Plant Systematics and Evolution

, Volume 304, Issue 10, pp 1289–1296 | Cite as

Holocentric chromosomes may be an apomorphy of Droseraceae

  • Pavel Kolodin
  • Hana Cempírková
  • Petr Bureš
  • Lucie Horová
  • Adam Veleba
  • Jana Francová
  • Lubomír Adamec
  • František ZedekEmail author
Short Communication


Holocentric chromosomes have evolved in various plant and animal taxa, which suggests they may confer a selective advantage in certain conditions, yet their adaptive potential has scarcely been studied. One of the reasons may reside in our insufficient knowledge of the phylogenetic distribution of holocentric chromosomes across eukaryotic phylogeny. In the present study, we focused on Droseraceae, a carnivorous plant family with an unknown chromosomal structure in monotypic genera Dionaea and Aldrovanda, and a closely related monotypic family Drosophyllaceae. We used flow cytometry to detect holocentric chromosomes by measuring changes in the ratio of the number of G2 nuclei to the number of G1 nuclei in response to gamma irradiation and determined chromosomal structures in Aldrovanda vesiculosa, Dionaea muscipula, Drosera tokaiensis, and Drosera ultramafica from Droseraceae and Drosophyllum lusitanicum from Drosophyllaceae. We confirmed monocentric chromosomes in D. lusitanicum and detected holocentric chromosomes in all four Droseraceae. Our novel finding of holocentric chromosomes in monotypic genera Aldrovanda and Dionaea suggests that all Droseraceae may be holocentric, but to confirm that further research is needed due to previously reported conflicting results in Drosera rotundifolia.


Aldrovanda Dionaea Drosera Drosophyllum Flow cytometry Gamma irradiation 



We would like to thank Michal Kouba for providing in vitro cultures of Drosera ultramafica and David Švarc for providing the seeds of Drosophyllum lusitanicum. We are grateful to Luboš Maťaš and Josef Hladík from Bioster Company for their assistance with gamma irradiation. This work was supported by the Czech Science Foundation, Grant No. GA17-21053S, and for LA by the Project RVO 67985939.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights statement

No human participants or animals were involved in this research.

Supplementary material

606_2018_1546_MOESM1_ESM.pdf (634 kb)
Online Resource 1. Examples of flow histograms with the calculations of the G2/G1 ratios (PDF 634 kb)
606_2018_1546_MOESM2_ESM.pdf (764 kb)
Online Resource 2. G2/G1 ratios of all analyzed samples (PDF 764 kb)


  1. Adamec L (1997) How to grow Aldrovanda vesiculosa outdoors. Carniv Pl Newslett 26:85–88Google Scholar
  2. Bardella VB, Grazia J, Fernandes JA, Vanzela AL (2014) High diversity in CMA3/DAPI-banding patterns in heteropterans. Cytogenet Genome Res 142:46–53. CrossRefPubMedGoogle Scholar
  3. Bureš P, Zedek F, Marková M (2013) Holocentric chromosomes. In: Wendel J, Greilhuber J, Doležel J, Leitch IJ (eds) Plant genome diversity. Vol. 2. Physical structure of plant genomes, vol. 2. Springer, Heidelberg, pp 187–208. CrossRefGoogle Scholar
  4. Carballo JA, Pincheira J, de la Torre C (2006) The G2 checkpoint activated by DNA damage does not prevent genome instability in plant cells. Biol Res 39:331–340. CrossRefPubMedGoogle Scholar
  5. Cuacos M, Franklin H, Chris F, Heckmann S (2015) Atypical centromeres in plants-what they can tell us. Frontiers Pl Sci 6:913. CrossRefGoogle Scholar
  6. Culligan K, Tissier A, Britt A (2004) ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Pl Cell 16:1091–1104. CrossRefGoogle Scholar
  7. d’Alençon E, Sezutsu H, Legeai F, Permal E, Bernard-Samain S, Gimenez S, Gagneur C, Cousserans F, Shimomura M, Brun-Barale A, Flutre T, Couloux A, East P, Gordon K, Mita K, Quesneville H, Fournier P, Feyereisen R (2010) Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci USA 107:7680–7685. CrossRefPubMedGoogle Scholar
  8. de Souza TB, Chaluvadi SR, Johnen L, Marques A, Socorro González-Elizondo M, Bennetzen JL, Vanzela ALL (2018) Analysis of retrotransposon abundance, diversity and distribution in holocentric Eleocharis (Cyperaceae) genomes. Ann Bot (Oxford) 122:279–290. CrossRefGoogle Scholar
  9. Demidov D, Schubert V, Kumke K, Weiss O, Karimi-Ashtiyani R, Buttlar J, Heckmann S, Wanner G, Dong Q, Han F, Houben A (2014) Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet Genome Res 143:150–156. CrossRefPubMedGoogle Scholar
  10. 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 Phytol 195:237–247. CrossRefPubMedGoogle Scholar
  11. Escudero M, Márquez-Corro JI, Hipp AL (2016) The phylogenetic origins and evolutionary history of holocentric chromosomes. Syst Bot 41:580–585. CrossRefGoogle Scholar
  12. Flach M (1966) Diffuse centromeres in a dicotyledonous plant. Nature 209:1369–1370CrossRefGoogle Scholar
  13. Godward MBE (1966) Conjugales. In: Godward MBE (ed) The chromosomes of the algae. Edward Arnold (Publishers) Ltd., London, pp 24–51Google Scholar
  14. Guerra M, García MA (2004) Heterochromatin and rDNA sites distribution in the holocentric chromosomes of Cuscuta approximata Bab. (Convolvulaceae). Genome 47:134–140. CrossRefPubMedGoogle Scholar
  15. Heckmann S, Schroeder-Reiter E, Kumke K, Ma L, Nagaki K, Murata M, Wanner G, Houben A (2011) Holocentric chromosomes of Luzula elegans are characterized by a longitudinal centromere groove, chromosome bending, and a terminal nucleolus organizer region. Cytogenet Genome Res 134:220–228. CrossRefPubMedGoogle Scholar
  16. Hoshi Y, Kondo K (1998) Chromosome phylogeny of the droseraceae by using CMA-DAPI fluorescent banding. Cytologia 63:329–339. CrossRefGoogle Scholar
  17. Jankowska M, Fuchs J, Klocke E, Fojtová M, Polanská P, Fajkus J, Schubert V, Houben A (2015) Holokinetic centromeres and efficient telomere healing enable rapid karyotype evolution. Chromosoma 124:519–528. CrossRefPubMedGoogle Scholar
  18. Kaur H, Kaur R, Suman V (2012) C-heterochromatin and its base composition in holokinetic chromosomes of two species of Heteroptera (Insecta: Hemiptera). Nucleus 55:163–166. CrossRefGoogle Scholar
  19. Kondo K, Lavarack PS (1984) A cytotaxonomic study of some Australian species of Drosera L. (Droseraceae). Bot J Linn Soc 88:317–333. CrossRefGoogle Scholar
  20. Kondo K, Nontachaiyapoom S (2008) An evidence on diffused centromeres in Drosera chromosomes provided by scanning electron microscopy. Chromosome Bot 3:79–81. CrossRefGoogle Scholar
  21. Kynast RG, Joseph JA, Pellicer J, Ramsay MM, Rudall PJ (2014) Chromosome behavior at the base of the angiosperm radiation: karyology of Trithuria submersa (Hydatellaceae, Nymphaeales). Amer J Bot 101:1447–1455. CrossRefGoogle Scholar
  22. Mandrioli M, Manicardi GC (2012) Unlocking holocentric chromosomes: new perspectives from comparative and functional genomics? Curr Genomics 13:343–349. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Marques A, Ribeiro T, Neumann P, Macas J, Novák P, Schubert V, Pellino M, Fuchs J, Ma W, Kuhlmann M, Brandt R, Vanzela AL, Beseda T, Šimková H, Pedrosa-Harand A, Houben A (2015) Holocentromeres in Rhynchospora are associated with genome-wide centromere-specific repeat arrays interspersed among euchromatin. Proc Natl Acad Sci USA 112:13633–13638. CrossRefPubMedGoogle Scholar
  24. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Márquez-Corro JI, Escudero M, Luceño M (2018) 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 26:139–152. CrossRefPubMedGoogle Scholar
  26. Melters DP, Paliulis LV, Korf IF, Chan SW (2012) Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res 20:579–593. CrossRefPubMedGoogle Scholar
  27. Mola LM, Papeschi AG (2006) Holokinetic chromosomes at a glance. J Basic Appl Genet 17:17–33Google Scholar
  28. Murakami A, Imai HT (1974) Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera). Chromosoma 47:167–178. CrossRefPubMedGoogle Scholar
  29. Nordenskiöld H (1963) A study of meiosis in progeny of x-irradiated Luzula purpurea. Hereditas 49:33–47. CrossRefGoogle Scholar
  30. Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Crissman HA, Darzynkiewicz Z (eds) Methods in cell biology, vol. 33. Academic Press, New York, pp 105–110Google Scholar
  31. Pazy B, Plitmann U (1994) Holocentric chromosome behaviour in Cuscuta (Cuscutaceae). Pl Syst Evol 191:105. CrossRefGoogle Scholar
  32. Preuss SB, Britt AB (2003) A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genetics 164:323–334PubMedPubMedCentralGoogle Scholar
  33. Rice A, Glick L, Abadi S, Einhorn M, Kopelman NM, Salman-Minkov A, Mayzel J, Chay O, Mayrose I (2015) The chromosome counts database (CCDB): a community resource of plant chromosome numbers. New Phytol 206:19–26. CrossRefPubMedGoogle Scholar
  34. Schrader F (1935) Notes on the mitotic behaviour of long chromosomes. Cytologia 6:422–430CrossRefGoogle Scholar
  35. Sheikh SA, Kondo K (1995) Differential staining with Orcein, Giemsa, CMA, and DAPI for comparative chromosome study of 12 species of Australian Drosera (Droseraceae). Amer J Bot 82:1278–1286. CrossRefGoogle Scholar
  36. Sheikh SA, Kondo K, Hoshi Y (1995) Study on diffused centromeric nature of Drosera chromosomes. Cytologia 60:43–47. CrossRefGoogle Scholar
  37. Shirakawa J, Hoshi Y, Kondo K (2011a) Chromosome differentiation and genome organization in carnivorous plant family Droseraceae. Chromosome Bot 6:111–119. CrossRefGoogle Scholar
  38. Shirakawa J, Nagano K, Hoshi Y (2011b) A chromosome study of two centromere differentiating Drosera species, D. arcturi and D. regia. Caryologia 64:453–563. CrossRefGoogle Scholar
  39. Stevens PF (2017) Angiosperm phylogeny website. Version 14, July 2017 [and more or less continuously updated since].” Available at: Accessed 28 Jun 2018
  40. Talbert PB, Bayes JJ, Henikoff S (2008) Evolution of centromeres and kinetochores: a two-part fugue. In: De Wulf P, Earnshaw WC (eds) The kinetochore. Springer, Berlin, pp 193–230. CrossRefGoogle Scholar
  41. Tanaka N, Tanaka N (1977) Chromosome Studies in Chionographis (Liliaceae) I. On the holokinetic nature of chromosomes in Chionographis japonica Maxim. Cytologia 42:753–763. CrossRefGoogle Scholar
  42. 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). Ann Bot (Oxford) 119:409–416. CrossRefGoogle Scholar
  43. Wanner G, Schroeder-Reiter E, Ma W, Houben A, Schubert V (2015) The ultrastructure of mono- and holocentric plant centromeres: an immunological investigation by structured illumination microscopy and scanning electron microscopy. Chromosoma 124:503–517. CrossRefPubMedGoogle Scholar
  44. Wrensch DL, Kethley JB, Norton RA (1994) Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. In: Houck MA (ed) Mites: ecological and evolutionary analyses of life-story patterns. Chapman and Hall, New York, pp 282–342CrossRefGoogle Scholar
  45. Zedek F, Bureš P (2016) Absence of positive selection on CenH3 in Luzula suggests that holokinetic chromosomes may suppress centromere drive. Ann Bot (Oxford) 118:1347–1352. CrossRefGoogle Scholar
  46. Zedek F, Bureš P (2018) Holocentric chromosomes: from tolerance to fragmentation to colonization of the land. Ann Bot (Oxford) 121:9–16. CrossRefGoogle Scholar
  47. 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. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Department of Experimental Biology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  3. 3.Section of Plant EcologyInstitute of Botany of the Czech Academy of SciencesTřeboňCzech Republic

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