Abstract
The dominant male sex determiner in chromosome III of the midge Chironomus thummi thummi is closely linked to a large cluster of tandem-repetitive DNA elements, the Cla elements, which are otherwise highly repetitive and distributed over more than 200 sites on all chromosomes. Chromosome III displays a hemizygous cluster of Cla elements in males but not in females. The chromosomal location of this hemizygous Cla element cluster is in the region of the male determiner M as localized by cytogenetic analysis. With Cla elements as hybridization probe, it was possible to clone a large part of the sex determining region. Molecular analysis of the DNA of males and females in this region displayed a number of differences between the two sexes. One striking difference is an unusual transposable element associated with the male sex determining region. The sex determining region also contains several other tandem-repetitive DNA elements in addition to the Cla elements. They are interspersed with single copy DNA. The accumulation of repetitive elements in the sex determining region is interpreted as the result of a lack of recombination between the male/female heteromorphic region, although recombination in the other sections of chromosome III occurs.
Similar content being viewed by others
References
Beermann W (1955) Geschlechtsbestimmung und Evolution der genetischen Y-Chromosomen bei Chironomus. Biol Zentralbl 74:525–544
Beermann W, Bauer H (1952) Der Chromosomenzyklus der Orthocladiinen (Nematocera, Diptera). Z Naturforsch 7b:557–563
Bridges CB (1922) The origin of variations in sexual and sex limited characters, Am Nat 56:51–63
Bull JJ (1983) Evolution of sex determining mechanisms. The Benjamin/Cummings Publishing Company, Menlo Park, Calif
Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033
Chen EY, Seeburg PH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170
Darlington CD (1958) Evolution of genetic systems, 2nd ed. Basic Books, New York
Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
Fischer J, Tichy H (1980) Über eine Heterochromatin-Mutation aus einer Wildpopulation von Chironomus nuditarsis. I. Zur Funktion des veränderten Genom-Abschnittes. Genetica 54:41–43
Green MM (1980) Transposable elements in Drosophila and other diptera. Annu Rev Genet 14:109–120
Hägele K (1985) Identification of a polytene chromosome band containing a male sex determiner of Chironomus thummi thummi. Chromosoma 91:167–171
Hägele K (1986) Localization of a male sex determining chromosome region in Chironomus thummi piger. Genetica 70:187–190
Hankeln T (1990) Molekulare Analyse phylogenetisch Bedeutsamer repetitiver DNA bei Chironomiden. Dissertation Ruhr-Universitaet Bochum, Germany
Hennig W (1990) The Y chromosome of Drosophila. In: Adolph KW (ed) Chromosomes: Eukaryotic, procaryotic, and viral, vol I, CRC Press, Boca Raton, Florida, USA, pp 213–238
Jeffreys AJ, Wilson V, Thein SL (1985) Hypervariable minisatellite regions in human DNA. Nature 314:67–73
John B (1988) The biology of heterochromatin. In: Verma (ed) Heterochromatin. Cambridge University Press, New York, pp 1–128
Keyl H-G (1962) Chromosomenevolution bei Chironomus. II. Chromosomenumbauten und phylogenetische Beziehungen der Arten. Chromosoma 13:464–514
Keyl H-G, Strenzke K (1956) Taxonomie und Cytologie von zwei Subspezies der Art Chironomus thummi. Z Naturforsch 11b:727–735
Kirchhoff C (1988) GATA tandem repeats detect minisatellite regions in blowfly DNA (Diptera: Calliphoridae). Chromosoma 96:107–111
Langer-Safer PR, Levine M, Ward DC (1982) Immunological method for mapping genes on Drosophila polytene chromosomes. Proc Natl Acad Sci USA 79:4381–4385
Mainx F (1964) The genetics of Megaselia scalaris Loew (Phoridae): A new type of sex determination in Diptera. Am Nat 98:415–430
Mainx F (1966) Die Geschlechtsbestimmung von Megaselia scalaris Loew (Phoridae). Z Vererbungslehre 98:49–60
Martin J, Lee BTO (1988) Sex determiners and speciation in the genus Chironomus. Pacific Sci 42:51–55
Martin J, Kuvangkadilok C, Peart DH, Lee BTO (1980) Multiple sex determining regions in a group of related Chironomus species (Diptera, Chironomidae). Heredity 44:367–382
Muller HJ (1932) Some genetic aspects of sex. Am Nat 66:118–138
Nakamura Y, Leppert M, O'Connell P, Wolff R, Holm T, Culver M, Martin C, Fujimoto E, Hoff M, Kumlin E, White R (1987) Variable number of tandem repeat (VNTR) markers for human gene mapping. Science 235:1616–1622
Nöthiger R, Steinmann-Zwicky M (1985) A single principle for sex determination in insects. Cold Spring Harbor Symp Quant Biol L: 615–621
Ohno S (1967) Sex chromosomes and sex-linked genes. Springer-Verlag, Berlin-Heidelberg-New York
Ribbert D (1967) Die Polytänchromosomen der Borstenbildungszellen von Calliphora erythrocephala. Chromosoma 21:296–344
Rosin S, Fischer J (1972) Polymorphismus des Realisators für männliches Geschlecht bei Chironomus. Rev Suisse Zool 79:119–141
Saiki RK, Gyllenstein UB, Erlich HA (1988) The polymerase chain reaction. In: Davie KE (ed) Genome analysis. A practical approach. IRL Press, Oxford
Sambrook I, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd edition, Cold Spring Harbor Laboratory Press, New York
Schaefer J, Schmidt ER (1981) Different repetition frequencies of a 120 base-pair DNA element and its arrangement in Chironomus thummi thummi and Chironomus thummi piger. Chromosoma 84:61–66
Schmidt ER (1981) The development of a 120 basepair repetitive DNA sequence in Chironomus thummi is correlated to the duplication of defined chromosomal segments. FEBS Lett 129:21–24
Schmidt ER (1984) Clustered and interspersed repetitive DNA sequence family of Chironomus. The nucleotide sequence of the Cla-elements and of various flanking sequences J Mol Biol 178:1–15
Schmidt ER (1992) Multicolor in-situ-hybridization — a useful technique for precise gene localisation. Sci Tech Inf X:80–84
Schmidt ER, Vistorin G, Keyl H-G (1980) An AT-rich DNA component in the genomes of Chironomus thummi thummi and Chironomus thummi piger. Chromosoma 76:35–45
Schmidt ER, Keyl H-G, Hankeln T (1988) In situ localization of two hemoglobin gene clusters in the chromosomes of 13 species of Chironomus. Chromosoma 96:353–359
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517
Steinemann M (1982) Multiple sex chromosomes in Drosophila miranda: a system to study the degeneration of a chromosome. Chromosoma 86:59–76
Steinemann M, Steinemann S (1992) Degenerating Y chromosome of Drosophila miranda: A trap for retrotransposons. Proc Natl Acad Sci USA 89:7591–7595
Traut W, Willhöft U (1990) A jumping sex determining factor in the fly Megaselia scalaris. Chromosoma 99:407–412
Ulanovsky LE, Trifonov EN (1987) Estimation of wedge components in curved DNA. Nature 32:720–722
Ullerich F-H (1963) Geschlechtschromosomen und Geschlechts-bestimmung bei einigen Calliphorinen (Calliphoridae, Diptera). Chromosoma 14:45–110
Willhöft U, Traut W (1990) Molecular differentiation of the homomorphic sex chromosomes in Megaselia scalaris (Diptera) detected by random DNA probes. Chromosoma 99:237–242
Winge O (1934) The experimental alteration of sex chromosomes into autosomes and vice versa, as illustrated by Lebistes. CR Lab Carlsberg Ser Phys 21:1–49
Yanisch-Peron C, Vieira I, Messing I (1985) Improved M13 cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC 19 vectors. Gene 33:103–119
Author information
Authors and Affiliations
Additional information
Communicated by: W. Hennig
Rights and permissions
About this article
Cite this article
Kraemer, C., Schmidt, E.R. The sex determining region of Chironomus thummi is associated with highly repetitive DNA and transposable elements. Chromosoma 102, 553–562 (1993). https://doi.org/10.1007/BF00368348
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00368348