BACKGROUND AND AIMS: While variation in genome size and chromosome numbers and their consequences are often investigated in plants, the biological relevance of variation in chromosome size remains poorly known. Here, we examine genome and mean chromosome size in the cyperid clade (families Cyperaceae, Juncaceae and Thurniaceae), which is the largest vascular plant lineage with predominantly holocentric chromosomes. METHODS: We measured genome size in 436 species of cyperids using flow cytometry, and augment these data with previously published datasets. We then separately compared genome and mean chromosome sizes (2C/2n) amongst the major lineages of cyperids and analysed how these two genomic traits are associated with various environmental factors using phylogenetically informed methods. KEY RESULTS: We show that cyperids have the smallest mean chromosome sizes recorded in seed plants, with a large divergence between the smallest and largest values. We found that cyperid species with smaller chromosomes have larger geographical distributions and that there is a strong inverse association between mean chromosome size and number across this lineage. CONCLUSIONS: The distinct patterns in genome size and mean chromosome size across the cyperids might be explained by holokinetic drive. The numerous small chromosomes might function to increase genetic diversity in this lineage where crossovers are limited during meiosis.

Bolus Herbarium Department of Biological Sciences University of Cape Town Private Bag X3 Rondebosch Cape Town 7701 South Africaand

Botany and N C W Beadle Herbarium School of Environmental and Rural Science University of New England Armidale NSW 2351 Australia

Botany Area Department of Molecular Biology and Biochemical Engineering Universidad Pablo de Olavide ctra de Utrera km 1 41013 Seville Spain

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Department of Plant Biology and Ecology University of Seville Reina Mercedes 6 41012 Seville Spain

Institut de recherche en biologie végétale Département de sciences biologiques Université de Montréal 4101 Sherbrooke East Montreal QC H1X 2B2 Canada

Institute of Botany of the Czech Academy of Sciences 252 43 Průhonice Czech Republic

Montreal Botanical Garden 4101 Sherbrooke East Montreal QC H1X 2B2 Canada

National Herbarium of New South Wales Australian Institute of Botanical Science Australian Botanic Garden Locked Bag 6002 Mount Annan New South Wales 2567 Australia

National Museum Department of Botany Cirkusová 1740 193 00 Prague 9 Czech Republic

New York Botanical Garden Bronx NY 10458 5126 USA

Royal Botanic Gardens Kew Richmond Surrey TW9 3AE UK

Systematic and Evolutionary Botany Lab Department of Biology Ghent University K L Ledeganckstraat 35 9000 Gent Belgium

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Avdulov  NP.  1931. Karyo-systematische untersuchungen der familie Gramineen. Bulletin of Applied Botany, of Genetics and Plant Breeding, Leningrad 44: 1–428.

Baez  M, Kuo Y-T, Dias Y, et al. . 2020. Analysis of the small chromosomal Prionium serratum (Cyperid) demonstrates the importance of reliable methods to differentiate between mono- and holocentricity. Chromosoma 129: 285–297. PubMed PMC

Benjamini  Y, Hochberg Y.  1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57: 28989–28300. doi:10.1111/j.2517-6161.1995.tb02031.x. DOI

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

Blomberg  SP, Garland T, Ives AR.  2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745. doi:10.1111/j.0014-3820.2003.tb00285.x. PubMed DOI

Brown  JH.  1984. On the relationship between abundance and distribution of species. The American Naturalist 124: 255–279. doi:10.1086/284267. DOI

Brožová  V, Proćków J, Drábková LZ.  2022. Toward finally unraveling the phylogenetic relationships of Juncaceae with respect to another cyperid family, Cyperaceae. Molecular Phylogenetics and Evolution 177: 107588. PubMed

Brummitt  RK, Pando F, Hollis S, Brummitt N.  2001. World geographical scheme for recording plant distributions. Pittsburgh, PA: Hunt Institute for Botanical Documentation, Carnegie-Mellon University.

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. doi:10.1007/bf02803644. DOI

Bureš  P, Zedek F.  2014. Holokinetic drive: centromere drive in chromosomes without centromeres. Evolution 68: 2412–2420. doi:10.1111/evo.12437. PubMed DOI

Bureš  P, Zedek F, Marková M.  2013. Holocentric chromosomes. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF, eds. Plant genome diversity, Vol. 2. Vienna: Springer, 187–208.

Burt  A.  2000. Perspective: sex, recombination, and the efficacy of selection – was Weismann right? Evolution 54: 337–351. doi:10.1111/j.0014-3820.2000.tb00038.x. PubMed DOI

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. doi:10.1093/aob/mcab028. PubMed DOI PMC

Can  M, Wei W, Zi H, et al. . 2020. Genome sequence of Kobresia littledalei, the first chromosome-level genome in the family Cyperaceae. Scientific Data 7: 1–8. PubMed PMC

Cardillo  M, Dinnage R, McAlister W.  2019. The relationship between environmental niche breadth and geographic range size across plant species. Journal of Biogeography 46: 97–109.

Cardoso  P.  2017. red – an R package to facilitate species red list assessments according to the IUCN criteria. Biodiversity Data Journal (5): e20530. PubMed PMC

Carta  A, Bedini G, Peruzzi L.  2018. Unscrambling phylogenetic effects and ecological determinants of chromosome number in major angiosperm clades. Scientific Reports 8: 14258. PubMed PMC

Carta  A, Bedini G, Peruzzi L.  2020. A deep dive into the ancestral chromosome number and genome size of flowering plants. New Phytologist 228: 1097–1106. doi:10.1111/nph.16668. PubMed DOI

Chamberlain  S, Barve V, Mcglinn D, Oldoni D, Desmet P, Geffert L, Ram K.  2020. rgbif: interface to the Global Biodiversity Information Facility API. https://cran.r-project.org/web/packages/rgbif/rgbif.pdf

Chung  K, Hipp AL, Roalson EH.  2012. Chromosome number evolves independently of genome size in a clade with nonlocalized centromeres (Carex: Cyperaceae). Evolution 66: 2708–2722. doi:10.1111/j.1558-5646.2012.01624.x. PubMed DOI

Doležel  J, Bartoš J, Voglmayr H, Greilhuber J.  2003. Nuclear DNA content and genome size of trout and human. Cytometry A 51: 127–128. PubMed

Dormann  CF, Elith J, Bacher S, et al. . 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36: 27–46.

Drábková  LZ, Vlček C.  2009. DNA variation within Juncaceae: comparison of impact of organelle regions on phylogeny. Plant Systematics and Evolution 278: 169–186.

Dunnett  CW.  1980. Pairwise multiple comparisons in the homogeneous variance, unequal sample size case. Journal of the American Statistical Association 75: 789–795. doi:10.1080/01621459.1980.10477551. DOI

Edelsbrunner  H, Mücke EP.  1994. Three-dimensional alpha shapes. ACM Transactions on Graphics 13: 43–72.

Elliott  TL, Muasya AM, Bureš P.  2022. Complex patterns of ploidy in a holocentric plant clade (Schoenus, Cyperaceae) in the Cape biodiversity hotspot. Annals of Botany. doi:10.1093/aob/mcac027. PubMed DOI PMC

Elliott  TL, Larridon I, Barrett RL, Bruhl JJ, Costa SM, Escudero M, Hipp AL, Jiménez-Mejías P, Kirschner J, Luceño M, Ignacio Márquez-Corro J, Martín-Bravo S, Roalson EH, Semmouri I, Spalink D, Wayt Thomas W, Villaverde T, Wilson KL, Muthama Muasya A.  2022. Addressing inconsistencies in Cyperaceae and Juncaceae taxonomy: Comment on Brožová et al. Molecular Phylogenetics and Evolution. doi:10.1016/j.ympev.2022.107665. PubMed DOI

Escudero  M, Hipp AL, Hansen TF, Voje KL, Luceño M.  2012. Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). New Phytologist 195: 237–247. doi:10.1111/j.1469-8137.2012.04137.x. PubMed DOI

Escudero  M, Maguilla E, Loureiro J, Castro M, Castro S, Modesto L.  2015. Genome size stability despite high chromosome number variation in Carex gr. laevigata. American Journal of Botany 102: 233–238. PubMed

Escudero  M, Márquez-Corro JI, Hipp AL.  2016. The phylogenetic origins and evolutionary history of holocentric chromosomes. Systematic Botany 41: 580–585. doi:10.1600/036364416x692442. DOI

Escudero  M, Hahn M, Hipp AL.  2018. RAD‐seq linkage mapping and patterns of segregation distortion in sedges: meiosis as a driver of karyotypic evolution in organisms with holocentric chromosomes. Journal of Evolutionary Biology 31: 833–843. doi:10.1111/jeb.13267. PubMed DOI

Flora of North America Editorial Committee.  1993. Flora of North America North of Mexico. New York: Oxford University Press.

Freckleton  R, Harvey P, Pagel M.  2002. Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist 160: 712–726. doi:10.1086/343873. PubMed DOI

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. doi:10.1126/science.220.4601.1049. PubMed DOI

Gardiner  JD, Behnsen J, Brassey CA.  2018. Alpha shapes: determining 3D shape complexity across morphologically diverse structures. BMC Evolutionary Biology 18: 1–16. PubMed PMC

Gaston  KJ, Spicer JI.  2001. The relationship between range size and niche breadth: a test using five species of Gammarus (Amphipoda). Global Ecology and Biogeography 10: 179–188. doi:10.1046/j.1466-822x.2001.00225.x. DOI

Global Carex Group,  Roalson  EH, Jiménez-Mejías P, et al. . 2021. A framework infrageneric classification of Carex (Cyperaceae) and its organizing principles. Journal of Systematics and Evolution 59: 726–762.

Goetghebeur  P.  1998. Cyperaceae. In: Kubitzki K, ed. The families and genera of vascular plants. Flowering plants, Monocotyledons: Alismatanae and Commelinanae (except Gramineae). New York: Springer, 141–190.

Govaerts  R, Jiménez-Mejías P, Koopman J, et al. . 2021. World checklist of selected plant families. Cyperaceae. Kew: Royal Botanic Gardens,

Greilhuber  J, Leitch IJ.  2013. Genome size and the phenotype. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF, eds. Plant genome diversity, Vol. 2. Vienna: Springer, 323–344.

Greilhuber  J, Doležel J, Lysák 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

Greilhuber  J, Borsch T, Müller K, Worberg A, Porembski S, Barthlott W.  2006. Smallest angiosperm genomes found in Lentibulariaceae, with chromosomes of bacterial size. Plant Biology 8: 770–777. PubMed

Guerra  M, Ribeiro T, Felix LP.  2019. Monocentric chromosomes in Juncus (Juncaceae) and implications for the chromosome evolution of the family. Botanical Journal of the Linnean Society 191: 475–483. doi:10.1093/botlinnean/boz065. DOI

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

Guignard  M, Leitch A, Acquisti C, et al. . 2017. Impacts of nitrogen and phosphorus: from genomes to natural ecosystems and agriculture. Frontiers in Ecology and Evolution 5: 70.

Harms  LJ.  1968. Cytotaxonomic studies in Eleocharis subser. Palustres: central United States taxa. American Journal of Botany 55: 966–974. doi:10.1002/j.1537-2197.1968.tb07456.x. DOI

Hasegawa  N.  1932. Comparison of chromosome types in Disporum. Cytologia 4: 350–368.

Heitz  H.  1925–1926. Der nachweis der chromosomen. Vergleichende Studien über ihre Zahl, Grösse ond Form im Pflanzenreich I. Zeitschrift für Botanik 18: 627–681.

Hidalgo  O, Pellicer J, Christenhusz M, Schneider H, Leitch AR, Leitch IJ.  2017. Is there an upper limit to genome size? Trends in Plant Science 22: 567–573. doi:10.1016/j.tplants.2017.04.005. PubMed DOI

Hijmans  RJ.  2020. Geographic data analysis and modeling [R package raster version 3.4-5]. https://rspatial.org/raster

Hofstatter  PG, Thangavel G, Lux T, et al. . 2022. Repeat-based holocentromeres influence genome architecture and karyotype evolution. Cell 185: 3153–3168.e18. doi:10.1016/j.cell.2022.06.045. PubMed DOI

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

IUCN.  2001. IUCN Red List categories and criteria: Version 3.1. IUCN Species Survival Commission. Gland, Switzerland and Cambridge, UK: IUCN.

Jankowska  M, Fuchs J, Klocke E, et al. . 2015. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma 124: 519–528. doi:10.1007/s00412-015-0524-y. PubMed DOI

Janzen  DH.  1967. Why mountain passes are higher in the tropics? The American Naturalist 101: 233–249.

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.

Johnson  C.  1998. Species extinction and the relationship between distribution and abundance. Nature 394: 272–274.

Kang  M, Wang J, Huang H.  2015. Nitrogen limitation as a driver of genome size evolution in a group of karst plants. Scientific Reports 5: 1–8. PubMed PMC

Karger  DN, Conrad O, Böhner J, et al. . 2017. Climatologies at high resolution for the earth’s land surface areas. Scientific Data 4: 170122. doi:10.1038/sdata.2017.122. PubMed DOI 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. doi:10.1111/j.1095-8339.2012.01238.x. DOI

Knight  CA, Ackerly DD.  2002. Variation in nuclear DNA content across environmental gradients: a quantile regression analysis. Ecology Letters 5: 66–76. doi:10.1046/j.1461-0248.2002.00283.x. DOI

Knight  CA, Molinari NA, Petrov DA.  2005. The large genome constraint hypothesis: evolution, ecology and phenotype. Annals of Botany 95: 177–190. doi:10.1093/aob/mci011. PubMed DOI PMC

Kostoff  D.  1939. Evolutionary significance of chromosome size and chromosome number in plants. Current Science 8: 306–310.

Krátká  M, Šmerda J, Lojdová K, Bureš P, Zedek F.  2021. Holocentric chromosomes probably do not prevent centromere drive in Cyperaceae. Frontiers in Plant Science 12: 229. PubMed PMC

LaBar  T, Adami C.  2020. Genome size and the extinction of small populations. In: Banzhaf W, Cheng BHC, Deb K, et al.., eds. Evolution in action: past, present and future. Cham, Switzerland: Springer, 167–183.

Lafarge  T, Pateiro-Lopez B.  2020. Implementation of the 3D alpha-shape for the reconstruction of 3D sets from a point cloud. alphashape3d: R package version 1.3.1. https://CRAN.R-project.org/package=alphashape3d

Larridon  I, Spalink D, Jiménez‐Mejías P, et al. . 2021a. The evolutionary history of sedges (Cyperaceae) in Madagascar. Journal of Biogeography 48: 917–932. doi:10.1111/jbi.14048. DOI

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

Lee  B, Cho Y, Kim S.  2019. Genome size estimation of 43 Korean Carex. Korean Journal of Plant Taxonomy 49: 334–344. doi:10.11110/kjpt.2019.49.4.334. DOI

Leitch  AR, Leitch IJ.  2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481–483. doi:10.1126/science.1153585. PubMed DOI

Leitch  IJ, Beaulieu JM, Chase MW, Leitch AR, Fay MF.  2010. Genome size dynamics and evolution in monocots. Journal of Botany 2010: 862516.

Leutner  B, Horning N, Schwalb-Willmann J, Hijmans R.  2017. RStoolbox: tools for remote sensing data analysis. R package version 0.1 7. https://CRAN.R-project.org/package=RStoolbox

Levin  DA, Funderburg SW.  1979. Genome size in angiosperms: temperate versus tropical species. The American Naturalist 114: 784–795. doi:10.1086/283528. DOI

Linder  HP, Rudall PJ.  2005. Evolutionary history of Poales. Annual Review of Ecology, Evolution, and Systematics 36: 107–124. doi:10.1146/annurev.ecolsys.36.102403.135635. DOI

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

Lucek  K, Augustijnen H, Escudero M.  2022. A holocentric twist to chromosomal speciation? Trends in Ecology & Evolution 37: 655–662. PubMed

Luceño  M, Vanzela ALL, Guerra M.  1998. Cytotaxonomic studies in Brazilian Rhynchospora (Cyperaceae), a genus exhibiting holocentric chromosomes. Canadian Journal of Botany 76: 440–449.

Lynch  M.  2007. The frailty of adaptive hypotheses for the origins of organismal complexity. Proceedings of the National Academy of Sciences, USA 104: 8597–8604. doi:10.1073/pnas.0702207104. PubMed DOI PMC

Lynch  M, Conery JS.  2003. The origins of genome complexity. Science 302: 1401–1404. doi:10.1126/science.1089370. PubMed DOI

Mandrioli  M, Manicardi GC.  2020. Holocentric chromosomes. PLoS Genetics 16: e1008918. doi:10.1371/journal.pgen.1008918. PubMed DOI PMC

Márquez-Corro  JI, Martín-Bravo S, Pedrosa-Harand A, Hipp AL, Luceño M, Escudero M.  2019a. Karyotype evolution in holocentric organisms. In: eLS. Chichester: John Wiley & Sons.doi: 10.1002/9780470015902.a0028758 DOI

Márquez-Corro  JI, Martín-Bravo S, Spalink D, Luceño M, Escudero M.  2019b. Inferring hypothesis-based transitions in clade-specific models of chromosome number evolution in sedges (Cyperaceae). Molecular Phylogenetics and Evolution 135: 203–209. doi:10.1016/j.ympev.2019.03.006. PubMed DOI

Márquez-Corro  JI, Martín-Bravo S, Jiménez‐Mejías P, et al. . 2021. Macroevolutionary insights into sedges (Carex: Cyperaceae): the effects of rapid chromosome number evolution on lineage diversification. Journal of Systematics and Evolution 59: 776–790.

Melters  DP, Paliulis LV, Korf IF, Chan SW.  2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Research 20: 579–593. PubMed

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

Ng  CH, Lee SL, Tnah LH, Ng KKS, Lee CT, Madon M.  2016. Genome size variation and evolution in Dipterocarpaceae. Plant Ecology & Diversity 9: 437–446.

Nijalingappa  B.  1974. Cytological studies in Scirpus (Cyperaceae). Proceedings of the Indian Academy of Sciences 80: 134–138.

Nishikawa  K, Furuta Y, Ishitobi K.  1984. Chromosomal evolution in genus Carex as viewed from nuclear DNA content, with special reference to its aneuploidy. The Japanese Journal of Genetics 59: 465–472. doi:10.1266/jjg.59.465. DOI

Orme  D.  2013. The CAPER package: comparative analysis of phylogenetics and evolution in R. https://cran.r-project.org/web/packages/caper/index.html.

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 2: 189–191. PubMed

Paradis  E, Claude J, Strimmer K.  2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. doi:10.1093/bioinformatics/btg412. PubMed DOI

Pellicer  J, Leitch IJ.  2020. The Plant DNA C-values database (release 7.1): an updated online repository of plant genome size data for comparative studies. New Phytologist 226: 301–305. 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. doi:10.3390/genes9020088. PubMed DOI PMC

Plačková  K, Zedek F, Schubert V, Houben A, Bureš P.  2022. Kinetochore size scales with chromosome size in bimodal karyotypes of Agavoideae. Annals of Botany 130: 77–84. PubMed PMC

Planta  J, Liang Y-Y, Xin H, et al. . 2022. Chromosome scale genome assemblies and annotations for Poales species Carex cristatella, Carex scoparia, Juncus effusus and Juncus inflexus. G3 Genes| Genomes| Genetics 12: jkac211. doi:10.1093/g3journal/jkac211. PubMed DOI PMC

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

Rice  A, Glick L, Abadi S, et al. . 2015. The Chromosome Counts Database (CCDB) – a community resource of plant chromosome numbers. New Phytologist 206: 19–26. PubMed

Richardson  L.  2019. Beautiful soup documentation Version 4.4.0. https://beautiful-soup-4.readthedocs.io/en/latest/

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

Roalson  EH, McCubbin AG, Whitkus R.  2007. Chromosome evolution in Cyperales. Aliso 23: 62–71A.

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. doi:10.1071/sb17002. DOI

Slatyer  RA, Hirst M, Sexton JP.  2013. Niche breadth predicts geographical range size: a general ecological pattern. Ecology Letters 16: 1104–1114. doi:10.1111/ele.12140. PubMed DOI

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

Šmarda  P, Hejcman M, Březinová A, et al. . 2013. Effect of phosphorus availability on the selection of species with different ploidy levels and genome sizes in a long-term grassland fertilization experiment. New Phytologist 200: 911–921. doi:10.1111/nph.12399. PubMed DOI

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, USA 111: E4096–E4102. PubMed PMC

Soltis  DE, Soltis PS, Bennett MD, Leitch IJ.  2003. Evolution of genome size in the angiosperms. American Journal of Botany 90: 1596–1603. doi:10.3732/ajb.90.11.1596. PubMed DOI

de Sousa  LM, Poggio L, Batjes NH, et al. . 2020. SoilGrids 2.0: producing quality-assessed soil information for the globe. Soil 7: 217–240.

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

Stace  CA.  2000. Cytology and cytogenetics as a fundamental taxonomic resource for the 20th and 21st centuries. Taxon 49: 451–477. doi:10.2307/1224344. DOI

Stapley  J, Feulner PGD, Johnston SE, Santure AW, Smadja CM.  2017. Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Philosophical Transactions of the Royal Society B: Biological Sciences 372: 20160455. PubMed PMC

Stebbins  GL.  1966. Chromosomal variation and evolution: polyploidy and chromosome size and number shed light on evolutionary processes in higher plants. Science 152: 1463–1469. doi:10.1126/science.152.3728.1463. PubMed DOI

Temsch  EM, Koutecký P, Urfus T, Šmarda P, Doležel J.  2022. Reference standards for flow cytometric estimation of absolute nuclear DNA content in plants. Cytometry A 101: 710–724. PubMed PMC

Tukey  JW.  1949. Comparing individual means in the analysis of variance. Biometrics 5: 99–114. PubMed

Vanzela  ALL, Guerra M, Luceño M.  1996. Rhynchospora tenuis Link (Cyperaceae), a species with the lowest number of holocentric chromosomes. Cytobios 88: 219–228.

Varela  S, Anderson RP, García-Valdés R, Fernández-González F.  2014. Environmental filters reduce the effects of sampling bias and improve predictions of ecological niche models. Ecography 37: 1084–1091.

Veleba  A, Bureš P, Adamec L, Šmarda P, Lipnerová I, Horová L.  2014. Genome size and genomic GC content evolution in the miniature genome‐sized family Lentibulariaceae. New Phytologist 203: 22–28. doi:10.1111/nph.12790. PubMed DOI

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. doi:10.1093/aob/mcw229. PubMed DOI PMC

Veleba  A, Zedek F, Horová L, Veselý P, Srba M, Šmarda P, Bureš P.  2020. Is the evolution of carnivory connected with genome size reduction? American Journal of Botany 107: 1253–1259. doi: 10.1002/ajb2.1526 PubMed DOI

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

Vinogradov  AE.  2003. Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19: 609–614. doi:10.1016/j.tig.2003.09.010. PubMed DOI

Wang  S, Veller C, Sun F, et al. . 2019. Per-nucleus crossover covariation and implications for evolution. Cell 177: 326–338. PubMed PMC

WCVP.  2022. World Checklist of Vascular Plants, version 2.0. Facilitated by the Royal Botanic Gardens, Kew. http://wcvp.science.kew.org/

Xu  S, Dai Z, Guo P, et al. . 2021. ggtreeExtra: compact visualization of richly annotated phylogenetic data. Molecular Biology and Evolution 38: 4039–4042. doi:10.1093/molbev/msab166. PubMed DOI PMC

Yang  X, Post WM, Thornton PE, Jain A.  2013. The distribution of soil phosphorus for global biogeochemical modeling. Biogeosciences 9: 2525–2537.

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. doi:10.1186/1471-2229-10-265. PubMed DOI PMC

Zedek  F, Veselý P, Horová L, Bureš P.  2016. Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants. Scientific Reports 6: 27161. doi:10.1038/srep27161. PubMed DOI PMC

Zedek  F, Veselý P, Tichý L, et al. . 2022. Holocentric plants are more competitive under higher UV‐B doses. New Phytologist 233: 15–21. PubMed

Zizka  A, Silvestro D, Andermann T, et al. . 2019. CoordinateCleaner: standardized cleaning of occurrence records from biological collection databases. Methods in Ecology and Evolution 10: 744–751. doi:10.1111/2041-210x.13152. DOI

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