Molecular and physical characterization of the complex pericentromeric heterochromatin of the vole species microtus thomasi

Cytogenetic and Genome Research

Volumn 144, Issue 2, 2014, Pages 131-141

  Rovatsos, Michalis T ^a   Marchal, Juan A ^b   Romero Fernández, Ismael ^b   Cano Linares, Maribel ^b   Fernández, Francisco J ^b   Giagia Athanasopoulou, Eva B ^c   Sánchez, Antonio ^b  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF JAÉN   (Spain)

^c UNIVERSITY OF PATRAS   (Greece)

Author keywords

Chromosomal races; Heterochromatin; Microtus; Pericentromeric region; Pericentromeric repeated sequences; Sex chromosomes

Indexed keywords

GENOMIC DNA; REPETITIVE DNA; SATELLITE DNA; DNA; HETEROCHROMATIN;

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME PREPARATION; CONSENSUS SEQUENCE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; HETEROCHROMATIN; HYBRIDIZATION; IN SITU HYBRIDIZATION; KARYOTYPE; MALE; MICROTUS; MICROTUS THOMASI; NONHUMAN; PRIORITY JOURNAL; SOUTHERN BLOTTING; TANDEM REPEAT; VOLE; X CHROMOSOME; Y CHROMOSOME; ANIMAL; ARVICOLINAE; CELL LINEAGE; CENTROMERE; CENTROSOME; CHEMISTRY; CROSS BREEDING; GENETICS; KARYOTYPING; METABOLISM; NUCLEOTIDE REPEAT; PHENOTYPE; TELOMERE; ULTRASTRUCTURE;

MICROTUS; MICROTUS THOMASI; MURIDAE;

ANIMALS; ARVICOLINAE; CELL LINEAGE; CENTROMERE; CENTROSOME; CROSSES, GENETIC; DNA; FEMALE; HETEROCHROMATIN; IN SITU HYBRIDIZATION, FLUORESCENCE; KARYOTYPING; MALE; PHENOTYPE; REPETITIVE SEQUENCES, NUCLEIC ACID; TELOMERE;

EID: 84925225006     PISSN: 14248581     EISSN: 1424859X     Source Type: Journal    
DOI: 10.1159/000368648     Document Type: Article

References (63)

1. Acosta MJ, Marchal JA, Martínez S, Puerma E, Bullejos M, et al: Characterization of the satellite DNA Msat-160 from the species Chionomys nivalis (Rodentia, Arvico linae). Genetica 130: 43-51 (2007
2. Acosta MJ, Marchal JA, Fernández-Espartero C, Bullejos M, Sánchez A: Retroelements (LINEs and SINEs) in vole genomes: Differential distribution in the constitutiv e heterochromatin. Chromosome Res 16: 949-959 (2008
3. Acosta MJ, Marchal JA, Mitsainas GP, Rovatsos MT, Fernández-Espartero CH, et al: A new pericentromeric repeated DNA sequence in Microtus tho masi . Cytogenet Genome Res 124: 27-36 (2009
4. Acosta MJ, Marchal JA, Fernández-Espartero C, Romero-Fernández I, Rovatsos MT, et al: Characterization of the satellite DNA Msat-160 from species o f Terricola ( Microtus ) and Arvicola (Rodentia, Arvicolinae). Genetica 138: 1085-1098 (2010
5. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al: Gapped BLAST and PSIBLAST: A n ew generation of protein database search programs. Nucleic Acids Res 25: 3389-3402 (1997
6. Arnason U, Widegren B: Composition and chromosomal localization of cetacean highly repetitive DNA with special referenc e to the blue whale, Balaenoptera musculus . Chromosoma 98: 323-329 (1989
7. Bachmann L, Sperlich D: Gradual evolution of a specific satellite DNA family in Drosophila ambigua , D. tristis , and D. obscura . Mol Biol Evol 10: 647-659 (1993
8. Benson G: Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Res 27: 573-580 (1999
9. Bulazel K, Metcalfe C, Ferreri GC, Yu J, Eldridge MD, O'Neill RJ: Cytogenetic and molecular evaluation of centromere-associated DNA sequences from a marsupial (Macropodidae: Macropus rufogriseus ) X chromosome. Genetics 172: 1129-1137 (2006
10. Bullejos M, Sánchez A, Burgos M, Hera C, Jiménez R, Díaz De La Guardia R: Multiple, polymorphic copies of SRY in both males and females of the vole Microtus cabrerae . Cytogenet Cell Genet 79: 167-171 (1997
11. Burgos M, Jiménez R, Díaz De La Guardia R: Comparative study of G-and C-banded chromosomes of five species of Microtidae. A chromosomal evolution analysis. Genome 30: 540-546 (1988 a
12. Burgos M, Jiménez R, Olmos DM, Díaz De La Guardia R: Heterogeneous heterochromatin and size variation in the sex chromosomes of Microtus cabrerae . Cytogenet Cell Genet 47: 75-79 (1988 b
13. Caron e DM, Longo MS, Ferreri GC, Hall L, Harris M, et al: A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 118: 113-125 (2009
14. Charlesworth B, Sniegowski P, Stephan W: The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215-220 (1994
15. Cheng YM, Li TS, Hsieh LJ, Hsu PC, Li YC, Lin CC: Complex genomic organization of Indian muntjac centromeric DNA. Chromosome Res 17: 1051-1062 (2009).
16. Denome RM O'Callaghan B Luitjens C Harper E Bianco R: Characterization of a satellite DNA from Antilocapra Americana. Gene 145 257-259(1994).
17. Fernández R, Barragán MJ, Bullejos M, Marchal JA, Martínez S, et al: Molecular and cytogenetic characterization of highly repeated DNA sequences in the vole M icrotus cabrerae . Heredity 87: 637-646 (2001
18. Fry K, Salser W: Nucleotide sequences of HS-alpha satellite DNA from kangaroo rat Dipodomys ordii and characterization of similar sequences in other rodents. Cell 12: 1069-1084 (1977
19. Garagna S, Marziliano N, Zuccotti M, Searle JB, Capanna E, Redi CA: Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci USA 98: 171-175 (2001
20. Giagia EB: Karyotypes of '44-chromosomes ' Pitymys species (Rodentia, Mammalia) and their distribution in southern Greece. Säug Mitt 32: 169-173 (1985).
21. Giagia EB, Ondrias JC: Karyological analysis of the vole Pitymys atticus (Rodentia, Mammalia) from Greece. Biol Gallo-Hellen 4: 205-212 (1973
22. Giagia-Athanasopoulou EB, Stamatopoulos C: G eographical distribution and interpopulation variation in the karyotypes of Microtus (Terricola) thomasi (Rodentia, Arvicolidae) in Greece. Caryologia 50: 303-315 (1997
23. Giagia-Athanasopoulou EB, Chondropoulos BP, Fraguedakis-Tsolis SE: Robertsonian chromosomal variation in the subalpine voles Microtus (Terricola) , (Rodentia, Arvicolidae) from Greece. Acta Theriol 40: 139-143 (19 95
24. Grewal SI, Elgin SC: Transcription and RNA interference in the formation of heterochromatin. Nature 447: 399-406 (2007
25. Hatch FT, Bodner AJ, Mazrimas JA, Moore DH: Satelli te DNA and cytogenetic evolution. DNA quantity, satellite DNA and karyotypic variations in kangaroo rats (genus Dipodomys ). Chromosoma 58: 155-168 (1976
26. Hsu TC, Patton JL: Bone marrow preparations for chromosome studies, in Benirschke K (ed): Comparative Mammalian Cytogenetics, pp 454-460 (Springer-Verlag, New York 1969
27. International Human Genome Se quencing Consortium: Initial sequencing and analysis of the human genome. Nature 409: 860-921 (2001
28. Ivanov SV, Modi WS: Molecular characterization of the complex sex-chromosome heterochromatin in the rodent Microtus chrotorrhinus . Cytogenet Cell Genet 75: 49-56 (1996
29. Kalscheuer V, Singh AP, Nanda I, Sperling K, Neitzel H: Evolution of the gonosomal heterochromatin of Microtus agrestis : Rapid amplifi cation of a large, multimeric, repeat unit containing a 3.0-kb (GATA)11-positive, middle repetitive element. Cytogenet Cell Genet 73: 171-178 (1996
30. Kuznetsova I, Podgornaya O, Ferguson-Smith MA: High-resolution organization of mouse centromeric and pericentromeric DNA. Cytogenet Genome Res 112: 248-255 (2006
31. Li YC, Lee C, Sanoudou D, Hsu TH, Li SY, Lin CC: Interstitial colocalization of two ce rvid satellite DNAs involved in the genesis of the Indian muntjac karyotype. Chromosome Res 8: 363-373 (2000
32. Marchal JA, Acosta MJ, Bullejos M, Díaz De La Guardia R, Sánchez A: Sex chromosomes, se x determination, and sex-linked sequences in Microtidae. Cytogenet Genome Res 101: 266-273 (2003
33. Marchal JA, Acosta MJ, Bullejos M, Díaz De La Guardia R, Sánchez A: A repeat DNA sequence from the Y chromosome in species of the genus Microtus . Chromosome Res 12: 757-765 (2004
34. Marchal JA, Acosta MJ, Bullejos M, Puerma E, Díaz De La Guardia R, Sánchez A: Distribution of L1-retroposons on the giant sex chromosomes of Microtus cabrerae (Arvicolidae, Rodentia): Functional and evolutionary implications. Chromosome Res 14: 177-186 (2006
35. Maruyama T, Imai HT: Evolutionary rate of the mammalian karyotype. J Theor Biol 90: 111-121 (1981
36. Mayorov VI, Adkison LR, Vorobyeva NV, Khrapov EA, Kholodhov NG, et al: Organization and chromosomal localization of a B1-like containing repeat of Microtu s subarvalis . Mamm Genome 7: 593-597 (1996).
37. Mazurok N.A. Rubtsova NV Isaenko AA Pavlova ME Slobodyanyuk SY et al. Comparative chromosome and mitochondrial DNA analyses and phylogenetic rela tionships within common voles ( Microtus , Arvicolidae. Chromosome Res 9 107-120(2001).
38. Melters DP, Bradnam KR, Young HA, Telis N, May MR, et al: Comparative analysis of tandem repeats from h undreds of species reveals unique insights into centromere evolution. Genome Biol 14:R10 (2013
39. Mitsainas GP, Rovatsos MT, Rizou EI, Giagia-Athanasopoulou EB: Sex chromosome variability outlines the pathwa y to the chromosomal evolution in Microtus thomasi (Rodentia, Arvicolinae). Biol J Linn Soc 96: 685-695 (2009
40. Modi WS: Phylogenetic analyses of chromosomal banding patterns among the Nearctic Arvicolidae (Mammalia: Rodentia). Syst Zool 36: 109-136 (1987 a
41. Modi WS: C-banding analysis and the evolution of heterochromatin among arvicolid rodents. J Mammal 68: 704-714 (1987 b
42. Modi WS: Nucleotide sequence and genomic organization of a tandem satellite array from the rock vole Microtus chrotorrhinus (Rodentia) Mamm Genome 3: 226-232 (1992
43. Modi WS: Comparative analyses of heterochromatin in Microtus : Sequence heterogeneity and localized expansion and contraction of satellite DNA arrays. Cytogenet Cell Genet 62: 142-148 (1993 a
44. Modi WS: Heterogeneity in the concerted evolution process of a tandem satellite array in meadow mice (Microtus) . J Mol Evol 37: 48-56 (1993 b
45. Modi WS: Rapid, l ocalized amplification of a unique satellite DNA family in the rodent Microtus chrotorrhinus . Chromosoma 102: 484-490 (1993 c
46. Modi WS, Serdyukova NA, Vorobieva NV, Graphodatsky AS: Chromosomal localiz ation of six repeated DNA sequences among species of Microtus (Rodentia). Chromosome Res 11: 705-713 (2003
47. Mouse Genome Sequencing Consortium: Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562 (2002
48. Neumann P, NavrátilováA, Schroeder-Reiter E, Koblí?kováA, SteinbauerováV, et al: Stretching the rules: Monocentric chromosomes with multiple centromere domains. PLoS Genet 8:e1002777 (2012
49. Palomeque T, Lorite P: Satellite DNA in insects: A review. Heredity 100: 564-573 (2008
50. Plohl M, Luchetti A, Me? trovi? N, Mantovani B: Satellite DNAs between selfishness and functionality: Structure, genomics and evolution of tandem repeats in centromeric (hetero) chromatin. Gene 409: 72-82 (2008
51. Riethman H, Ambrosini A, Castaneda C, Finklestein J, Hu XL, et al: Mapping and initial analysis of human subtelomeric sequence assemblies. Genome Res 14: 18-28 (2004
52. Rovatsos MT: Study of the Phylogenetic Relations of the Chromosomal Races of the Underg round Vole Microtus thomasi with Cytogenetic and Molecular Approaches. PhD thesis, University of Patras, Patras (2012
53. Rovatsos MT, Giagia-Athanasopoulou EB: Taxonomical status and phylogenetic relations between the ' thomasi' and 'atticus' chromosomal races of the underground vole Microtus thomasi (Rodentia, Arvicolinae). Mamm Biol 77: 6-12 (2012
54. Rovatsos MT, Mitsainas GP, Stamatopoulos C, Giagia-Athanasopoulou EB: First reports of XXY aneuploidy in natural populations of Thomas' pine vole Microtus thomasi (Rodentia: Arvicolidae) from Greece. Mamm Biol 73: 342-349 (2008
55. Rovatsos MT, Mitsainas GP, Paspali G, Oruci S, Giagia-Athanasopoulou EB: Geographical distribution and chromosomal study of the underground vole Microtus thomasi in Alba nia and Montenegro. Mamm Biol 76: 22-27 (2011a
56. Rovatsos MT, Marchal JA, Romero-Fernández I, Fernández FJ, Giagia-Athanosopoulou EB, Sánchez A: Rapid, independent, and extensive amplification of telomeric repeats in pericentromeric regions in karyotypes of arvicoline rodents. Chromosome Res 19: 869-882 (2011b
57. Rudd MK, Willard HF: Analysis o f the centromeric regions of the human genome assembly. Trends Genet 20: 529-533 (2004).
58. Rudd MK Wray GA Willard HF. The evolutionary dynamics of alpha-satellite. Genome Res. 16. 88-96 (2006).
59. Sánchez A, Bullejos M, Burgos M, Jiménez R, Díaz De La Guardia R: An alternative to blunt-end ligation for cloning DNA fragments with incompatible ends. Trends Genet 12: 44 (1996
60. Shevchenko AT, Mazurok NA, Slobodyanyuk SY, Zakian SM: Comparative analysis of the MSAT-160 repeats in four species of common vole ( Microtus , Arvicolidae). Chromosome Res 10: 117-126 (2002
61. T hompson JD, Higgins DG, Gibson TJ: CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 46 73-4680 (1994
62. Ugarkovi? D, Plohl M: Variation in satellite DNA profiles-causes and effects. EMBO J 21: 5955-5959 (2002
63. Zhang XY, Horz W: Nucleosomes are positioned on mouse satellite DNA in multiple highly specific frames that are correlated with a diverged subrepeat of nine base-pairs. J Mol Evol 176: 105-129 (1984