, Volume 21, Issue 1, pp 109–120 | Cite as

Genetic background of enhanced radioresistance in an anhydrobiotic insect: transcriptional response to ionizing radiations and desiccation

  • Alina Ryabova
  • Kyosuke Mukae
  • Alexander Cherkasov
  • Richard Cornette
  • Elena Shagimardanova
  • Tetsuya Sakashita
  • Takashi Okuda
  • Takahiro KikawadaEmail author
  • Oleg GusevEmail author
Special Feature: Original Paper 11th International Congress on Extremophiles
Part of the following topical collections:
  1. 11th International Congress on Extremophiles


It is assumed that resistance to ionizing radiation, as well as cross-resistance to other abiotic stresses, is a side effect of the evolutionary-based adaptation of anhydrobiotic animals to dehydration stress. Larvae of Polypedilum vanderplanki can withstand prolonged desiccation as well as high doses of ionizing radiation exposure. For a further understanding of the mechanisms of cross-tolerance to both types of stress exposure, we profiled genome-wide mRNA expression patterns using microarray techniques on the chironomid larvae collected at different stages of desiccation and after exposure to two types of ionizing radiation—70 Gy of high-linear energy transfer (LET) ions (4He) and the same dose of low-LET radiation (gamma rays). In expression profiles, a wide transcriptional response to desiccation stress that much exceeded the amount of up-regulated transcripts to irradiation exposure was observed. An extensive group of coincidently up-regulated overlapped transcripts in response to desiccation and ionizing radiation was found. Among this, overlapped set of transcripts was indicated anhydrobiosis-related genes: antioxidants, late embryogenesis abundant (LEA) proteins, and heat-shock proteins. The most overexpressed group was that of protein-L-isoaspartate/D-aspartate O-methyltransferase (PIMT), while probes, corresponding to LEA proteins, were the most represented. Performed functional analysis showed strongly enriched gene ontology terms associated with protein methylation. In addition, active processes of DNA repair were detected. We assume that the cross-tolerance of the sleeping chironomid to both desiccation and irradiation exposure comes from a complex mechanism of adaptation to anhydrobiosis.


Bioinformatics and evolutionary relationship of enzymes Molecular biology Radiation tolerance Anhydrobiosis 



This work was supported in part by the Grants-in-Aid from MEXT/JSPS KAKENHI (Grant Number 16K07308, 25252060, 16K15073, and 15H05622) and a part of this study is also the result of the project “Characterization of the Mechanisms Underlying the Radiation Resistance Associated with Cryptobiosis” carried out under the Grant “Strategic Promotion Program for Basic Nuclear Research” by MEXT. Bioinformatics analysis was supported by Russian Science Foundation Grant for international groups (No. 14-44-00022).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

792_2016_888_MOESM1_ESM.pdf (609 kb)
Supplementary material 1 (PDF 609 kb)


  1. Billi D, Friedmann E, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66(4):1489–1492. doi: 10.1128/AEM.66.4.1489-1492.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Calahan D, Dunham M, DeSevo C, Koshland DE (2011) Genetic analysis of desiccation tolerance in Sachharomyces cerevisiae. Genetics 189(2):507–519. doi: 10.1534/genetics.111.130369 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Challabathula D, Puthur JT, Bartels D (2015) Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants. Ann N Y Acad Sci 1365(1):89–99. doi: 10.1111/nyas.12884 CrossRefPubMedGoogle Scholar
  4. Cornette R, Kikawada T (2011) The induction of anhydrobiosis in the sleeping chironomid: current status of our knowledge. IUBMB Life 63:419–429. doi: 10.1002/iub.463 CrossRefPubMedGoogle Scholar
  5. Cornette R, Kanamori Y, Watanabe M, Nakahara Y, Gusev O, Mitsumasu K, Kadono-Okuda K, Shimomura M, Mita K, Kikawada T, Okuda T (2010) Identification of anhydrobiosis-related genes from an expressed sequence tag database in the cryptobiotic midge Polypedilum vanderplanki (Diptera; Chironomidae). J Biol Chem 285(46):35889–35899. doi: 10.1074/jbc.M110.150623 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cox MM, Battista JR (2005) Deinococcus radiodurans–the consummate survivor. Nat Rev Microbiol 3(11):882–892. doi: 10.1038/nrmicro1264 CrossRefPubMedGoogle Scholar
  7. Cromie GA, Connelly JC, Leach DRF (2001) Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol Cell 8(6):1163–1174CrossRefPubMedGoogle Scholar
  8. Crowe LM, Crowe JH (1992) Anhydrobiosis: a strategy for survival. Adv Space Res 12(4):239–247CrossRefPubMedGoogle Scholar
  9. Desrosiers RR, Fanelus I (2011) Damaged proteins bearing L-isoaspartyl residues and aging: a dynamic equilibrium between generation of isomerized forms and repair by PIMT. Curr Aging Sci 4(1):8–18CrossRefPubMedGoogle Scholar
  10. Dinakar C, Bartels D (2013) Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front Plant Sci 4:482. doi: 10.3389/fpls.2013.00482 CrossRefPubMedPubMedCentralGoogle Scholar
  11. França MB, Panek AD, Eleutherio EC (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146(4):621–631CrossRefPubMedGoogle Scholar
  12. Furuchi T, Sakurako K, Katane M, Sekine M, Homma H (2010) The role of protein L-isoaspartyl/D-aspartyl O-methyltransferase (PIMT) in intracellular signal transduction. Chem Biodivers 7(6):1337–1348. doi: 10.1002/cbdv.200900273 CrossRefPubMedGoogle Scholar
  13. Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D (2012) Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol Life Sci 69(19):3175–3186. doi: 10.1007/s00018-012-1088-0 CrossRefPubMedGoogle Scholar
  14. Gladyshev E, Meselson M (2008) Extreme resistance of bdelloid rotifers to ionizing radiation. PNAS 105(13):5139–5144. doi: 10.1073/pnas.0800966105 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5:36. doi: 10.3389/fpls.2014.00036 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gusev O, Nakahara Y, Vanyagina V, Malutina L, Cornette R, Sakashita T, Hamada N, Kikawada T, Kobayashi Y, Okuda T (2010) Anhydrobiosis-associated nuclear DNA damage and repair in the sleeping chironomid: linkage with radioresistance. PLoS One 5(11):e14008. doi: 10.1371/journal.pone.0014008 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gusev O, Suetsugu Y, Cornette R, Kawashima T, Logacheva MD, Kondrashov AS, Penin AA, Hatanaka R, Kikuta S, Shimura S, Kanamori H, Katayose Y, Matsumoto T, Shagimardanova E, Alexeev D, Govorun V, Wisecaver J, Mikheyev A, Koyanagi R, Fujie M, Nishiyama T, Shigenobu S, Shibata TF, Golygina V, Hasebe M, Okuda T, Satoh N, Kikawada T (2014) Comparative genome sequencing reveals genomic signature of extreme desiccation tolerance in the anhydrobiotic midge. Nat Commun 5:4784. doi: 10.1038/ncomms5784 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Halberg KA, Jørgensen A, Møbjerg N (2013) Desiccation tolerance in the tardigrade Richtersius coronifer relies on muscle mediated structural reorganization. PLoS One 8(12):e85091. doi: 10.1371/journal.pone.0085091 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hall EJ, Giaccia AJ (2006) Radiobiology for the radiologist, 6th ed. Philadelphia: Lippincott Williams&Wilkins p 546Google Scholar
  20. Han W, Yu PKN (2010) Ionizing radiation, DNA double strand break and mutation. Chapter 7. In: Advances in genetics research, Vol. 4. Nova Science Publishers, Inc., New YorkGoogle Scholar
  21. Hand SC, Menze MA (2015) Molecular approaches for improving desiccation tolerance: insights from the brine shrimp Artemia franciscana. Planta 242(2):379–388. doi: 10.1007/s00425-015-2281-9 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hengherr S, Heyer AG, Köhler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades–evidence for divergence in responses to dehydration. FEBS J 275(2):281–288CrossRefPubMedGoogle Scholar
  23. Hengherr S, Worland MR, Reuner A, Brummer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749–755. doi: 10.1086/605954 CrossRefPubMedGoogle Scholar
  24. Hinton HE (1960) A fly larva that tolerates dehydration and temperatures of −270 °C to +102 °C. Nature 188(4747):336–337. doi: 10.1038/188336a0 CrossRefGoogle Scholar
  25. Hoekstra FA, Golovina EA, Buitink J (2001a) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6(9):431–438. doi: 10.1016/S1360-1385(01)02052-0 CrossRefPubMedGoogle Scholar
  26. Hoekstra FA, Golovina EA, Tetteroo FA, Wolkers WF (2001b) Induction of desiccation tolerance in plant somatic embryos: how exclusive is the protective role of sugars? Cryobiology 43(2):140–150CrossRefPubMedGoogle Scholar
  27. Ito C, Goto SG, Numata H (2013) Desiccation and heat tolerance of eggs of the Asian tadpole shrimp. Triops granarius. Zoolog Sci 30(9):760–766. doi: 10.2108/zsj.30.760 CrossRefPubMedGoogle Scholar
  28. Khare S, Linster CL, Clarke SG (2011) The interplay between protein L-isoaspartyl methyltransferase activity and insulin-like signaling to extend lifespan in Caenorhabditis elegans. PLoS One 6(6):e20850. doi: 10.1371/journal.pone.0020850 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kikawada T, Minakawa N, Watanabe M, Okuda T (2005) Factors inducing successful anhydrobiosis in the African Chironomid Polypedilum vanderplanki: significance of the larval tubular nest. Integr Comp Biol 45(5):710–714CrossRefPubMedGoogle Scholar
  30. Kikawada T, Nakahara Y, Kanamori Y, Iwata K-I, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348(1):56–61. doi: 10.1016/j.bbrc.2006.07.003 CrossRefPubMedGoogle Scholar
  31. Koster KL, Leopold AC (1988) Sugars and desiccation tolerance in seeds. Plant Physiol 88(3):829–832CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553(3):387–390. doi: 10.1016/S0014-5793(03)01062-7 CrossRefPubMedGoogle Scholar
  33. Leprince O, Buitink J (2015) Introduction to desiccation biology: from old borders to new frontiers. Planta 242(2):369–378. doi: 10.1007/s00425-015-2357-6 CrossRefPubMedGoogle Scholar
  34. Mattimore V, Battista J (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633–637CrossRefPubMedPubMedCentralGoogle Scholar
  35. McGill LM, Shannon AJ, Pisani D, Félix MA, Ramløv H, Dix I, Wharton DA, Burnell AM (2015) Anhydrobiosis and freezing-tolerance: adaptations that facilitate the establishment of Panagrolaimus nematodes in polar habitats. PLoS One 10(3):e0116084. doi: 10.1371/journal.pone.0116084 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Moskalev A, Zhikrivetskaya S, Krasnov G, Shaposhnikov M, Proshkina E, Borisoglebsky D, Danilov A, Peregudova D, Sharapova I, Dobrovolskaya E, Solovev I, Zemskaya N, Shilova L, Snezhkina A, Kudryavtseva A (2015) A comparison of the transcriptome of Drosophila melanogaster in response to entomopathogenic fungus, ionizing radiation, starvation and cold shock. BMC Genom 16(Suppl 13):S8. doi: 10.1186/1471-2164-16-S13-S8 CrossRefGoogle Scholar
  37. Musilova M, Wright G, Ward JM, Dartnell LR (2015) Isolation of radiation-resistant bacteria from Mars analog Antarctic dry valleys by preselection, and the correlation between radiation and desiccation resistance. Astrobiology 15(12):1076–1090. doi: 10.1089/ast.2014.1278 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Potts M, Slaughter SM, Hunneke FU, Garst JF, Helm RF (2005) Desiccation tolerance of prokaryotes: application of principles to human cells. Integr Comp Biol 45(5):800–809. doi: 10.1093/icb/45.5.800 CrossRefPubMedGoogle Scholar
  39. Rebecchi L, Altiero T, Guidetti R (2007) Anhydrobiosis: the extreme limit of desiccation tolerance. ISJ 4:65–81Google Scholar
  40. Schmitt FJ, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837(6):835–848. doi: 10.1016/j.bbabio.2014.02.005 CrossRefPubMedGoogle Scholar
  41. Shapiro-Ilan DI, Brown I, Lewis EE (2014) Freezing and desiccation tolerance in entomopathogenic nematodes: diversity and correlation of traits. J Nematol 46(1):27–34PubMedPubMedCentralGoogle Scholar
  42. Shen-Miller J, Mudgett MB, Schopf JW, Clarke S, Berger R (1995) Exceptional seed longevity and robust growth: ancient sacred lotus from China. Am J Bot 82(11):1367–1380. doi: 10.2307/2445863 CrossRefGoogle Scholar
  43. Somme L (1996) Anhydrobiosis and cold tolerance in tardigrades. Eur J Entomol 93(3):349–357Google Scholar
  44. Tanaka M, Earl AM, Howell HA, Park MJ, Eisen JA, Peterson SN, Battista JR (2004) Analysis of Deinococcus radiodurans’s transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 168:21–33. doi: 10.1534/genetics.104.029249 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41(1):15–31. doi: 10.1303/aez.2006.15 CrossRefGoogle Scholar
  46. Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799–2802PubMedGoogle Scholar
  47. Watanabe M, Kikawada T, Okuda T (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J Exp Biol 206:2281–2286CrossRefPubMedGoogle Scholar
  48. Watanabe M, Sakashita T, Fujita A, Kikawada T, Horikawa DD et al (2006a) Biological effects of anhydrobiosis in an African chironomid, Polypedilum vanderplanki on radiation tolerance. Int J Radiat Biol 82:587–592CrossRefPubMedGoogle Scholar
  49. Watanabe M, Sakashita T, Fujita A, Kikawada T, Nakahara Y et al (2006b) Estimation of radiation tolerance to high LET heavy ions in an anhydrobiotic insect, Polypedilum vanderplanki. Int J Radiat Biol 82:835–842CrossRefPubMedGoogle Scholar
  50. Watanabe M, Nakahara Y, Sakashita T, Kikawada T, Fujita A, Hamada N, Horikawa DD, Wada S, Kobayashi Y, Okuda T (2007) Physiological changes leading to anhydrobiosis improve radiation tolerance in Polypedilum vanderplanki larvae. J Insect Physiol 53(6):573–579CrossRefPubMedGoogle Scholar
  51. Yoshinaga K, Yoshioka H, Kurosaki H, Hirasawa K, Uritani M, Hasegawa M (1997) Protection by trehalose of DNA from radiation damage. Biosci Biotechnol Biochem 61(1):160–161CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  1. 1.Institute of Fundamental Biology and MedicineKazan Federal UniversityKazanRussia
  2. 2.Graduate School of Science and EngineeringSaitama UniversitySaitamaJapan
  3. 3.Anhydrobiosis Research GroupInstitute of Agrobiological Sciences, NAROTsukubaJapan
  4. 4.Takasaki Advanced Radiation Research InstituteNational Institutes for Quantum and Radiological Science and TechnologyTakasakiJapan
  5. 5.Department of Integrated Biosciences, Graduate School of Frontier SciencesThe University of TokyoKashiwaJapan
  6. 6.Center for Life Science Technologies, RIKENYokohamaJapan
  7. 7.RIKEN Innovation Center, RIKENYokohamaJapan

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