Endoreduplication in Drosophila melanogaster progeny after exposure to acute γ-irradiation

  • Daria A. Skorobagatko
  • Alexey A. Mazilov
  • Volodymyr Yu. StrashnyukEmail author
Original Article


The purpose of this investigation was to study the effect of acute γ-irradiation of parent adults on the endoreduplication of giant chromosomes in F1 generation of Drosophila melanogaster Meig. A wild-type Oregon-R strain was used as the material. Virgin females and males of Drosophila adults at the age of 3 days were irradiated with doses of 8, 16 and 25 Gy. Giant chromosomes were studied by cytomorphometry on squashed preparations of Drosophila salivary glands stained with acetoorsein. The preparations were obtained at late third instar larvae. The mean values of the polyteny degree of chromosomes (PDC) in males increased after 8 Gy by 10.6%, after 25 Gy by 7.4%, and did not change after the dose of 16 Gy. In females, the PDC did not differ from the control irrespective of the irradiation dose. An increase in endoreduplication was also evidenced by the accelerated development of offsprings of both sexes after irradiation of parents with 25 Gy, and in males also at a dose of 16 Gy. The statistical impact of power of radiation on polyteny was 26.8%, while the impact of sex was 4.9%. The impact of power of radiation on the developmental rate of offspring was 4.4% in males and 7.5% in females. The enhancement of endoreduplication is considered as a consequence of increasing selection pressure after irradiation. The possible involvement of epigenetic effects in the effect of ionizing radiation on endoreduplication is discussed.


Giant chromosomes Polyteny degree Developmental rate Embryonic mortality Ionizing radiation 



This work was supported by the Ministry of Education and Science of Ukraine (Project State registration number: 0117U004836).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Alexander M, Bergendahl J (1964) Dose rate effects in the developing germ cells of male Drosophila. Genetics 49:1–16Google Scholar
  2. Bandura JL, Zielke N (2017) Polyploidy in animal development and desease. In: Li XQ (ed) Somatic genome variation: in animals, plants, and microorganisms, 1st edn. Wiley-Blackwell, New York, pp 3–44Google Scholar
  3. Britton JS, Edgar BA (1998) Environmental control of the cell cycle in Drosophila: nutrition activated mitotic and endoreduplicative cells by distinct mechanisms. Development 125:2149–2158Google Scholar
  4. Can KL, Hicks GG (2006) Adsence of an immediate G 1/S checkpoint in primary MEFs following gamma-radiation identified a novel checkpoint switch. Cell Cycle 5:1823–1830CrossRefGoogle Scholar
  5. Cookson SJ, Radziejwoski A, Granier C (2006) Cell and leaf size plasticity in Arabidopsis: what is the role of endoreduplication. Plant Cell Environ 29:1273–1283CrossRefGoogle Scholar
  6. Deckbar D, Jeggo PA, Löbrich M (2011) Understanding the limitation of radiation-induced cell cycle checkpoints. Crit Rev Biochem Mol Biol 46:271–283CrossRefGoogle Scholar
  7. Dubrova YuE (2006) Genomic instability in the offspring of irradiated parents: facts and interpretations. Russ J Genet 42:1116–1126CrossRefGoogle Scholar
  8. Dyka LD, Shakina LA, Strashnyuk VYu, Shckorbatov YuG (2016) Effects of 36,6 GHz and static magnetic field on degree of endoreduplication in Drosophila melanogaster polytene chromosomes. Int J Radiat Biol 92:222–227CrossRefGoogle Scholar
  9. Edgar BA, Orr-Weaver TI (2001) Endoreduplication cell cycle: more or less. Cell 105:297–306CrossRefGoogle Scholar
  10. Edgar BA, Zielke N, Gutierrez C (2014) Endocycles: a recurrent evolutionary innovation for post-mitotic cell growth. Nat Rev Mol Cell Biol 15:197–210CrossRefGoogle Scholar
  11. Einor D, Bonisoli-Alquati A, Costantini D, Mousseau TA, Møller AP (2016) Ionizing radiation, antioxidant response and oxidative damage: a meta-analysis. Sci Total Environ 548–549:463–471ADSCrossRefGoogle Scholar
  12. Fox DT, Duronio RJ (2013) Endoreplication and polyploidy: insights into development and disease. Development 140:3–12CrossRefGoogle Scholar
  13. Geodakian VA (1998) Evolutionary role of sex chromosomes (a new concept). Russ J Genet 34:1171–1184 (In Russian) Google Scholar
  14. Golub NI, Chernyk II (2008) Mutations induced by X-ray irradiation and certain chemical reagents that alter the life span of Drosophila melanogaster. Cytol Genet 42:30–36CrossRefGoogle Scholar
  15. Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101–110CrossRefGoogle Scholar
  16. Hassel C, Zhang B, Dixon M, Calvi BR (2014) Induction of endocycles represses apoptosis independently of differentiation and predisposes cells to genome instability. Development 141:112–123CrossRefGoogle Scholar
  17. Hourcade JD, Pérez-Crespo M, Fernández-González R, Pintado B, Gutiérrez-Adán A (2010) Selection against spermatozoa with fragmented DNA after postovulatory mating depends on the type of damage. Reprod Biol Endocrinol 8:9. CrossRefGoogle Scholar
  18. Hua BL, Orr-Weaver TL (2017) DNA replication control during Drosophila development: insights into the onset of S phase, replication initiation, and fork progression. Genetics 207:29–47CrossRefGoogle Scholar
  19. Hudson AM, Cooley L (2014) Methods for studying oogenesis. Methods 68:207–217CrossRefGoogle Scholar
  20. Huxley JS (1924) Sex determination and related problems. Med Sci Abstr Rev 10:91–124Google Scholar
  21. Irwin M, Marin MC, Phillips AC, Seelan RS, Smith DI, Liu W, Flores ER, Tsai KY, Jacks T, Vousden KH, Kaelin WG Jr (2000) Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 407:645–648ADSCrossRefGoogle Scholar
  22. Izmaylov DM, Obukhova LK, Okladnova OV, Akifyev AP (1993) Phenomenon of life span instability in Drosophila melanogaster: II. Change in rhythm of natural variations of life span after single exposure to γ-irradiation. Exp Gerontol 28:181–194CrossRefGoogle Scholar
  23. Kiknadze II, Gruzdev AD (1970) Change in chromosome length related to polyteny in the chironomid salivary gland. Genetica 12:953–960 (In Russian) Google Scholar
  24. Korochkin LI (2006) What is epigenetics. Russ J Genet 42:1156–1164 (In Russian) CrossRefGoogle Scholar
  25. Larkins BA, Dilkes BP, Dante RA, Coelho CM, Woo Y, Liu Y (2001) Investigating hows and why of DNA endoreduplication. J Exp Bot 52:183–194CrossRefGoogle Scholar
  26. Lee HO, Davidson JM, Duronio RJ (2009) Endoreduplication: polyploidy with a purpose. Genes Dev 23:2461–2477CrossRefGoogle Scholar
  27. Lilly MA, Spradling AC (1996) The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev 10:2514–2526CrossRefGoogle Scholar
  28. Lindsley DL, Tokuyasu KT (1980) Spermatogenesis. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila. Acad Press, London, pp 225–294Google Scholar
  29. Losick VP, Fox DT, Spradling AC (2013) Polyploidization and cell fusion contribute to wound healing in the adult Drosophila epithelium. Curr Biol 23:2224–2232CrossRefGoogle Scholar
  30. Marguerat S, Bähler J (2012) Coordinating genome expression with cell size. Trends Genet 28:560–565CrossRefGoogle Scholar
  31. McKee BD, Tsai JH, Yan R (2012) Meiosis in male Drosophila. Spermatogenesis 2(3):167–184CrossRefGoogle Scholar
  32. McLaughlin JM, Bratu DP (2015) Drosophila melanogaster oogenesis: an overview. In: Walker JM (ed) Methods in molecular biology. Humana Press, Clifton, pp 1–20Google Scholar
  33. Mehrotra S, Maqbool SB, Kolpakas A, Murnen K, Calvi BR (2008) Endocycling cells do not apoptose in response to DNA rereplication genotoxic stress. Genes Dev 22:3158–3171CrossRefGoogle Scholar
  34. Moskalev AA, Plyusnina EN, Shaposhnikov MV (2011) Radiation hormesis and radioadaptive response in Drosophila melanogaster flies with different genetic backgrounds: the role of cellular stress-resistance mechanisms. Biogerontology 12:253–263CrossRefGoogle Scholar
  35. Mushak P (2007) Hormesis and its place in nonmonotonic dose–response relationships: some scientific reality checks. Environ Health Perspect 115:201–211CrossRefGoogle Scholar
  36. Nagl W (1976) DNA endoreduplication and polyteny understood as evolutionary strategies. Nature 261:614–615ADSCrossRefGoogle Scholar
  37. Nahle Z, Polakoff J, Davuluri RV, McCurrach ME, Jacobson MD, Narita M, Zhang MQ, Lazebnik Y, Bar-Sagi D, Lowe SW (2002) Direct coupling of the cell cycle and cell death machinery by E2F. Nat Cell Biol 4:859–864CrossRefGoogle Scholar
  38. Øvrebø JI, Edgar BA (2018) Polyploidy in tissue homeostasis and regeneration. Development. CrossRefGoogle Scholar
  39. Rarog MA, Strashnyuk VYu, Kondrat’eva AO, Dmitruk TV, Vorob’eva LI, Shakhbazov VG (1999) Effect of culture density on expressivity of character eyeless and polyteny of giant chromosomes in Drosophila melanogaster. Russ J Genet 35:766–769Google Scholar
  40. Rodman TC (1967) DNA replication in salivary gland nuclei of Drosophila melanogaster at successive larval and prepupal stages. Genetics 55:375–386Google Scholar
  41. Sarup P, Loeschcke V (2011) Life extension and the position of the hormetic zone depends on sex and genetic background in Drosophila melanogaster. Biogerontology 12:109–117CrossRefGoogle Scholar
  42. Shakina LA, Strashnyuk VYu (2011) Genetic, molecular, and humoral endocycle-regulating mechanisms. Russ J Genet 47:1151–1160CrossRefGoogle Scholar
  43. Sihna P, Lakhotia SC (1983) Replication in Drosophila chromosomes XI. Stimulation of initiation of polytene replication cycles in vitro by juvenile hormone. Cell Differ 12:11–17CrossRefGoogle Scholar
  44. Skorobagatko DA, Shakina LA, Strashnyuk VYu, Mazilov AA (2015a) Lethal and recombinative action of γ-radiation in genetically unstable Drosophila melanogaster Bar strain. Radiatsionnaya Biologiya Radioekologiya 55:145–154Google Scholar
  45. Skorobagatko DA, Strashnyuk VYu, Mazilov AA (2015b) Fitness components in the offsprings of Drosophila melanogaster Meig. after acute γ-irradiation. Factors Exp Evol Org 16:78–82. Russian)
  46. Skorobagatko DA, Strashnyuk VY, Mazilov AA (2016) Lifespan in the progeny of Drosophila melanogaster after acute γ-irradiation. J VN Karazin Kharkiv Natl Univ Ser Biol 26:74–84. Russian)
  47. Strashnyuk VYu, Nepeivoda SN, Shakhbazov VG (1995) Cytomorphometric analysis of Drosophila melanogaster Meig. polytene chromosomes in relation to heterosis, selection for adaptively valuable traits, and sex. Russ J Genet 31:17–21Google Scholar
  48. Strashnyuk VYu, Al-Hamed S, Nepeivoda SN, Shakhbazov VG (1997) Cetogenetic and cytobiophysical investigation of mechanisms of temperature adaptation and heterosis in Drosophila melanogaster Meig. Russ J Genet 33:793–799Google Scholar
  49. Sugimoto-Shirasu K, Roberts K (2003) “Big it up”: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6:544–553CrossRefGoogle Scholar
  50. Tikhomirova MM (1990) Genetic analysis (In Russian). LSU Publition, LeningradGoogle Scholar
  51. Ullah Z, Kohn MJ, Yagi R, Vassilev LT, DePamphilis ML (2008) Differentiation of trophoblast stem cells into giant cells is triggered by p57/Kip2 inhibition of CDK1 activity. Genes Dev 22:3024–3036CrossRefGoogle Scholar
  52. Ullah Z, Lee CY, Lilly MA, DePamphilis ML (2009) Developmentally programmed endoreduplication in animals. Cell Cycle 8(10):1501–1509CrossRefGoogle Scholar
  53. Vaiserman AM, Koshel NM, Mechova LV, Voitenko VP (2004) Cross-life stage and crossgenerational effects of gamma irradiations at the egg stage on Drosophila melanogaster life histories. Biogerontology 5:327–337CrossRefGoogle Scholar
  54. Vasil’eva LA, Antonenko OV, Zakharov IK (2011) Role of transposable elements in the genome of Drosophila melanogaster. Russ J Genet 47:463–488 (In Russian) CrossRefGoogle Scholar
  55. Wichmann A, Uyetake L, Tin Tin Su (2010) E2F1 and E2F2 have opposite effects on radiation-induced p53-independent apoptosis in Drosophila. Dev Biol 346:80–89CrossRefGoogle Scholar
  56. Xiang J, Bandura J, Zhang P, Jin Y, Reuter H, Edgar BA (2017) EGFR-dependent TOR-independent endocycles support Drosophila gut epithelial regeneration. Nat Commun 8:1–13. CrossRefGoogle Scholar
  57. Zhimulev IF, Koryakov DE (2009) Polytene chromosomes. In: Encyclopedia of life sciences (ELS). JohnWiley & Sons, Ltd: Chichester.
  58. Zhuravleva LA, Strashnyuk VYu, Shakhbazov VG (2004) Influence of culture density on the polyteny degree of giant chromosomes in inbred lines and hybrids of Drosophila melanogaster. Cytol Genet 38:46–51 (In Russian) Google Scholar
  59. Zielke N, Kim KJ, Tran V, Shibutani ST, Bravo MJ, Nagarajan S, van Straaten M, Woods B, von Dassow G, Rottig C, Lehner CF, Grewal SS, Duronio RJ, Edgar BA (2011) Control of Drosophila endocycles by E2F and CRL4CDT2. Nature 480:123–127ADSCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Genetics and CytologyVN Karazin Kharkiv National UniversityKharkivUkraine
  2. 2.Laboratory of Radiation Research and Environmental ProtectionNSC ‘Kharkiv Institute of Physics and Technology’KharkivUkraine

Personalised recommendations