Abstract
Digestion of genomic DNA from seven species of Tribolium (Coleoptera) with Sau3AI, TaqI and ClaI restriction enzymes shows the presence of remarkable amounts of highly repetitive DNA sequences in these species. In Tribolium freemani the sequences are tandemly repeated with a satellite monomer of 166 bp, A-T rich (70.5 per cent), representing 31 per cent of the total genome and located in centromeric chromosome areas as demonstrated by in situ hybridization. The sequence has the potential to form secondary structures such as stems or cruciforms due to the presence of frequent inverted repeats. Tribolium castaneum, T. anaphe and T. madens show homologous sequences to T. freemani satellite DNA but T. confusum, T. audax, T. brevicornis and other tenebrionid beetles, such as Tenebrio molitor and Misolampus goudoti, do not. A phylogenetic dendrogram, based on the homology and abundance of highly repetitive sequences deduced by dot-blot hybridization, chemotaxonomic and karyological characters, is proposed for the seven studied species of Tribolium.
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Alvarez-Fuster, A, Juan, C, and Petitpierre, E. 1991. Genome size in Tribolium flour-beetles: inter-and intraspecific variation. Genet Res, 58, 1–5.
Ambros, P F, Matzke, M A, and Matzke, A J M. 1986. Detection of a 17 kb unique sequence (T-DNA) in plant chromosomes. Chromosoma, 94, 11–18.
Arnason, U, Höglund, M, and Widegren, B. 1984. Conservation of a highly repetitive DNA in cetaceans. Chromosoma, 89, 238–242.
Arnason, U, and Widegren, B. 1986. Pinniped phylogeny enlighted by molecular hybridizations using highly repetitive DNA. Mol Biol Evol, 3, 356–365.
Arnason, U, and Widegren, B. 1989. Composition and chromosomal localization of cetacean highly repetitive DNA with special reference to the blue whale, Balenoptera musculus. Chromosoma, 98, 323–329.
Beltz, G A, Jacobs, K A, Eickbush, T H, Cherbas, P T, and Kafatos, F C. 1983. Isolation of multigene families and determination of homologies by filter hybridization methods. Meth Enzymol, 100, 266–285.
Brown, S J, Henry, J K, Black, IV, W C, and Denell, R E. 1990. Molecular genetic manipulation of the red flour beetle: genome organization and cloning of a ribosomal protein gene. Insect Biochem, 20, 185–193.
Davis, C A, and Wyatt, G R. 1989. Distribution and sequence homogeneity of an abundant satellite in the beetle, Tenebrio molitor. Nucl Acids Res, 17, 5579–5586.
Dod, B, Mottez, E, Desmarais, E, Bonhomme, F, and Roizes, G. 1989. Concerted evolution of light satellite DNA in genus Mus implies amplification and homogenization of large blocks of repeats. Mol Biol Evol, 6, 478–491.
Dover, G A. 1982. Molecular drive: a cohesive mode of species evolution. Nature, 285, 111–117.
Fanning, T G, Modi, W S, Wayne, R K, and O'Brien, S J. 1988. Evolution of heterochromatin-associated satellite DNA loci in felids and canids (Carnivora). Cytogenet. Cell Genet, 48, 214–219.
Fanning, T G, Seuanez, H N, and Forman, L. 1989. Satellite DNA sequences in the neotropical marmoset Callimico goeldii (Primates, Platyrrhini). Chromosoma, 98, 396–401.
Feinberg, A P, and Vogelstein, B. 1983. A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem, 132, 6–13.
Fowler, R F, and Skinner, D M. 1985. Cryptic satellites rich in inverted repeats comprise 30% of the genome of a hermit crab. J Biol Chem, 260, 1296–1303.
Hinton, H E. 1948. A synopsis of the genus Tribolium MacLey with some remarks on the evolution of its species groups. Bull Entomol Res, 39, 13–55.
Howard, R W. 1987. Chemosystematic studies of the Triboliini (Coleoptera: Tenebrionidae): phylogenetic inferences from the defensive chemicals of eight Tribolium spp., Palorus ratzeburgi (Wissmann), and Latheticus oryzae Warterhouse. Ann Entomol Soc Am, 80, 398–405.
Israelewski, N. 1983. Structure and function of an AT-rich, interspersed repetitive sequence from Chironomus thummi: solenoidal DNA, 142 bp palindrome-frame and homologies with the sequence for site specific recombination of bacterial transposons. Nucl Acid Res, 11, 6985–6996.
Juan, C, Gosalvez, J, and Petitpierre, E. 1990. Improving beetle karyotype analysis: restriction endonuclease banding of Tenebrio molitor fixed chromosomes. Heredity, 65, 157–162.
Juan, C, Gosalvez, J, Mezzanotte, R, and Petitpierre, E. 1991. Cytological and biochemical characterization of the in situ endonuclease digestion of fixed Tenebrio molitor chromosomes. Chromosoma, 100, 432–438.
Juan, C, and Petitpierre, E. 1989. C-banding and DNA content in seven species of Tenebrionidae (Coleoptera). Genome, 32, 834–839.
Juan, C, and Petitpierre, E. 1990. Karyological differences among Tenebrionidae (Coleoptera). Genetica, 80, 101–108.
Koenen, M. 1989. Recovery of DNA fragments from agarose gels using liquid nitrogen. Trends Genet, 5, 137.
Lawrence, J F. 1982. Coleoptera. In: Parker J. A. (ed.) Synopsis and Classification of Living Organisms. McGraw-Hill, New York.
Maniatis, T, Fritsch, E F, and Sambrook, J. 1982. Molecular Cloning A Laboratory Manual. Cold Spring Harbor Laboratory, New York.
Manuelidis, L, Langer-Safer, P R, and Ward, D C. 1982. High resolution mapping of satellite DNA using biotin-labeled DNA probes. J Cell Biol, 95, 619–625.
Martinez-Balbas, A, Rodriguez-Campos, A, Garcia-Ramirez, M, Sainz, J, Carrera, J, Aymami, J, and Azorin, F. 1989. Satellite DNAs contain sequences that induce curvature. Biochemistry, 29, 2342–2348.
Musich, P R, Brown, F L, and Maio, J J. 1980. Highly repetitive component alpha and related alphoid DNAs in man and monkeys. Chromosoma, 80, 331–348.
Petitpierre, E, Gatewood, J, and Schmid, C W. 1988. Satellite DNA from the mealworm beetle Tenebrio molitor. Experientia, 44, 498–499.
Plohl, M, Borstnik, B, Ugarkovic, D, and Gamulin, V. 1990. Sequence-induced curvature of Tenebrio molitor satellite DNA. Biochemie, 72, 665–670.
Redi, C A, Garagna, S, Dellavalle, G, Bottiroli, G, Dell'Orto, P, Viale, G, Pevareli, F A, Raimondi, E, and Forejt, J. 1990. Differences in the organization and chromosomal allocation of satellite DNA between the European long tailed house mice Mus domesticus and Mus musculus. Chromosoma, 99, 11–17.
Samallow, P B, Dawson, P S, and Russel, A R. 1983. X-linked and autosomal inheritance patterns of homologous genes in two species of Tribolium. Biochem Genet, 21, 167–176.
Sanger, F, Nicklen, S, and Coulson, A R. 1977. DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci, USA, 74, 5463–5467.
Shimeld, L. 1989. A cytogenetic examination of eight species of Tribolium. Tribolium Inf Bull, 29, 102–107.
Skinner, D M. 1977. Satellite DNAs. Bioscience, 27, 790–796.
Smith, S G. 1952. The evolution of heterochromatin in the genus Tribolium (Tenebrionidae: Coleoptera). Chromosoma, 4, 585–610.
Sokoloff, A. 1972. The Biology of Tribolium, With Special Emphasis on Genetic Aspects, Vol I. Oxford University Press, Oxford.
Southern, E M. 1975. Long periodicities in mouse satellite DNA. J Mol Biol, 94, 51–70.
Ugarkovic, D, Plohl, M, and Gamulin, V. 1989. Sequence variability of satellite DNA from the mealworm Tenebrio molitor. Gene, 83, 181–183.
Wool, D. 1982. Critical examination of postulated cladistic relationships among species of flour beetles (Tribolium, Tenebrionidae, Coleoptera). Biochem Genet, 20, 333–349.
Wu, C I, Lyttle, T W, Wu, M L, and Lin, G F. 1988. Association between a satellite DNA sequence and the responder of segregation distorter in D. melanogaster. Cell, 54, 179–189.
Acknowledgements
We are very grateful to Dr E. Desmarais for his valuable help on DNA cloning and sequencing and to Dr J. Gosalvez who critically read the manuscript. The discussions with Drs C. R. Altaba and M. Palmer and suggestions from an anonymous referee substantially improved the paper. This research has been supported by projects DGICYT numbers PB87/0584 and PB90/ 0357 (Spain) and Acciones integradas Hispano Britanicas' number 8A. The satellite DNA sequence has been deposited in EMBL under accession number X58539.
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Juan, C., Vazquez, P., Rubio, J. et al. Presence of highly repetitive DNA sequences in Tribolium flour-beetles. Heredity 70, 1–8 (1993). https://doi.org/10.1038/hdy.1993.1
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DOI: https://doi.org/10.1038/hdy.1993.1
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