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Characterization of two unrelated satellite DNA families in the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera, Chrysomelidae)

Published online by Cambridge University Press:  01 March 2013

Pedro Lorite ,
M. Isabel Torres  and
Teresa Palomeque
Pedro Lorite
Affiliation:
Departamento de Biología Experimental, Universidad de Jaén, 23071 Jaén, Spain
M. Isabel Torres
Affiliation:
Departamento de Biología Experimental, Universidad de Jaén, 23071 Jaén, Spain
Teresa Palomeque*
Affiliation:
Departamento de Biología Experimental, Universidad de Jaén, 23071 Jaén, Spain
*
*Author for correspondence Phone: (+34) 953-212156 E-mail: [email protected]
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Abstract

The Colorado potato beetle (Leptinotarsa decemlineata, family Chrysomelidae), a phytophagous insect, which feeds preferably on potatoes, constitutes a serious pest of this crop and causes extensive damage to tomatoes and eggplants. It has a remarkable ability to develop resistance quickly against insecticides and shows a diversified and flexible life history. Consequently, the control of this pest has become difficult, requiring the development of new alternative biotechnology-based strategies. Such strategies require a thorough knowledge of the beetle's genome, including the repetitive DNA. Satellite DNA (stDNA), composed of long arrays of tandemly arranged repeat units, constitutes the major component of heterochromatin and is located mainly in centromeric and telomeric chromosomal regions. We have studied two different unrelated satellite-DNA families of which the consensus sequences were 295 and 109 bp in length, named LEDE-I and LEDE-II, respectively. Both were AT-rich (70.8% and 71.6%, respectively). Predictive models of sequence-dependent DNA bending and the study of electrophoretic mobility on non-denaturing polyacrylamide gels have shown that the DNA was curved in both satellite-DNA families. Among other features, the chromosome localization of both stDNAs has been studied. In situ hybridization performed on meiotic and mitotic nuclei showed chromosomes, including the X chromosome, with zero, one, or two stDNAs. In recent years, it has been proposed that the repetitive DNA may play a key role in biological diversification processes. This is the first molecular and cytogenetic study conducted on L. decemlineata repetitive DNA and specifically on stDNA, which is one of the important constituents of eukaryotic genomes.

Keywords

Colorado potato beetleLeptinotarsasatellite DNAin situ hybridization
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 5 , October 2013 , pp. 538 - 546
Copyright
Copyright © Cambridge University Press 2013 

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References

Abdeen, A., Virgós, A., Olivella, E., Villanueva, J., Avilés, X., Gabarra, R. & Prat, S. (2005) Multiple insect resistance in transgenic tomato plants over-expressing two families of plant proteinase inhibitors. Plant Molecular Biology 57, 189–202.Google Scholar
Alyokhin, A. (2009) Colorado potato beetle management on potatoes: current challenges and future prospects. Vegetable and Cereal Science and Biotechnology 3(Special Issue), 10–19.Google Scholar
Altschul, S.F., Stephen, F., Madden, L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Barceló, F., Pons, J., Petitpierre, E., Barjau, I. & Portugal, J. (1997) Polymorphic curvature of satellite DNA in three subspecies of the beetle Pimelia sparsa. European Journal of Biochemistry 244, 318–324.Google Scholar
Baus Lončar, M., Paić, F. & Ugarković, Đ. (2005) Molecular cytogenetic study of heterochromatin in some coleopteran insects. Entomologia Croatica 9, 47–56.Google Scholar
Betrán, E., Rozas, J., Navarro, A. & Barbadilla, A. (1997) The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 146, 89–99.Google Scholar
Bosco, G., Campbell, P., Leiva-Neto, J.T. & Markow, T.A. (2007) Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177, 1277–1290.Google Scholar
Charlesworth, B., Sniegowski, P. & Stephan, W. (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371, 215–220.Google Scholar
Dover, G. (2002) Molecular drive. Trends in Genetics 18, 587–589.Google Scholar
Escribá, M.C., Greciano, P.G., Méndez-Lago, M., de Pablos, B., Trifonov, V.A., Ferguson-Smith, M.A., Goday, C. & Villasante, A. (2011) Molecular and cytological characterization of repetitive DNA sequences from the centromeric heterochromatin of Sciara coprophila. Chromosoma 120, 387–397.CrossRefGoogle ScholarPubMed
Faulkner, G.J. & Carninci, P. (2009) Altruistic functions for selfish DNA. Cell Cycle 15, 2895–9000.Google Scholar
Feliciello, I., Chinali, G. & Ugarković, D. (2011) Structure and population dynamics of the major satellite DNA in the red flour beetle Tribolium castaneum. Genetica 139, 999–1008.CrossRefGoogle ScholarPubMed
Goodsell, D.S. & Dickerson, R.E. (1994) Bending and curvature calculations in B-DNA. Nucleic Acids Research 22, 5497–5503.Google Scholar
Grechko, V.V. (2011) Repeated DNA sequences as an engine of biological diversification. Molecular Biology 45, 704–727.Google Scholar
Hsiao, T.H. & Hsiao, C. (1983) Chromosomal analysis of Leptinotarsa and Labidomera species (Coleoptera: Chrysomelidae). Genetica 60, 139–150.Google Scholar
Hua-Van, A., Le Rouzic, A., Boutin, T.S., Filée, J. & Capy, P. (2011) The struggle for life of the genome's selfish architects. Biology Direct 17, 6–19.Google Scholar
ICGEBnet (2012) A Computer Resource for Molecular Biology presents. Available online at http://hydra.icgeb.trieste.it/dna/bend_it.html (accessed 11 June 2012).Google Scholar
Kalitsis, P. & Choo, K.H. (2012) The evolutionary life cycle of the resilient centromere. Chromosoma 121, 327–340.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Lorite, P., Palomeque, T., Garnería, I. & Petitpierre, E. (2001) Characterization and chromosome location of satellite DNA in the leaf beetle Chrysolina americana (Coleoptera, Chrysomelidae). Genetica 110, 143–150.Google Scholar
Lorite, P., Carrillo, J.A., Garneria, I., Petitpierre, E. & Palomeque, T. (2002) Satellite DNA in the elm leaf beetle, Xanthogaleruca luteola (Coleoptera, Chrysomelidae): characterization, interpopulation analysis, and chromosome location. Cytogenetics and Genome Research 98, 302–307.Google Scholar
Lorite, P., Carrillo, J.A., Aguilar, J.A. & Palomeque, T. (2004) Isolation and characterization of two families of satellite DNA with repetitive units of 135 bp and 2.5 kb in the ant Monomorium subopacum (Hymenoptera, Formicidae). Cytogenetics and Genome Research 105, 83–92.Google Scholar
Lobov, I.B., Tsutsui, K., Mitchell, A.R. & Podgornaya, O.I. (2001) Specificity of SAF-A and lamin B binding in vitro correlates with the satellite DNA bending state. Journal of Cellular Biochemistry 83, 218–229.CrossRefGoogle ScholarPubMed
Matyasek, R., Fulnecek, J., Leitch, A.R. & Kovarik, A. (2011) Analysis of two abundant, highly related satellites in the allotetraploid Nicotiana arentsii using double-strand conformation polymorphism analysis and sequencing. New Phytology 192, 747–759.Google Scholar
McClean, P. (1998) DNA – basics of structure and analysis. Nucleic acid hybridizations. Available online at http://www.ndsu.edu/pubweb/~mcclean/plsc731/dna/dna6.htm (accessed 21 November 2012).Google Scholar
Mravinac, B. & Plohl, M. (2010) Parallelism in evolution of highly repetitive DNAs in sibling species. Molecular Biology and Evolution 27, 1857–1867.Google Scholar
Mravinac, B., Plohl, M., & Ugarković, Đ. (2005) Preservation and high sequence conservation of satellite DNAs suggest functional constraints. Journal of Molecular Evolution 61, 542–550.Google Scholar
Munteanu, M. G., Vlahovicek, K., Parthasaraty, S., Simon, I. & Pongor, S. (1998) Rod models of DNA: sequence-dependent anisotropic elastic modelling of local bending phenomena. Trends in Biochemical Sciences 23, 341–346.Google Scholar
Nei, M. & Kumar, S. (2000) Molecular Evolution and Phylogenetics. Oxford University Press, New York.Google Scholar
Palomeque, T. & Lorite, P. (2008) Satellite DNA in insects – a review. Heredity 100, 564–573.Google Scholar
Palomeque, T., Muñoz-López, M., Carrillo, J.A. & Lorite, P. (2005) Characterization and evolutionary dynamics of a complex family of satellite DNA in the leaf beetle Chrysolina carnifex (Coleoptera, Chrysomelidae). Chromosome Research 13, 795–807.CrossRefGoogle ScholarPubMed
Pérez-Gutiérrez, M.A., Suárez-Santiago, V.N., López-Flores, I., Romero, A.T. & Garrido-Ramos, M.A. (2012) Concerted evolution of satellite DNA in Sarcocapnos: a matter of time. Plant Molecular Biology 78, 19–29.Google Scholar
Petitpierre, E., Segarra, C. & Juan, C. (1993) Genome size and chromosomal evolution in leaf beetles (Coleoptera, Chrysomelidae). Hereditas 119, 1–6.Google Scholar
Pezer, Z. & Ugarković, Đ. (2009) Transcription of pericentromeric heterochromatin in beetles–satellite DNAs as active regulatory elements. Cytogenetic and Genome Research 124, 268–276.Google Scholar
Piiroinen, S., Lindström, L. & Lyytinen, A. (2010) Resting metabolic rate can vary with age independently from body mass changes in the Colorado potato beetle, Leptinotarsa decemlineata. Journal of Insect Physiology 56, 277–282.Google Scholar
Petek, M., Turnšek, N., Gašparič, M.B., Novak, M.P., Gruden, K., Slapar, N., Popovič, T., Štrukelj, B., Gruden, K., Štrukelj, B. & Jongsma, M.A. (2012) A complex of genes involved in adaptation of Leptinotarsa decemlineata larvae to induced potato defense. Archives of Insect Biochemistry and Physiology 79, 153–181.Google Scholar
Plohl, M., Luchetti, A., Meštrović, N. & Mantovani, B. (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero) chromatin. Gene 15, 72–82.Google Scholar
Plohl, M., Meštrović, N. & Mravinac, B. (2012) Satellite DNA evolution pp. 126–152in Garrido-Ramos, M.A. (Ed) Repetitive DNA. Genome Dynamic vol. 7. Basel, Karger.Google Scholar
Pons, J., Bruvo, B., Petitpierre, E., Plohl, M., Ugarkovic, D. & Juan, C. (2004) Complex structural features of satellite DNA sequences in the genus Pimelia (Coleoptera: Tenebrionidae): random differential amplification from a common ‘satellite DNA library’. Heredity 92, 418–427.Google Scholar
Robles, F., De la Herrán, R., Ludwig, A., Ruiz Rejón, C., Ruiz Rejón, M. & Garrido-Ramos, M.A. (2004) Evolution of ancient satellite DNAs in sturgeon genomes. Gene 18, 133–142.Google Scholar
Strachan, T., Webb, D. & Dover, G.A. (1985) Transition stages of molecular drive in multiple-copy DNA families in Drosophila. EMBO Journal 4, 1701–1708.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.Google Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Ugarkovic, Đ., Petitpierre, E., Juan, C. & Plohl, M. (1995) Satellite DNAs in Tenebrionid species: structure, organization and evolution. Croatica Chemica Acta 68, 627–638.Google Scholar
Vlahovicek, K., Kajan, L. & Pongor, S. (2003) DNA analysis servers: plot.it, bend.it, model.it and IS. Nucleic Acids Research 31, 3686–3687.Google Scholar
Whalon, M.E., Mota-Sanchez, D., Hollingworth, R.M. & Duynslager, L. (2012) Arthropod Pesticide resistance data base. Available online at http://www.pesticideresistance.org/ (accessed 21 November 2012).Google Scholar
Zhu, F., Xu, J., Palli, R., Ferguson, J. & Palli, S.R. (2011) Ingested RNA interference for managing the populations of the Colorado potato beetle, Leptinotarsa decemlineata. Pest Management Science 67, 175–182.Google Scholar
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