, Muasya AM, Barrett RL, et al.  2013. Radiation and repeated transoceanic dispersal of Schoeneae (Cyperaceae) through the southern hemisphere. American Journal of Botany 100: 2494–2508. PubMed

Walczyk  AM, Hersch-Green EI. 2019. Impacts of soil nitrogen and phosphorus levels on cytotype performance of the circumboreal herb Chamerion angustifolium: implications for polyploid establishment. American Journal of Botany 106: 906–921. PubMed

White  V, Hardie A, Raath P. 2020. Relationships between commonly-used South African and international soil phosphorus extraction tests on pristine and cultivated soils. South African Journal of Plant and Soil 37: 265–272.

Wood  TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences USA 106: 13875–13879. PubMed PMC

Yano  O, Hoshino T. 2005. Molecular phylogeny and chromosomal evolution of Japanese Schoenoplectus (Cyperaceae), based on ITS and ETS 1f sequences. Acta Phytotaxonomica et Geobotanica 56: 183–195.

Yano  O, Hoshino T. 2007. Karyomorphological studies of four species of Japanese Scleria (Cyperaceae). Cytologia 72: 275–278.

Yu  G, Smith DK, Zhu H, Guan Y, Lam TT-Y. 2017. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods in Ecology and Evolution 8: 28–36.

Zedek  F, Šmerda J, Šmarda P, Bureš P. 2010. Correlated evolution of LTR retrotransposons and genome size in the genus Eleocharis. BMC Plant Biology 10: 265. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...