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Rearrangements in chironomidae (Diptera) genomes induced by various environmental stress factors

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Russian Journal of Genetics: Applied Research

To the famous scientist, colleague and friend Prof. Dr. Iya Ivanovna Kiknadze, who is still full of energy and keeps working in the field of Genetics: Cytogenetics and Evolution, especially of family Chironomidae, Diptera.

Abstract

Invertebrates are known to be an appropriate tool for assessment of the state of aquatic ecosystems. Some insect groups are frequently used in alternative test methods due to their specific characteristics such as: higher sensitivity than in vertebrates, short live cycles, large population size, availabity at a very low cost, etc. Species of family Chironomidae are very suitable invertebrates for risk assessment within the scope of programs of aquatic ecosystem and human health protection. They are widely distributed, sensitive to many pollutants; some of them can be cultivated; they have a short lite cycle; and their larvae are of great importance in aquatic food chains. They have excellent salivary gland chromosomes, which are promising tools to assess genotoxicity in the environment. Due to their good resolution they allow detection of a broad range of cytogenetic aberrations at the structural and functional levels. Somatic structural aberrations (inversions, deletions, deficiencies, amplification, and others) can be used as biomarkers at the cytogenetical level for measurement of the toxic effects of different stress agents in the environment. Due to deletions in chromosome G in some chironomid species, it was transformed to so called pompon-like chromosome G, which can be used to test the genotoxicity of various agents in an aquatic ecosystem. It is emphasized that the BR system is a very interesting model for studying the response of the genome to pollutants tn the environment. Together with the standard activity of this system, a clear reversed level of activity was observed. Changes of the activity of the Nucleolar Organizer were also detected. It is shown that these important key structures are affected by trace metal toxicity. The protective role of heterochromatin is discussed. It has been shown that in the model ecotoxicological species C. piger and C. riparius the distribution of somatic rearrangements in their genome is nonrandom. They concentrate mainly at or close to sites rich in repetitive DNA loci. Structural and functional aberrations in polytene chromosomes can serve as early-warning indicators of environmental pollutions. Changes at the population and community levels can be analyzed by using these biomarkers of individual response.

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References

  • Andreeva, E.N., Kiknadze, I.I., and Aimanova, K., Comparative Analysis of Polytene Chromosome Banding Pattern of Closely Related Species Glyptotendipes salinus Michatlova and G. barbipes Staeger (Diptera, Chironomidae), Tsitologia, 1998, vol. 40, no. 11, pp. 972–979.

    Google Scholar 

  • Beermann, W., Directed Changes in Die Pattern of Balbiani Ring Puffing in Chironomus: Effect of a Sugar Treatment, Chromosoma, 1973, vol. 41, pp. 297–326.

    Article  PubMed  CAS  Google Scholar 

  • Bovero, S., Hankeln, T., Michailova, P., et al., Nonrandom Chromosomal Distribution of Spontaneous Breakpoints and Satellite DNA Cluster in Two Geographically Distant Populations of Chironomus riparius (Diptera, Chironomidae), Genetica, 2002, vol. 115, pp. 273–281.

    Article  PubMed  Google Scholar 

  • Bremner, I., Manifestations of Copper Excess, Amer. J. Clin. Nutr., 1998, vol. 67, pp. 1069–1073.

    Google Scholar 

  • Coogan, T.P., Bare, R.M., and Walkes, M.P., Cadmium-Induced DNA Strand Damage in Cultured Liver Cells: Reduction in Cadmium Genotoxicity Following Zinc Pretreatment, Toxicol. Appl. Pharmacol., 1992, vol. 113, pp. 27–33.

    Article  Google Scholar 

  • De Pauw, N., Ghetti, P.F., Manzini, P., and Spaggiari, R., Biological Assessment Methods for Running Waters in River Water Quality—Ecological Assessment and Control, Brussels: European Commission, 1992, pp. 217–248.

    Google Scholar 

  • Diez, L., Cortes, E., Merimo, J., and Santa Cruz, M., Galactoze Induced Puffing Changes in Chironomus thunini Balbiani Rings and Their Dependence on Protein Synthesis, Chromosoma, 1990, vol. 99, pp. 61–70.

    Article  CAS  Google Scholar 

  • Elgohary, W.G., Sidhu, S., Krezoski, S.O., et al., Protection of DNA in HL-60 Cells from Damage Generated by Hydroxyl Radicals Produced by Reaction of H2O2 with Cell Iron by Zinc-Metallothionein, Chem.-Biol. Interactions, 1998, vol. 115, pp. 85–107.

    Article  CAS  Google Scholar 

  • Fischer, J., Zur Fortplanzungsbiologie von Chironomus nuditarsis, Rev. Zool., 1969, vol. 76, pp. 23–35.

    Google Scholar 

  • Fischer, J. and Tichy, H., Über Eine Heterochromatin Mutation Aus Einer Wildpopulation Von Chironomus nuditarsli. I. Zur Funktion Des Veranderten Genom-Abschnittes, Genetica, 1980, vol. 54, pp. 41–43.

    Article  Google Scholar 

  • Forstner, U. and Salomons, W., Trace Metal Analysis on Polluted Sediments. I. Assessment of Sources and Intensities, Environ. Technol. Lett., 1980, vol. 1, pp. 494–505.

    Article  Google Scholar 

  • Golubovsky, M.D., The Century of Genetics: Evolution of Ideas and Concept Burey Art, Saint-Petersburg, 2000. p. 262.

  • Gunderina, L. and Aimanova, K.G., Genetic Consequences of Exposure to γ-Radiation in Chironomus thummi: Aberrations of Polytene Chromosomes, Russ. J. Genet., 1998, vol. 34, pp. 273–280.

    CAS  Google Scholar 

  • Hägele, K., DNA—Replicationinuster der Speicheldrusen Chromosomen Von Chironomiden, Chromosoma, 1970, vol. 31, pp. 91–138.

    Article  PubMed  Google Scholar 

  • Hägele, K., Differential Staining of Polytene Chromosome Bands in Chironomus by Gimsa Banding Methods, Chromosoma, 1977, vol. 59, pp. 207–216.

    Article  PubMed  Google Scholar 

  • Hankeln, T., Molekular Analyse Phylogenetisch Bedeutsamer Repetitiver DNA Chironomiden: Ph. D. Thesis, Buchum: Ruhr University, 1990.

    Google Scholar 

  • Henikoff, S., Position Effect Variegation after 60 Years, Hereditas, 1990, vol. 6, pp. 422–426.

    CAS  Google Scholar 

  • Hoffrichter, O., Studied zur Morphologie und Karyosystematik der Gattungen Glyptotendipes (Chironomidae, Diptera), Dissertation, Freiburg: Albert L. Universität, Freiburg, 1977.

    Google Scholar 

  • Ilkova, J., Chromosome Variability of Species of Subfamily Chironominae (Diptera, Chironomidae) from Polluted Regions Near Sofia, Acta Zool. Bulgaria, 2004, vol. 56, no. 1, pp. 15–30.

    Google Scholar 

  • Ilkova, J., Hankeln, T., Schmidt, E., et al. Genome Instability of Chironomus riparius Mg. and Chironomus piger Strenzke (Diptera, Chironomidae), Caryologia, 2007, vol. 60, no. 4, pp. 299–305.

    Google Scholar 

  • Jannssen de Bisthoven, L.G., Timmermans, K.R., and Ollevier, F., The Concentration of Cadmium, Lead, Copper and Zinc in Chironomus riparius Larvae with Deformed Versus Normal Menta, Hydrobiologia, 1992, vol. 239, pp. 141–149.

    Article  Google Scholar 

  • Karlik, S.J., Eichhom, G.L., and McLachlan Crapper, D.R., Molecular Interactions of Aluminium with DNA, Neurotoxicology, 1980, vol. 1, pp. 83–88.

    CAS  Google Scholar 

  • Kiknadze, I. and Panova, T., Heteromorphic Puffs in Chironomus thummi, Tsitologia, 1972, vol. 9, pp. 1081–1091.

    Google Scholar 

  • Kiknadze I.I., Comparative Puffing Characteristics in Salivary Gland Chromosomes in Larval Development and Metamoiphosis. Puffing in IVth Chromosome, Tsitologia, 1976, vol. 18, pp. 1322–1329.

    Google Scholar 

  • Kiknadze, I., Zainiev, G., Panova, T., et al., Identification of Balbiani Ring Chromosomes in Chironomus thummi Polytene Chromosomes, Biol. Zbl., 1985, vol. 1, pp. 113–123.

    Google Scholar 

  • Kiknadze, I., Chromosomal Polymoiphism in Natural Populations of Plumosus Species-Group of West Siberia, Entomol. Scand., 1987, Suppl. 29, pp. 113–121.

  • Kiknadze, I., Kolesnikov, N., Panova, T., et al., Transposable Elements in Chironomidae. Localization of pCth. C12HR Sequences in the Polytene Chromosomes of Closely Related Subspecies, C. th. thummi and C. th. piger, Moscow, 1987.

  • Kiknadze, I., Gunderina, L., Filippova, M., and Seray, E., Chromosomal Polymorphism in Natural and Laboratory Populations in Chironomus thummi thummi Kieff, Genetica, 1988, vol. 24, pp. 1795–1805.

    Google Scholar 

  • Kiknadze, I.I., Shilova, A., Kekris, I., et al., Karyotype and Morphology of Larvae in Chironomini, Novosibirsk: Atlas, 1991.

    Google Scholar 

  • King, M., Species Evolution: Role of Chromosome Changes, UK, Cambridge: Cambridge Univ. Press, 1993.

    Google Scholar 

  • Kleimann, R., Crerar, D., Paceli, R., Biochemistry of Acid Mine Drainage and a Method to Control Acid Formation, Mineral Engineering, 1981, vol. 33, pp. 300–305.

    Google Scholar 

  • Lagadic, L. and Caquet, Th., Invertebrates in Testing of Environmental Chemicals: Are they Alternatives?, Environ. Health Persp., 1998, vol. 106,Suppl. 2, pp. 593–613.

    Article  CAS  Google Scholar 

  • Michailova, P., Method of Breeding the Species from Family Chironomidae, Diptera in Experimental Conditions, CR. Acad. Bulg. des Sciences, 1985, vol. 38, no. 9, pp. 1179–1181.

    Google Scholar 

  • Michailova, P., Comparative Karyological Studies on Three Species of the Genus Glyptotendipes Kieff. (Diptera, Chironomidae) from Hungary and Bulgaria. Glyptotendipes salinus sp. n. from Bulgaria, Folia Biol., 1987, no. 1/2, pp. 43–56.

  • Michailova, P., The Polytene Chromosomes and Their Significance to the Systematics of the Family Chironomidae, Diptera, Acta Zool. Fenn., 1989, vol. 186, pp. 1–107.

    Google Scholar 

  • Michailova, P. and Belcheva, R., Different Effect of Lead on an External Morphology and Polytene Chromosomes of Glyptotendipes barbipes (Staeger) (Diptera, Chironomidae), Folia Biol., 1990, vol. 38, no. 1/4, pp. 83–88.

    Google Scholar 

  • Michailova, P. and Contreras-Lichtenberg, R., Contribution of the Knowledge of Glyptotendipes pallens (Meigen, 1804) and Glyptotendipes glaucus (Meigen, 1818), Ann. Naturhist. Mus., 1995, vol. 97B, pp. 395–410.

    Google Scholar 

  • Michailova, P., Petrova, N., Ramella, L., et al., Cytogenetic Characteristics of a Population of Chironomus reporius Meigen (Diptera, Chironomidae) from a Polluted Po River Station, Genetica, 1996, vol. 98, pp. 161–178.

    Article  Google Scholar 

  • Michailova, P., Ramella, L., Sella, G., and Bovero, S., C-Band Variation in Polytene Chromosomes of Chironomus riparius Mg (Diptera, Chironomidae) from a Polluted Piedmont Station (Italy), Cytobios., 1997, vol. 90, pp. 139–151.

    PubMed  CAS  Google Scholar 

  • Michailova, P., Petrova, N., Sella, G., et al., Structural—Functional Rearrangements in Chromosome G in Chironomus riparius Meigen (Diptera, Chironomidae) Collected from a Heavy Metal Polluted Area Near Turin, Italy, Environ. Pollut., 1998, vol. 103, pp. 27–35.

    Article  Google Scholar 

  • Michailova, P. and Todorova, J., Cytogenetic Characteristics of Glyptotendipes pallens Mg. (Diptera, Chironomidae) Reared in Standard Laboratory Conditions, Cytobios., 1998, vol. 94, pp. 151–160.

    Google Scholar 

  • Michailova, P. and Mettenen, A., Cytotaxonomical Variability of Chironomus plumosus L. and Chironomus anthracinus Zett. (Diptera, Chironomidae) from Industrial and Municipal Polluted Areas of Finland, Caryologia, 2000, vol. 53, no. 1, pp. 69–81.

    Google Scholar 

  • Michailova, P., Petrova, N., Bovero, S., et al., Effect of Environmental Pollution on the Chromosomal Variability of Chironomus riparius Meigen (Diptera, Chironomidae) Larvae from Two Piedmont Stations, Genetica, 2000, vol. 108, pp. 171–180.

    Article  PubMed  CAS  Google Scholar 

  • Micliailova, P., Ilkova, J., Petrova, N., and White, K., Rearrangements in the Salivary Gland Chromosomes of Chironomus riparius Mg. (Diptera, Chironomidae) Following Exposure to Lead, Caryologia, 2001a, vol. 54. pp. 349–363.

    Google Scholar 

  • Michailova, P., Petrova, N., Sella, G., et al., Genotoxic Effects of Chromium on Polytene Chromosomes of Chironomus riparius Meigen 1804 (Diptera, Chironomidae), Caryologia, 2001b, vol. 54, no. 1, pp. 59–71.

    Google Scholar 

  • Michailova, P., Todorova, K., and White, K., The Effect of Lead on the Salivary Gland Chromosomes of Glyptotendipes salinus Michailova (Chironomidae, Diptera), Biologia, Section, Cellular and Mol. Biol., 2002, vol. 57, no. 3, pp. 359–367.

    CAS  Google Scholar 

  • Michailova, P., Ilkova, I., and White, K.N., Functional and Structural Rearrangements of Salivary Gland Chromosomes of Chironomus riparius Mg. (Diptera, Chironomidae) in Response to Freshly Neutralized Aluminium, Environ. Pollut., 2003, vol. 123, pp. 193–207.

    Article  PubMed  CAS  Google Scholar 

  • Michailova, P., Petrova, N., Ilkova, J., et al., Genotoxic Effect of Copper on Salivary Gland Chromosomes of Chironomus riparius Meigen 1804 (Diptera, Chironomidae), Environ. Pollut., 2006, vol. 144, pp. 647–654.

    Article  PubMed  CAS  Google Scholar 

  • Michailova, P., Ilkova, J., Petrova, N., et al., Relationship between Chromosome Rearrangements and Repetitive DNA Clusters in Chironomus riparius Mg. (Diptera, Chironomidae) from Anthropogenic Polluted Palaearctic Regions, Compar. Cytogenet., 2007, vol. 1, pp. 45–49.

    Google Scholar 

  • Michailova, P., Ilkova, J., Kerr, R., and White, K., Effect of Trace Metals at Acid and Neutral Conditions on the Structure and Function of Polytene Chromosomes in Chironomus Species, Boletim do Museu Municipal do (Funchal), 2008, Suppl. 13, pp. 61–68.

    Google Scholar 

  • Michailova, P., Ilkova, J., Kerr, R., and White, K., Chromosome Variability in Chironomus acidophilus Keyl from the Afon Goach, UK—a River Subject to Long-Term Metal Pollution, Aquatic Insects, 2009a, vol. 31, no. 3, pp. 213–225.

    Article  Google Scholar 

  • Michailova, P., Szarek-Gwiazda, E., and Kovnacki, A., Effect of Contaminants on the Genome of Some Species of Genus Chironomus (Chironomidae, Diptera) Live in Sediments of Dunajec River and Czorsztyn Reservoir, Water, Air and. Soil Pollut., 2009b, vol. 202, pp. 245–258.

    Article  CAS  Google Scholar 

  • Michailova, P., Ilkova, J., Hankeln, T., et al., Somatic Breakpoints, Distribution of Repetative DNA and Non-LTR Retrotransposones Insertion Sites in the Chromosomes of Chironomus piger Strenzke (Diptera, Chironomidae), Genetica, 2009c, vol. 135, pp. 137–148.

    Article  PubMed  CAS  Google Scholar 

  • Mottus, R., Reeves, R., and Grigliatti, T., Butyrate Suppression of Position Effect Variegation in Drosophila melanogaster, Mol. Genet., 1980, vol. 178, pp. 465–169.

    Article  CAS  Google Scholar 

  • Nocentini, S., Inhibition of DNA Replication and Repair by Cadmium in Mammalian Cells. Protective Interaction of Zinc, Nucl. Acids Res., 1987, vol. 26, pp. 4211–4225.

    Article  Google Scholar 

  • Petrova, N. and Michailova, P., Cytogenetic Characteristics of Chironomus bernensis Wülker and Klötzli (Diptera, Chironomidae) from a Heavy Metal Polluted Station in Northern Italy, Ann. Zool., 2002, vol. 52, no. 2, pp. 227–233.

    Google Scholar 

  • Petrova, N.A., Michailova, P., and Ilkova, J., Comparative Cytogenetic Variation of the Salivary Gland Polytene Chromosomes in Chironomus riparius Mg. 1804 (Diptera, Chironomidae) from Two Polluted Biotopes of Bulgaria and Russia, Rus. J. Genet., 2004, vol. 40, no. 1, pp. 40–48.

    Article  CAS  Google Scholar 

  • Planello, R., Martinez-Guitarte, L., and Morcillo, G., Ribosomal Genes As Early Target of Cadmium-Induced Toxicity in Chironomus riparius Larvae, Sci. Total Environ., 2007, vol. 373, pp. 113–121.

    Article  PubMed  CAS  Google Scholar 

  • Saether, O., Chironomid Communities as Water Quality Indicators, Holarctic Ecol., 1979, vol. 2, pp. 65–74.

    Google Scholar 

  • Sanderson, C., McLachlan Crapper, D.R., and De Boni, U., Altered Steroid Induced Puffing by Chromatin Bound Aluminium in a Polytene Chromosome of the Blackfly Simulium vittatum, Canad. J. Genet. Cytol., 1980, vol. 24, pp. 27–36.

    Google Scholar 

  • Santa-Cruz, M., Villanueva, A., and Diez, L., Effect of Galactose Treatment in the Puffing Pattern of Chironomus thummi Balbiani Rings, Chromosoma, 1978, vol. 69, pp. 93–100.

    Article  PubMed  CAS  Google Scholar 

  • Schaefer, J. and Schmidt, E., Different Repetition Frequencies of 120 Base-Pair DNA Element and Its Arrangement in Chironomus thummi thummi and C. piger, Chromosoma, 1981, vol. 84, pp. 61–66.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, E., Clustred and Interspersed Repetitive DNA Sequence Family of Chironomids, J. Mol. Biol., 1984, vol. 178, pp. 1–5.

    Article  PubMed  CAS  Google Scholar 

  • Sella, G., Robotti, C., Michailova, P., and Ramella, L., Repetitive DNA Size Variation in Three Sections of the Chromosome EF in a Population of Chironomus riparius Mg (Diptera, Chironomidae) from Piedmont (Italy), Caryologia, (Firenze), 2001, vol. 54, no. 2, pp. 155–160.

    Google Scholar 

  • Sella, G., Bovero, S., Ginpero, M., et al., Inherited and Somatic Cytogenetic Variability in Palaearctic Populations of Chironomus riparius Meigen (Diptera, Chironomidae), Genome, 2004, vol. 47, pp. 332–244.

    Article  PubMed  CAS  Google Scholar 

  • Timmemians, K., Peeters, W., and Tonkes, M., Cadmium, Zinc, Lead and Copper in Larvae of Chironomus riparius (Diptera, Chironomidae) Uptake and Effects, Trace Metal in Cotoxicokinetics of Chironomids: Ph. D. Dissertation, Amsterdam, 1989, pp. 89–121.

  • Walker, C., Kaiser, K., and Klein, W., et al., Alternative Testing Methodologies for Ecotoxicity, Environ. Health Persp., 1998, vol. 106,Suppl. 2, pp. 441–451.

    Article  CAS  Google Scholar 

  • Warwick, W.F., Morphological Defonniries in Chironomidae (Diptera) Larval as Biological Indicators of Toxic Stress in Toxic Contaminants and Ecosystem Health, Evan, M.S., Ed., A Great Lakes Focus, John Wiley and Sons, 1988, p. 80.

  • Warwick, W.F., The Use of Morphological Deformities in Chironomid Larvae for Biological Effects Monitoring. Inland Waters Directorate Scientific Publications, Series 173, Environment Canada ON, 1990, pp. 1–34.

  • Wieslander, L., The Balbiani Ring Multigene Family: Coding Sequences and Evolution of a Tissue-Specific Function, Proc. Nucl. Acids Res., 1994, vol. 48, pp. 275–313.

    CAS  Google Scholar 

  • Wülker, W. and Klötzli, M., Revision der Gattung Chironomus Meig. IV. Arten des lacunarius Komlexes, Arch. Hydrobiol., 1973, Vol. 72, no. 4, pp. 474–489.

    Google Scholar 

  • Yagi, S., Effects of Legation on Ethanol Induced Balbiani Ring Puffing in Salivary Gland of Chironomus, Chromosoma, 1984, vol. 89, pp. 274–279.

    Article  Google Scholar 

  • Zampicinini, G.P., Blinov, A., Cervella, P., and Sella, G., Insertional Polymorphism of a Non-LTR Mobile Element (NLRCth1) in European Populations of Chironomus riparius (Diptera, Chironomidae) as Detected by Transposon Insertion Display, Genome, 2004, vol. 47, no. 11, pp. 54–1163.

    Google Scholar 

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Michailova, P.V. Rearrangements in chironomidae (Diptera) genomes induced by various environmental stress factors. Russ J Genet Appl Res 1, 10–20 (2011). https://doi.org/10.1134/S2079059711010035

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