BACKGROUND: Genome size is influenced by natural selection and genetic drift acting on variations from polyploidy and repetitive DNA sequences. We hypothesized that centromere drive, where centromeres compete for inclusion in the functional gamete during meiosis, may also affect genome and chromosome size. This competition occurs in asymmetric meiosis, where only one of the four meiotic products becomes a gamete. If centromere drive influences chromosome size evolution, it may also impact post-polyploid diploidization, where a polyploid genome is restructured to function more like a diploid through chromosomal rearrangements, including fusions. We tested if plant lineages with asymmetric meiosis exhibit faster chromosome size evolution compared to those with only symmetric meiosis, which lack centromere drive as all four meiotic products become gametes. We also examined if positive selection on centromeric histone H3 (CENH3), a protein that can suppress centromere drive, is more frequent in these asymmetric lineages. METHODS: We analysed plant groups with different meiotic modes: asymmetric in gymnosperms and angiosperms, and symmetric in bryophytes, lycophytes and ferns. We selected species based on available CENH3 gene sequences and chromosome size data. Using Ornstein-Uhlenbeck evolutionary models and phylogenetic regressions, we assessed the rates of chromosome size evolution and the frequency of positive selection on CENH3 in these clades. RESULTS: Our analyses showed that clades with asymmetric meiosis have a higher frequency of positive selection on CENH3 and increased rates of chromosome size evolution compared to symmetric clades. CONCLUSIONS: Our findings support the hypothesis that centromere drive accelerates chromosome and genome size evolution, potentially also influencing the process of post-polyploid diploidization. We propose a model which in a single framework helps explain the stability of chromosome size in symmetric lineages (bryophytes, lycophytes and ferns) and its variability in asymmetric lineages (gymnosperms and angiosperms), providing a foundation for future research in plant genome evolution.

CEITEC Central European Institute of Technology Masaryk University Kamenice 5 625 00 Brno Czech Republic

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

Erratum In

Ann Bot. 2025 Feb 19;135(3):603. doi: 10.1093/aob/mcae200. PubMed

See more in PubMed

Akaike H. 1978. A Bayesian analysis of the minimum AIC procedure. Annals of the Institute of Statistical Mathematics 30: 9–14.

Barker MS, Wolf PG.. 2010. Unfurling fern biology in the genomics age. Bioscience 60: 177–185.

Barrington DS. 1993. Ecological and historical factors in fern biogeography. Journal of Biogeography 20: 275–280.

Beaulieu JM, OʹMeara B.. 2022. OUwie: analysis of evolutionary rates in an OU framework. R package version 2.10, https://CRAN.R-project.org/package=OUwie(14 January 2024, date last accessed).

Bennett MD, Smith JB, Ward J, Jenkins G.. 1981. The relationship between nuclear DNA content and centromere volume in higher plants. Journal of Cell Science 47: 91–115. PubMed

Bennetzen JL, Wang H.. 2014. The contributions of transposable elements to the structure, function and evolution of plant genomes. Annual Review of Plant Biology 65: 505–530. PubMed

Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL.. 2005. GenBank. Nucleic Acids Research 33: D34–D38. PubMed PMC

Blackwell PG. 2005. Ornstein–Uhlenbeck process. In: Armitage P, Colton T, eds. Encyclopedia of biostatistics. Hoboken/New Jersey/USA: John Wiley & Sons, Ltd. doi: https://doi.org/10.1002/0470011815.b2a07038 DOI

Boavida LC, McCormick S.. 2010. Gametophyte and sporophyte. In: Encyclopedia of Life Sciences (ELS). Chichester: John Wiley & Sons Ltd. doi: https://doi.org/10.1002/9780470015902.a0002038.pub2 DOI

Bowman JL, Kohchi T, Yamato KT, et al.2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171: 287–304.e15. PubMed

Brown RC, Lemmon BE.. 2013. Sporogenesis in bryophytes: patterns and diversity in meiosis. The Botanical Review 79: 178–280.

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: 536507. PubMed PMC

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

Bureš P, Elliott TL, Veselý P, et al.2024. The global distribution of angiosperm genome size is shaped by climate. New Phytologist 242: 744–759. PubMed

Burnham KP, Anderson DR.. 2002. Model selection and multimodel inference. New York, NY: Springer New York. doi: https://doi.org/10.1007/b97636 DOI

Butler MA, King AA.. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. The American Naturalist 164: 683–695. PubMed

Chen FZ, You LJ, Yang F, et al.2020. CNGBdb: China National Genebank Database. Yi Chuan = Hereditas 42: 799–809. PubMed

Chmatal L, Gabriel SI, Mitsainas GP, et al.2014. Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Current Biology 24: 2295–2300. PubMed PMC

Chmatal L, Schultz RM, Black BE, Lampson MA.. 2017. Cell biology of cheating – transmission of centromeres and other selfish elements through asymmetric meiosis. Progress in Molecular and Subcellular Biology 56: 377–396. PubMed

Choi IY, Kwon EC, Kim NS.. 2020. The C- and G-value paradox with polyploidy, repeatomes, introns, phenomes and cell economy. Genes Genomics 42: 699–714. PubMed

Clark FE, Akera T.. 2021. Unravelling the mystery of female meiotic drive: where we are. Open Biology 11: 210074. PubMed PMC

Clark J, Hidalgo O, Pellicer J, et al.2016. Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny. The New Phytologist 210: 1072–1082. PubMed

Cooper N, Thomas GH, Venditti C, Meade A, Freckleton RP.. 2015. A cautionary note on the use of Ornstein Uhlenbeck models in macroevolutionary studies. Biological Journal of the Linnean Society 118: 64–77. PubMed PMC

Cui J, Zhu Y, Du H, et al.2023. Chromosome-level reference genome of tetraploid Isoetes sinensis provides insights into evolution and adaption of lycophytes. GigaScience 12: giad079. PubMed PMC

Dalal Y, Furuyama T, Vermaak D, Henikoff S.. 2007. Structure, dynamics, and evolution of centromeric nucleosomes. Proceedings of the National Academy of Sciences of the United States of America 104: 15974–15981. PubMed PMC

Daniel A. 2002. Distortion of female meiotic segregation and reduced male fertility in human Robertsonian translocations: consistent with the centromere model of co-evolving centromere DNA/centromeric histone (CENP-A). American Journal of Medical Genetics 111: 450–452. PubMed

Dawe RK. 2022. The maize abnormal chromosome 10 meiotic drive haplotype: a review. Chromosome Research 30: 205–216. PubMed

Du J, Tian Z, Hans CS, et al.2010. Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insights from genome-wide analysis and multi-specific comparison. The Plant Journal 63: 584–598. PubMed

Dudka D, Lampson MA.. 2022. Centromere drive: model systems and experimental progress. Chromosome Research 30: 187–203. PubMed PMC

Elisafenko EA, Evtushenko EV, Vershinin AV.. 2021. The origin and evolution of a two-component system of paralogous genes encoding the centromeric histone CENH3 in cereals. BMC Plant Biology 21: 541. PubMed PMC

Elliott TL, Zedek F, Barrett RL, et al.2022. Chromosome size matters: genome evolution in the cyperid clade. Annals of Botany 130: 999–1014. PubMed PMC

Faizullah L, Morton JA, Hersch-Green EI, Walczyk AM, Leitch AR, Leitch IJ.. 2021. Exploring environmental selection on genome size in angiosperms. Trends in Plant Science 26: 1039–1049. PubMed

Fang Y, Qin X, Liao Q, et al.2022. The genome of homosporous maidenhair fern sheds light on the euphyllophyte evolution and defences. Nature Plants 8: 1024–1037. PubMed PMC

Finseth FR, Nelson TC, Fishman L.. 2021. Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers. PLoS Genetics 17: e1009418. PubMed PMC

Fishman L, Kelly JK.. 2015. Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution 69: 1208–1218. PubMed PMC

Fishman L, Saunders A.. 2008. Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322: 1559–1562. PubMed

Fujiwara T, Liu H, Meza-Torres EI, et al.2023. Evolution of genome space occupation in ferns: linking genome diversity and species richness. Annals of Botany 131: 59–70. PubMed PMC

Gorelick R, Carpinone J, Derraugh LJ.. 2017. No universal differences between female and male eukaryotes: anisogamy and asymmetrical female meiosis. Biological Journal of the Linnean Society 120: 1–21.

Hansen TF. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51: 1341–1351. PubMed

Haufler CH. 2014. Ever since Klekowski: testing a set of radical hypotheses revives the genetics of ferns and lycophytes. American Journal of Botany 101: 2036–2042. PubMed

Henikoff S, Ahmad K, Malik HS.. 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102. PubMed

Hou X, Wang D, Cheng Z, Wang Y, Jiao Y.. 2022. A near-complete assembly of an Arabidopsis thaliana genome. Molecular Plant 15: 1247–1250. PubMed

Houchmandzadeh B, Marko JF, Chatenay D, Libchaber A.. 1997. Elasticity and structure of eukaryote chromosomes studied by micromanipulation and micropipette aspiration. The Journal of Cell Biology 139: 1–12. PubMed PMC

Irvine DV, Amor DJ, Perry J, et al.2004. Chromosome size and origin as determinants of the level of CENP-A incorporation into human centromeres. Chromosome Research 12: 805–815. PubMed

Iwata-Otsubo A, Dawicki-McKenna JM, Akera T, et al.2017. Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Current Biology 27: 2365–2373.e8. PubMed PMC

Katoh K, Rozewicki J, Yamada KD.. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. PubMed PMC

Kessler M. 2010. Biogeography of ferns. In: Mehltreter K, Walker LR, Sharpe JM, eds. Fern ecology. Cambridge: Cambridge University Press, 22–60.

Kinosian SP, Rowe CA, Wolf PG.. 2022. Why do heterosporous plants have so few chromosomes? Frontiers in Plant Science 13: 807302. PubMed PMC

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

Kramer EM, Tayjasanant PA, Cordone B.. 2021. Scaling laws for mitotic chromosomes. Frontiers in Cell and Developmental Biology 9: 684278. PubMed PMC

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: 642661. PubMed PMC

Kubis S, Schmidt T, Heslop-Harrison JS.. 1998. Repetitive DNA elements as a major component of plant genomes. Annals of Botany 82: 45–55.

Kumar S, Suleski M, Craig JE, et al.2022. TimeTree 5: an expanded resource for species divergence times. Molecular Biology and Evolution 39: msac174. PubMed PMC

Lechner M, Findeiß S, Steiner L, Marz M, Stadler PF, Prohaska SJ.. 2011. Proteinortho: Detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12: 124. PubMed PMC

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

Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR.. 2016. Evolutionary mysteries in meiosis. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 371: 20160001. PubMed PMC

Li Z, McKibben MT, Finch GS, Blischak PD, Sutherland BL, Barker MS.. 2021. Patterns and processes of diploidization in land plants. Annual Review of Plant Biology 72: 387–410. PubMed

Lin G, He C, Zheng J, et al.2021. Chromosome-level genome assembly of a regenerable maize inbred line A188. Genome Biology 22: 175. PubMed PMC

Linde AM, Eklund DM, Cronberg N, Bowman JL, Lagercrantz U.. 2021. Rates and patterns of molecular evolution in bryophyte genomes, with focus on complex thalloid liverworts, Marchantiopsida. Molecular Phylogenetics and Evolution 165: 107295. PubMed

Linde AM, Singh S, Bowman JL, Eklund M, Cronberg N, Lagercrantz U.. 2023. Genome evolution in plants: complex thalloid liverworts (Marchantiopsida). Genome Biology and Evolution 15: evad014. PubMed PMC

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

Lisch D. 2013. How important are transposons for plant evolution? Nature Reviews. Genetics 14: 49–61. PubMed

Liu H-M, Ekrt L, Koutecky P, et al.2019. Polyploidy does not control all: lineage-specific average chromosome length constrains genome size evolution in ferns. Journal of Systematics and Evolution 57: 418–430.

Lynch M, Conery JS.. 2003. The origins of genome complexity. Science 302: 1401–1404. PubMed

Lysak MA. 2014. Live and let die: centromere loss during evolution of plant chromosomes. New Phytologist 203: 1082–1089.

Lysak MA. 2022. Celebrating Mendel, McClintock, and Darlington: on end-to-end chromosome fusions and nested chromosome fusions. Plant Cell 34: 2475–2491. PubMed PMC

Maheshwari P. 1937. A critical review of the types of embryo sacs in angiosperms. New Phytologist 36: 359–417.

Maheshwari S, Tan EH, West A, Franklin FC, Comai L, Chan SW.. 2015. Naturally occurring differences in CENH3 affect chromosome segregation in zygotic mitosis of hybrids. PLoS Genetics 11: e1004970. PubMed PMC

Malik HS, Henikoff S.. 2003. Phylogenomics of the nucleosome. Nature Structural Biology 10: 882–891. PubMed

Mandáková T, Lysak MA.. 2018. Post-polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology 42: 55–65. PubMed

Mandrioli M, Manicardi GC.. 2020. Holocentric chromosomes. PLoS Genetics 16: e1008918. PubMed PMC

Marchant DB, Chen G, Cai S, et al.2022. Dynamic genome evolution in a model fern. Nature Plants 8: 1038–1051. PubMed PMC

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

Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL.. 2012. Detecting individual sites subject to episodic diversifying selection. PLoS Genetics 8: e1002764. PubMed PMC

Nakazato T, Barker MS, Rieseberg LH, Gastony GL.. 2008. Evolution of the nuclear genome of ferns and lycophytes. In: Ranker TA, Haufler CH, eds.Biology and evolution of ferns and lycophytes. Cambridge: Cambridge University Press, 175–198.

Nicklas RB. 1965. Chromosome velocity during mitosis as a function of chromosome size and position. Journal of Cell Biology 25: 119–135. PubMed PMC

Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W.. 2023. caper: Comparative Analyses of Phylogenetics and Evolution in R. R package version 1.0.3, https://CRAN.R-project.org/package=caper(14 January 2024, date last accessed).

Otto SP, Goldstein DB.. 2021. Recombination and the evolution of diploidy. Genetics 131: 745–751. PubMed PMC

Paradis E, Schliep K.. 2019. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35: 526–528. PubMed

Pardo-Manuel de Villena F, Sapienza C.. 2001. Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179–1189. PubMed PMC

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. The 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. PubMed PMC

Plačková K, Bureš P, Zedek F.. 2021. Centromere size scales with genome size across Eukaryotes. Scientific Reports 11: 19811. PubMed 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

R Core Team. 2022. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/(14 January 2024, date last accessed).

Renzaglia KS, Rasch EM, Pike LM.. 1995. Estimates of nuclear DNA content in bryophyte sperm cells: phylogenetic considerations. American Journal of Botany 82: 18–25.

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

Roddy AB, Théroux-Rancourt G, Abbo T, et al.2020. The scaling of genome size and cell size limits maximum rates of photosynthesis with implications for ecological strategies. International Journal of Plant Sciences 181: 75–87.

Rosin LF, Mellone BG.. 2017. Centromeres drive a hard bargain. Trends in Genetics 33: 101–117. PubMed PMC

Sandler L, Novitski E.. 1957. Meiotic drive as an evolutionary force. The American Naturalist 91: 105–110.

Santangelo JS, Battlay P, Hendrickson BT, et al.2023. Haplotype-resolved, chromosome-level assembly of white clover (Trifolium repens L., Fabaceae). Genome Biology and Evolution 15: evad146. PubMed PMC

Schnarf K. 1936. Contemporary understanding of embryo-sac development among angiosperms. Botanical Review 2: 565–585.

Shimamoto Y, Maeda YT, Ishiwata S, Libchaber AJ, Kapoor TM.. 2011. Insights into the micromechanical properties of the metaphase spindle. Cell 145: 1062–1074. PubMed PMC

Showman S, Talbert PB, Xu Y, Adeyemi RO, Henikoff S.. 2024. Expansion of human centromeric arrays in cells undergoing break-induced replication. Cell Reports 43: 113851. PubMed PMC

Šmarda P, Bureš P.. 2010. Understanding intraspecific variation in genome size in plants. Preslia 82: 41–61.

Šmarda P, Knápek O, Březinová A, et al.2019. Genome sizes and genomic guanine+cytosine (GC) contents of the Czech vascular flora with new estimates for 1700 species. Preslia 91: 117–142.

Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL.. 2015. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Molecular Biology and Evolution 32: 1342–1353. PubMed PMC

Soto Gomez M, Brown MJM, Pironon S, et al.2024. Genome size is positively correlated with extinction risk in herbaceous angiosperms. New Phytologist 243: 2470–2485. PubMed

Spielman SJ, Weaver S, Shank SD, Magalis BR, Li M, Kosakovsky Pond SL.. 2019. Evolution of viral genomes: interplay between selection, recombination, and other forces. In: Anisimova M, ed. Evolutionary genomics: statistical and computational methods. New York: Humana New York, 427–468. doi: https://doi.org/10.1007/978-1-4939-9074-0_14 PubMed DOI

Stenøien HK. 2008. Slow molecular evolution in 18S rDNA, rbcL and nad5 genes of mosses compared with higher plants. Journal of Evolutionary Biology 21: 566–571. PubMed

Szövényi P, Ricca M, Hock Z, Shaw JA, Shimizu KK, Wagner A.. 2013. Selection is no more efficient in haploid than in diploid life stages of an angiosperm and a moss. Molecular Biology and Evolution 30: 1929–1939. PubMed

Szövényi P, Gunadi A, Li FW.. 2021. Charting the genomic landscape of seed-free plants. Nature Plants 7: 554–565. PubMed

Talbert P, Henikoff S.. 2022. Centromere drive: chromatin conflict in meiosis. Current Opinion in Genetics and Development 77: 102005. PubMed

Talbert PB, Bayes JJ, Henikoff S.. 2009. Evolution of centromeres and kinetochores: a two-part fugue. In: De Wulf P, Earnshaw W, eds. The kinetochore. New York: Springer, 193–229. doi: https://doi.org/10.1007/978-0-387-69076-6_7 DOI

Tenaillon MI, Hollister JD, Gaut BS.. 2010. A triptych of the evolution of plant transposable elements. Trends in Plant Science 15: 471–478. PubMed

Uhlenbeck GE, Ornstein LS.. 1930. On the theory of the Brownian motion. Physical Review 36: 823–841.

Ui TJ, Hussey RG, Roger RP.. 1984. Stokes drag on a cylinder in axial motion. Physics of Fluids 27: 787–795.

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

Wagenmakers EJ, Farrell S.. 2004. AIC model selection using Akaike weights. Psychonomic Bulletin & Review 11: 192–196. PubMed

Wagner WH, Wagner FS.. 1980. Polyploidy in pteridophytes. In: Lewis WH, ed. Polyploidy: biological relevance. New York: Plenum Press, 199–214. doi: https://doi.org/10.1007/978-1-4613-3069-1_11 DOI

Wang N, Liu J, Ricci WA, Gent JI, Dawe RK.. 2021. Maize centromeric chromatin scales with changes in genome size. Genetics 217: iyab020. PubMed PMC

Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Kosakovsky Pond SL.. 2018. Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Molecular Biology and Evolution 35: 773–777. PubMed PMC

Wickham H. 2016. Programming with ggplot2. In: ggplot2. Use R!. Cham: Springer, 241–253. doi: https://doi.org/10.1007/978-3-319-24277-4_12 DOI

Williams CG. 2009. Conifer reproductive biology. New York/New York/USA: Springer. doi: https://doi.org/10.1007/978-1-4020-9602-0 DOI

Wu T, Lane SIR, Morgan SL, Jones KT.. 2018. Spindle tubulin and MTOC asymmetries may explain meiotic drive in oocytes. Nature Communications 9: 2952. PubMed PMC

Yu G, Smith D, Zhu H, Guan Y, Tsan-Yuk Lam T.. 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.

Záveská Drábková L. 2013. A survey of karyological phenomena in the Juncaceae with emphasis on chromosome number variation and evolution. The Botanical Review 79: 401–446.

Zedek F, Bureš P.. 2016a. CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model. Scientific Reports 6: 33308. PubMed PMC

Zedek F, Bureš P.. 2016b. Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Annals of Botany 118: 1347–1352. PubMed PMC

Zedek F, Bureš P.. 2018. Holocentric chromosomes: from tolerance to fragmentation to colonization of the land. Annals of Botany 121: 9–16. PubMed PMC

Zhang H, Dawe RK.. 2012. Total centromere size and genome size are strongly correlated in ten grass species. Chromosome Research 20: 403–412. PubMed PMC

Zhou X, Peng T, Zeng Y, et al.2023. Chromosome-level genome assembly of Niphotrichum japonicum provides new insights into heat stress responses in mosses. Frontiers in Plant Science 14: 1271357. PubMed PMC