Holocentric chromosomes

Autoři: Mauro Mandrioli aff001;  Gian Carlo Manicardi aff001
Působiště autorů: Dipartimento di Scienze della Vita, Università di Modena e Reggio Emilia, Modena, Italy aff001
Vyšlo v časopise: Holocentric chromosomes. PLoS Genet 16(7): e1008918. doi:10.1371/journal.pgen.1008918
Kategorie: Topic Page
doi: 10.1371/journal.pgen.1008918


Holocentric chromosomes possess multiple kinetochores along their length rather than the single centromere typical of other chromosomes [1]. They have been described for the first time in cytogenetic experiments dating from 1935 and, since this first observation, the term holocentric chromosome has referred to chromosomes that: i. lack the primary constriction corresponding to centromere observed in monocentric chromosomes [2]; ii. possess multiple kinetochores dispersed along the chromosomal axis so that microtubules bind to chromosomes along their entire length and move broadside to the pole from the metaphase plate [3]. These chromosomes are also termed holokinetic, because, during cell division, chromatids move apart in parallel and do not form the classical V-shaped figures typical of monocentric chromosomes [46]. Holocentric chromosomes evolved several times during both animal and plant evolution and are currently reported in about eight hundred diverse species, including plants, insects, arachnids and nematodes [7,8]. As a consequence of their diffuse kinetochores, holocentric chromosomes may stabilize chromosomal fragments favouring karyotype rearrangements [9,10]. However, holocentric chromosome may also present limitations to crossing over causing a restriction of the number of chiasma in bivalents [11] and may cause a restructuring of meiotic divisions resulting in an inverted meiosis [12].

Klíčová slova:

Caenorhabditis elegans – Centromeres – Evolutionary genetics – Chromatids – Chromosome structure and function – Karyotypes – Meiosis – Moths and butterflies


1. Schrader F. Notes an the Mitotic Behavior of Long Chromosomes. Cytologia. 1935;6(4): 422–430. doi: 10.1508/cytologia.6.422

2. Mandrioli M, Manicardi GC. Analysis of insect holocentric chromosomes by atomic force microscopy. Hereditas. 2003;138(2): 129–132. doi: 10.1034/j.1601-5223.2003.01661.x 12921164

3. Hughes-Schrader S, Schrader F. The kinetochore of the hemiptera. Chromosoma. 1961;12(1): 327–350. doi: 10.1007/bf00328928 13716663

4. Wrensch DL, Kethley JB, Norton RA. Cytogenetics of Holokinetic Chromosomes and Inverted Meiosis: Keys to the Evolutionary Success of Mites, with Generalizations on Eukaryotes. In: Houck MA, editor. Mites. Boston: Springer; 1994. pp. 282–343. doi: 10.1007/978-1-4615-2389-5%5F11

5. White MJD. Animal cytology and evolution. 3rd ed. Cambridge [England]: University Press; 1973.

6. Mandrioli M, Manicardi GC. Unlocking Holocentric Chromosomes: New Perspectives from Comparative and Functional Genomics? Curr Genomics. 2012;13(5):343–349. doi: 10.2174/138920212801619250 23372420

7. Melters DP, Paliulis LV, Korf IF, Chan SWL. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 2012;20(5): 579–593. doi: 10.1007/s10577-012-9292-1 22766638

8. Benavente R. Holocentric chromosomes of arachnids: Presence of kinetochore plates during meiotic divisions. Genetica. 1982;59(1): 23–27. doi: 10.1007/bf00130811

9. Monti V, Lombardo G, Loxdale HD, Manicardi GC, Mandrioli M. Continuous occurrence of intra-individual chromosome rearrangements in the peach potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genetica 2012;140(1–3): 93–103. doi: 10.1007/s10709-012-9661-x 22644285

10. Manicardi GC, Nardelli A, Mandrioli M. Fast chromosomal evolution and karyotype instability: recurrent chromosomal rearrangements in the peach potato aphid Myzus persicae (Hemiptera: Aphididae). Biol J Linn Soc Lond. 2015;116 (3): 519–529. doi: 10.1111/bij.12621

11. Nokkala S, Kuznetsova VG, Maryanska-Nadachowska A, Nokkala C. Holocentric chromosomes in meiosis. I. Restriction of the number of chiasmata in bivalents. Chromosome Res. 2004;12(7):733–739. doi: 10.1023/B:CHRO.0000045797.74375.70 15505408

12. Lukhtanov VA, Dincă V, Friberg M, Šíchová J, Olofsson M, Vila R, et al. Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. Proc Natl Acad Sci USA. 2018;115 (41): E9610–E9619. doi: 10.1073/pnas.1802610115 30266792

13. Bureš P, Zedek F, Marková M. Holocentric Chromosomes. In: Greilhuber J, Dolezel J, Wendel J, editors. Plant Genome Diversity Volume 2. Vienna: Springer; 2012. pp. 187–208. doi: 10.1007/978-3-7091-1160-4%5F12

14. Escudero M, Márquez-Corro JI, Hipp AL. The Phylogenetic Origins and Evolutionary History of Holocentric Chromosomes. Syst Bot. 2016;41(3): 580–585. doi: 10.1600/036364416x692442

15. Nagaki K, Kashihara K, Murata M. Visualization of Diffuse Centromeres with Centromere-Specific Histone H3 in the Holocentric Plant Luzula nivea. Plant Cell. 2005;17 (7): 1886–1893. doi: 10.1105/tpc.105.032961 15937225

16. Howe M, McDonald KL, Albertson DG, Meyer BJ. Him-10 Is Required for Kinetochore Structure and Function on Caenorhabditis elegans Holocentric Chromosomes. J Cell Biol. 2001;153 (6): 1227–1238. doi: 10.1083/jcb.153.6.1227 11402066

17. Zedek F, Bureš P. Evidence for Centromere Drive in the Holocentric Chromosomes of Caenorhabditis. PLoS ONE. 2012;7(1): e30496. doi: 10.1371/journal.pone.0030496 22291967

18. Ogawa K. Chromosome Studies in the Myriapoda. Jpn J Genet. 1953;28 (1): 12–18. doi: 10.1266/jjg.28.12

19. Richards RI. Fragile and unstable chromosomes in cancer: causes and consequences. Trends Genet 2001;17(6): 339–345. doi: 10.1016/s0168-9525(01)02303-4 11377796

20. Freudenreich CH. Chromosome fragility: molecular mechanisms and cellular consequences. Front Biosci. 2007;12(12): 4911. doi: 10.2741/2437 17569619

21. Manicardi GC, Mandrioli M, Blackman RL. The cytogenetic architecture of the aphid genome. Biol Rev Camb Philos Soc. 2014;90 (1): 112–125. doi: 10.1111/brv.12096 24593177

22. Monti V, Mandrioli M, Rivi M, Manicardi GC. The vanishing clone: karyotypic evidence for extensive intraclonal genetic variation in the peach potato aphid, Myzus persicae (Hemiptera: Aphididae). Biol J Linn Soc Lond. 2011;105(2): 350–358. doi: 10.1111/j.1095-8312.2011.01812.x

23. Monti V, Giusti M, Bizzaro D, Manicardi GC, Mandrioli M. Presence of a functional (TTAGG) n telomere-telomerase system in aphids. Chromosome Res. 2011;19(5): 625–633. doi: 10.1007/s10577-011-9222-7 21667174

24. Mandrioli M, Borsatti F. Analysis of heterochromatic epigenetic markers in the holocentric chromosomes of the aphid Acyrthosiphon pisum. Chromosome Res. 2007;15(8):1015–1022. doi: 10.1007/s10577-007-1176-4 18004669

25. Marec F, Tothová A, Sahara K, Traut W. Meiotic pairing of sex chromosome fragments and its relation to atypical transmission of a sex-linked marker in Ephestia kuehniella (Insecta: Lepidoptera). Heredity. 2001;87 (6): 659–671. doi: 10.1046/j.1365-2540.2001.00958.x 11903561

26. Hill J, Rastas P, Hornett EA, Neethiraj R, Clark N, Morehouse N, et al. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Sci Adv. 2019;5(6): eaau3648. doi: 10.1126/sciadv.aau3648 31206013

27. d'Alençon E, Sezutsu H, Legeai F, Permal E, Bernard-Samain S, Gimenez, S, et al. Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci USA. 2010;107(17): 7680–7685. doi: 10.1073/pnas.0910413107 20388903

28. Lukhtanov VA, Dincă V, Talavera G, Vila R. Unprecedented within-species chromosome number cline in the Wood White butterfly Leptidea sinapis and its significance for karyotype evolution and speciation. BMC Evol Biol. 2011;11(1). doi: 10.1186/1471-2148-11-109 21507222

29. Drinnenberg IA, deYoung D, Henikoff S, Malik HS. Author response: Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. eLife 2014;3:e03676. doi: 10.7554/elife.03676.020

30. Mutafova T, Dimitrova Y, Komandarev S. The karyotype of four Trichinella species. Parasitenkd. 1982;67(1): 115–120. doi: 10.1007/bf00929519 7072318

31. Špakulová M, Králová I, Cutillas C. Studies on the karyotype and gametogenesis in Trichuris muris. J Helminthol. 1994;68(1):67–72. doi: 10.1017/s0022149x0001350x 8006389

32. Post R. The chromosomes of the filariae. Filaria J. 2005;4(1):10. doi: 10.1186/1475-2883-4-10 16266430

33. Pimpinelli S, Goday C. Unusual kinetochores and chromatin diminution in Parascaris. Trends Genet. 1989;5: 310–315. doi: 10.1016/0168-9525(89)90114-5 2686123

34. Dernburg AF. Here, There, and Everywhere. J Cell Biol. 2001;153 (6): F33–F38. doi: 10.1083/jcb.153.6.f33 11402076

35. Maddox PS, Oegema K, Desai A, Cheeseman IM. "Holo"er than thou: Chromosome segregation and kinetochore function in C. elegans. Chromosome Res. 2004;12(6): 641–653. doi: 10.1023/B:CHRO.0000036588.42225.2f 15289669

36. Albertson DG, Thomson JN. The kinetochores of Caenorhabditis elegans. Chromosoma 1982;86(3): 409–428. doi: 10.1007/BF00292267 7172865

37. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A. Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 2005;7(12):1248–1255. doi: 10.1038/ncb1331 16273096

38. Subirana JA, Messeguer X. A Satellite Explosion in the Genome of Holocentric Nematodes. PLoS ONE. 2013;8(4):e62221. doi: 10.1371/journal.pone.0062221 23638010

39. Godward, Maud B. E. Chromosomes of the Algae. Edward Arnold; 1966. ISBN 9780713120585

40. Kolodin P, Cempírkova H, Bures P, Horova L, Veleba A, Francova J. Holocentric chromosomes may be an apomorphy of Droseraceae. Plant Syst Evol. 2018; 304: 1289–1296.

41. Luceño M, Vanzela ALL, Guerra M. Cytotaxonomic studies in Brazilian Rhynchospora (Cyperaceae), a genus exhibiting holocentric chromosomes. Can J Bot. 1998;76 (3): 440–449. doi: 10.1139/b98-013

42. Kuta E, Bohanec B, Dubas E, Vizintin L, Przywara L. Chromosome and nuclear DNA study on Luzula—a genus with holokinetic chromosomes. Genome. 2004;47(2): 246–256. doi: 10.1139/g03-121 15060577

43. Kynast RG, Joseph JA, Pellicer J, Ramsay MM, Rudall PJ. Chromosome behavior at the base of the angiosperm radiation: Karyology of Trithuria submersa (Hydatellaceae, Nymphaeales). Am J Bot. 2014;101(9): 1447–1455. doi: 10.3732/ajb.1400050 25253705

44. Zedek F, Veselý P, Horová L, Bureš P. Flow cytometry may allow microscope-independent detection of holocentric chromosomes in plants. Sci Rep. 2016;6(1). doi: 10.1038/srep27161 27255216

45. Haizel T, Lim YK, Leitch AR, Moore G. Molecular analysis of holocentric centromeres of Luzula species. Cytogenet Genome Res. 2005;109(1–3):134–143. doi: 10.1159/000082392 15753569

46. Zedek F, Bureš P. Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Ann Bot. 2016;118(7): 1347–1352. doi: 10.1093/aob/mcw186 27616209

47. Madej A, Kuta E. Holokinetic chromosomes of Luzula luzuloides [Juncaceae in callus culture"] (in English). Acta Biol Crac Ser Bot. 2001;(43).

48. Nordenskiöld H., Hedda (1961), "Tetrad Analysis and the Course of Meiosis in Three Hybrids of Luzula Campestris" (in en), Hereditas 1961;47(2): 203–238. doi: 10.1111/j.1601-5223.1961.tb01771.x, ISSN 1601-5223, https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1601-5223.1961.tb01771.x

49. Escudero M, Vargas P, Arens P, Ouborg NJ, Luceño M. The east-west-north colonization history of the Mediterranean and Europe by the coastal plant Carex extensa (Cyperaceae). Mol Ecol. 2010;19(2):352–370. doi: 10.1111/j.1365-294X.2009.04449.x 20002603

50. Hipp AL, Rothrock PE, Roalson EH. The Evolution of Chromosome Arrangements in Carex (Cyperaceae). Bot Rev. 2008;75(1):96–109. doi: 10.1007/s12229-008-9022-8

51. Escudero M, Weber JA, Hipp AL. Species coherence in the face of karyotype diversification in holocentric organisms: the case of a cytogenetically variable sedge (Carex scoparia, Cyperaceae). Ann Bot. 2013;112(3):515–526. doi: 10.1093/aob/mct119 23723260

52. Wanner G, Schroeder-Reiter E, Ma W, Houben A, Schubert V. The ultrastructure of mono- and holocentric plant centromeres: an immunological investigation by structured illumination microscopy and scanning electron microscopy. Chromosoma. 2015;124 (4): 503–517. doi: 10.1007/s00412-015-0521-1 26048589

53. Cuacos M, Franklin FCH, Heckmann S. Atypical centromeres in plants—what they can tell us. Front Plant Sci. 2015;6:913. doi: 10.3389/fpls.2015.00913 26579160

54. Jankowska M, Fuchs J, Klocke E, Fojtová M, Polanská P, Fajkus J, et al. Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma. 2015;124(4):519–528. doi: 10.1007/s00412-015-0524-y 26062516

55. Bogdanov YF. Inverted meiosis and its place in the evolution of sexual reproduction pathways. Russ J Genet. 2016;52(5):473–490. doi: 10.1134/s1022795416050033

56. Viera A, Page J, Rufas JS. Inverted Meiosis: The True Bugs as a Model to Study. In: Benavente R, Volff J-N, editors. Meiosis. Basel: Karger; 2008. pp. 137–156, doi: 10.1159/000166639 18948713

57. Vanzela ALL, Cuadrado A, Guerra M. Localization of 45S rDNA and telomeric sites on holocentric chromosomes of Rhynchospora tenuis (Cyperaceae). Genet Mol Biol. 2003;26(2):199–201. doi: 10.1590/S1415-47572003000200014

58. Martinez-Perez E, Schvarzstein M, Barroso C, Lightfoot J, Dernburg AF, Villeneuve AM. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 2008;22(20): 2886–2901. doi: 10.1101/gad.1694108 18923085

59. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, et al. The mosaic genome of warm-blooded vertebrates. Science. 1985;228(4702):953–958. doi: 10.1126/science.4001930 4001930

60. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 2011;479(7374): 487–492. doi: 10.1038/nature10640 22113690

61. The C. elegans Sequencing Consortium. Genome Sequence of the Nematode C. elegans: A Platform for Investigating Biology. Science 1998;282(5396):2012–2018. doi: 10.1126/science.282.5396.2012 9851916

62. Manicardi GC, Mandrioli M, Bizzaro D, Bianchi U. Patterns of DNase I sensitivity in the holocentric chromosomes of the aphid Megoura viciae. Genome. 1998;41(2):169–172. doi: 10.1139/gen-41-2-169

63. Márquez-Corro JI, Escudero M, Luceño M. Do holocentric chromosomes represent an evolutionary advantage? A study of paired analyses of diversification rates of lineages with holocentric chromosomes and their monocentric closest relatives. Chromosome Res. 2017;26(3):139–152. doi: 10.1007/s10577-017-9566-8 29043597

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