Centromere drive model describes an evolutionary process initiated by centromeric repeats expansion, which leads to the recruitment of excess kinetochore proteins and consequent preferential segregation of an expanded centromere to the egg during female asymmetric meiosis. In response to these selfish centromeres, the histone protein CenH3, which recruits kinetochore components, adaptively evolves to restore chromosomal parity and counter the detrimental effects of centromere drive. Holocentric chromosomes, whose kinetochores are assembled along entire chromosomes, have been hypothesized to prevent expanded centromeres from acquiring a selective advantage and initiating centromere drive. In such a case, CenH3 would be subjected to less frequent or no adaptive evolution. Using codon substitution models, we analyzed 36 CenH3 sequences from 35 species of the holocentric family Cyperaceae. We found 10 positively selected codons in the CenH3 gene [six codons in the N-terminus and four in the histone fold domain (HFD)] and six branches of its phylogeny along which the positive selection occurred. One of the positively selected codons was found in the centromere targeting domain (CATD) that directly interacts with DNA and its mutations may be important in centromere drive suppression. The frequency of these positive selection events was comparable to the frequency of positive selection in monocentric clades with asymmetric female meiosis. Taken together, these results suggest that preventing centromere drive is not the primary adaptive role of holocentric chromosomes, and their ability to suppress it likely depends on their kinetochore structure in meiosis.

Department of Botany and Zoology Faculty of Science Masaryk University Brno Czechia

Zobrazit více v PubMed

Akera T., Chmátal L., Trimm E., Yang K., Aonbangkhen C., Chenoweth D., et al. . (2017). Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358, 668–672. 10.1126/science.aan0092, PMID: PubMed DOI PMC

Akera T., Trimm E., Lampson M. A. (2019). Molecular strategies of meiotic cheating by selfish centromeres. Cell 178, 1132–1144. 10.1016/j.cell.2019.07.001, PMID: PubMed DOI PMC

Baez M., Kuo Y. T., Dias Y., Souza T., Boudichevskaia A., Fuchs J., 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. 10.1007/s00412-020-00745-6, PMID: PubMed DOI PMC

Braselton J. P. (1971). The ultrastructure of the non-localized kinetochores of Luzula and Cyperus. Chromosoma 36, 89–99. 10.1007/BF00326424 DOI

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

Bureš P., Zedek F., Marková M. (2013). “Holocentric chromosomes” in Plant genome diversity. Vol. 2. eds. Greilhuber J., Dolezel J., Wendel J. (Vienna: Springer; ), 187–208.

Cabral G., Marques A., Schubert V., Pedrosa-Harand A., Schlögelhofer P. (2014). Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes. Nat. Commun. 5:5070. 10.1038/ncomms6070, PMID: PubMed DOI PMC

Cortes-Silva N., Ulmer J., Kiuchi T., Hsieh E., Cornilleau G., Ladid I., et al. . (2020). CenH3-independent kinetochore assembly in Lepidoptera requires CCAN, including CENP-T. Curr. Biol. 30, 561.e10–572.e10. 10.1016/j.cub.2019.12.014, PMID: PubMed DOI

Dalal Y., Furuyama T., Vermaak D., Henikoff S. (2007). Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl. Acad. Sci. U. S. A. 104, 15974–15981. 10.1073/pnas.0707648104, PMID: PubMed DOI PMC

Drinnenberg I. A., deYoung D., Henikoff S., Malik H. S. (2014). Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife 3:e03676. 10.7554/eLife.03676, PMID: PubMed DOI PMC

Elde N. C., Roach K. C., Yao M. C., Malik H. S. (2011). Absence of positive selection on centromeric histones in Tetrahymena suggests unsuppressed centromere: drive in lineages lacking male meiosis. J. Mol. Evol. 72, 510–520. 10.1007/s00239-011-9449-0, PMID: PubMed DOI PMC

Escudero M., Marquez-Corro J. I., Hipp A. L. (2016). The phylogenetic origins and evolutionary history of holocentric chromosomes. Syst. Bot. 41, 580–585. 10.1600/036364416X692442 DOI

Finseth F. R., Nelson T. C., Fishmam L. (2020). Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers. bioRxiv [Preprint]. Available at: https://www.biorxiv.org/content/ 10.1101/2020.09.11.293597v1 (Accessed December 16, 2020). PubMed DOI PMC

Fishman L., Kelly J. K. (2015). Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution 69, 1208–1218. 10.1111/evo.12661, PMID: PubMed DOI PMC

Furness C. A., Rudall P. J. (2011). Selective microspore abortion correlated with aneuploidy: an indication of meiotic drive. Sex. Plant Reprod. 24, 1–8. 10.1007/s00497-010-0150-z, PMID: PubMed DOI

Gassmann R., Rechtsteiner A., Yuen K. W., Muroyama A., Egelhofer T., Gaydos L., et al. . (2012). An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 484, 534–537. 10.1038/nature10973, PMID: PubMed DOI PMC

Guerra M., Ribeiro T., Felix L. P. (2019). Monocentric chromosomes in Juncus (Juncaceae) and implications for the chromosome evolution of the family. Bot. J. Linn. Soc. 191, 475–483. 10.1093/botlinnean/boz065 DOI

Hakansson A. (1954). Meiosis and pollen mitosis in X-rayed and untreated spikelets of Eleocharis palustris. Hereditas 40, 325–345. 10.1111/j.1601-5223.1954.tb02976.x DOI

Heckmann S., Jankowska M., Schubert V., Kumke K., Ma W., Houben A. (2014). Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans. Nat. Commun. 5:4979. 10.1038/ncomms5979, PMID: PubMed DOI PMC

Heckmann S., Macas J., Kumke K., Fuchs J., Schubert V., Ma L., et al. . (2013). The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J. 73, 555–565. 10.1111/tpj.12054, PMID: PubMed DOI

Henikoff S., Ahmad K., Malik H. S. (2001). The centromere paradox: stable inheritance with rapidly evolving dna. Science 293, 1098–1102. 10.1126/science.1062939, PMID: PubMed DOI

Iwata-Otsubo A., Dawicki-McKenna J. M., Akera T., Falk S. J., Chmátal L., Yang K., et al. . (2017). Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Curr. Biol. 27, 2365.e8–2373.e8. 10.1016/j.cub.2017.06.069, PMID: PubMed DOI PMC

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

Kolodin P., Cempírková H., Bureš P., Horová L., Veleba A., Francová J., et al. . (2018). Holocentric chromosomes may be an apomorphy of Droseraceae. Plant Syst. Evol. 304, 1289–1296. 10.1007/s00606-018-1546-8 DOI

Kursel L. E., Malik H. S. (2018). The cellular mechanisms and consequences of centromere drive. Curr. Opin. Cell Biol. 52, 58–65. 10.1016/j.ceb.2018.01.011, PMID: PubMed DOI PMC

Lampson M. A., Black B. E. (2017). Cellular and molecular mechanisms of centromere drive. Cold Spring Harb. Symp. Quant. Biol. 82, 249–257. 10.1101/sqb.2017.82.034298, PMID: PubMed DOI PMC

Malik H. S., Henikoff S. (2009). Major evolutionary transitions in centromere complexity. Cell 138, 1067–1082. 10.1016/j.cell.2009.08.036, PMID: PubMed DOI

Mandrioli M., Manicardi G. C. (2012). Unlocking holocentric chromosomes: new perspectives from comparative and functional genomics? Curr. Genomics 13, 343–349. 10.2174/138920212801619250, PMID: PubMed DOI PMC

Mandrioli M., Manicardi G. C. (2020). Holocentric chromosomes. PLoS Genet. 16:e1008918. 10.1371/journal.pgen.1008918, PMID: PubMed DOI PMC

Marques A., Pedrosa-Harand A. (2016). Holocentromere identity: from the typical mitotic linear structure to the great plasticity of meiotic holocentromeres. Chromosoma 125, 669–681. 10.1007/s00412-016-0612-7, PMID: PubMed DOI

Marques A., Ribeiro T., Neumann P., Macas J., Novák P., Schubert V., et al. . (2015). Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc. Natl. Acad. Sci. U. S. A. 112, 13633–13638. 10.1073/pnas.1512255112, PMID: PubMed DOI PMC

Marques A., Schubert V., Houben A., Pedrosa-Harand A. (2016). Restructuring of holocentric centromeres during meiosis in the plant Rhynchospora pubera. Genetics 204, 555–568. 10.1534/genetics.116.191213, PMID: PubMed DOI PMC

Márquez-Corro J. I., 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). Mol. Phylogenet. Evol. 135, 203–209. 10.1016/j.ympev.2019.03.006, PMID: PubMed DOI

Melters D. P., Paliulis L. V., Korf I. F., Chan S. W. (2012). Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosom. Res. 20, 579–593. 10.1007/s10577-012-9292-1, PMID: PubMed DOI

Murrell B., Wertheim J. O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S. L. (2012). Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8:e1002764. 10.1371/journal.pgen.1002764, PMID: PubMed DOI PMC

Neumann P., Oliveira L., Čížková J., Jang T. S., Klemme S., Novák P., et al. . (2020). Impact of parasitic lifestyle and different types of centromere organization on chromosome and genome evolution in the plant genus Cuscuta. New Phytol. 229, 2365–2377. 10.1111/nph.17003, PMID: PubMed DOI

Oliveira L., Neumann P., Jang T. S., Klemme S., Schubert V., Koblížková A., et al. . (2020). Mitotic spindle attachment to the holocentric chromosomes of Cuscuta europaea does not correlate with the distribution of CENH3 chromatin. Front. Plant Sci. 10:1799. 10.3389/fpls.2019.01799, PMID: PubMed DOI PMC

Palfalvi G., Hackl T., Terhoeven N., Shibata T. F., Nishiyama T., Ankenbrand M., et al. . (2020). Genomes of the venus flytrap and close relatives unveil the roots of plant carnivory. Curr. Biol. 30, 2312.e5–2320.e5. 10.1016/j.cub.2020.04.051, PMID: PubMed DOI PMC

Pazy B., Plitmann U. (1994). Holocentric chromosome behaviour in Cuscuta (Cuscutaceae). Plant Syst. Evol. 191, 105–109. 10.1007/BF00985345 DOI

Plohl M., Meštrović N., Mravinac B. (2014). Centromere identity from the DNA point of view. Chromosoma 123, 313–325. 10.1007/s00412-014-0462-0, PMID: PubMed DOI PMC

Redelings B. D., Suchard M. A. (2005). Joint bayesian estimation of alignment and phylogeny. Syst. Biol. 54, 401–418. 10.1080/10635150590947041, PMID: PubMed DOI

Rice A., Glick L., Abadi S., Einhorn M., Kopelman N. M., Salman-Minkov A., et al. . (2015). The chromosome counts database (CCDB)—a community resource of plant chromosome numbers. New Phytol. 206, 19–26. 10.1111/nph.13191, PMID: PubMed DOI

Rocha D. M., Marques A., Andrade C. G., Guyot R., Chaluvadi S. R., Pedrosa-Harand A., et al. . (2016). Developmental programmed cell death during asymmetric microsporogenesis in holocentric species of Rhynchospora (Cyperaceae). J. Exp. Bot. 67, 5391–5401. 10.1093/jxb/erw300, PMID: PubMed DOI PMC

San Martin J. A., de Jesus Andrade C. G., Mastroberti A. A., de Araújo Mariath J. E., Vanzela A. L. (2013). Asymmetric cytokinesis guide the development of pseudomonads in Rhynchospora pubera (Cyperaceae). Cell Biol. Int. 37, 203–212. 10.1002/cbin.10028, PMID: PubMed DOI

Semmouri I., Bauters K., Léveillé-Bourret É., Starr J. R., Goetghebeur P., Larridon I. (2019). Phylogeny and systematics of cyperaceae, the evolution and importance of embryo morphology. Bot. Rev. 85, 1–39. 10.1007/s12229-018-9202-0 DOI

Smith M. D., Wertheim J. O., Weaver S., Murrell B., Scheffler K., Kosakovsky Pond S. L. (2015). Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol. Biol. Evol. 32, 1342–1353. 10.1093/molbev/msv022, PMID: PubMed DOI PMC

Spielman S. J., Weaver S., Shank S. D., Magalis B. R., Li M., Kosakovsky Pond S. L. (2019). “Evolution of viral genomes: interplay between selection, recombination, and other forces” in Evolutionary genomics. Methods in Molecular Biology. Vol. 1910. ed. Anisimova M. (New York: Humana; ), 427–468. PubMed

Talbert P. B., Bayes J. J., Henikoff S. (2009). “Evolution of centromeres and kinetochores: a two-part fugue” in The Kinetochore. eds. de Wulf P., Earnshaw W. (New York: Springer; ), 193–229.

The Angiosperm Phylogeny Group (2016). An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20. 10.1111/boj.12385 DOI

Weaver S., Shank S. D., Spielman S. J., Li M., Muse S. V., Kosakovsky Pond S. L. (2018). Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol. Biol. Evol. 35, 773–777. 10.1093/molbev/msx335, PMID: PubMed DOI PMC

Yang Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591. 10.1093/molbev/msm088, PMID: PubMed DOI

Zedek F., Bureš P. (2012). Evidence for centromere drive in the holocentric chromosomes of Caenorhabditis. PLoS One 7:e30496. 10.1371/journal.pone.0030496, PMID: PubMed DOI PMC

Zedek F., Bureš P. (2016a). Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Ann. Bot. 118, 1347–1352. 10.1093/aob/mcw186, PMID: PubMed DOI PMC

Zedek F., Bureš P. (2016b). CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model. Sci. Rep. 6:33308. 10.1038/srep33308, PMID: PubMed DOI PMC

Zedek F., Bureš P. (2018). Holocentric chromosomes: from tolerance to fragmentation to colonization of the land. Ann. Bot. 121, 9–16. 10.1093/aob/mcx118, PMID: PubMed DOI PMC

Zedek F., Bureš P. (2019). Pest arthropods with holocentric chromosomes are more resistant to sterilizing ionizing radiation. Radiat. Res. 191, 255–261. 10.1667/RR15208.1, PMID: PubMed DOI

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

Zhang T., Talbert P. B., Zhang W., Wu Y., Yang Z., Henikoff J. G., et al. . (2013). The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc. Natl. Acad. Sci. U. S. A. 110, E4875–E4883. 10.1073/pnas.1319548110, PMID: PubMed DOI PMC

Centromere drive may propel the evolution of chromosome and genome size in plants

Chromosome size matters: genome evolution in the cyperid clade

Centromere size scales with genome size across Eukaryotes