A High-Resolution Comparative Chromosome Map of Cricetus cricetus and Peromyscus eremicus Reveals the Involvement of Constitutive Heterochromatin in Breakpoint Regions

Cytogenetic and Genome Research

Volumn 145, Issue 1, 2015, Pages 59-67

  Vieira Da Silva, Ana ^a   Louzada, Sandra ^a   Adega, Filomena ^a   Chaves, Raquel ^a  

^a UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

Author keywords

Ancestral karyotype; Chromosome painting; Comparative map; Evolutionary breakpoints; Heterochromatin; Karyotype evolution

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CHROMOSOME MAP; CHROMOSOME PAINTING; CHROMOSOME REARRANGEMENT; CONSTITUTIVE HETEROCHROMATIN; EUROPEAN HAMSTER; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENOME; KARYOTYPE; MALE; MOUSE; NONHUMAN; PEROMYSCUS; PEROMYSCUS EREMICUS; PRIORITY JOURNAL; RAT; ANIMAL; CELL CULTURE; CHROMOSOME; CHROMOSOME BREAKAGE; COMPARATIVE STUDY; GENE REARRANGEMENT; GENETICS; HAMSTER; HETEROCHROMATIN; MOLECULAR EVOLUTION;

ANIMALIA; CRICETIDAE; CRICETUS CRICETUS; MAMMALIA; MUROIDEA; MUS MUSCULUS; PEROMYSCUS EREMICUS; RATTUS; RATTUS NORVEGICUS; RODENTIA;

HETEROCHROMATIN;

ANIMALS; CELLS, CULTURED; CHROMOSOME BREAKPOINTS; CHROMOSOME MAPPING; CHROMOSOME PAINTING; CHROMOSOMES, MAMMALIAN; CRICETINAE; EVOLUTION, MOLECULAR; GENE REARRANGEMENT; GENOME; HETEROCHROMATIN; IN SITU HYBRIDIZATION, FLUORESCENCE; KARYOTYPE; MICE; PEROMYSCUS; RATS;

EID: 84931956587     PISSN: 14248581     EISSN: 1424859X     Source Type: Journal    
DOI: 10.1159/000381840     Document Type: Article

References (66)

1. Adega F, Guedes-Pinto H, Chaves R: Satellite DNA in the karyotype evolution of domestic animals-clinical considerations. Cytogenet Genome Res 126: 12-20 (2009).
2. Adkins RM, Walton AH, Honeycutt RL: Higherlevel systematics of rodents and divergence time estimates based on two congruent nuclear genes. Mol Phylogenet Evol 26: 409-420 (2003).
3. Badenhorst D, Dobigny G, Adega F, Chaves R, O'Brien PC, et al: Chromosomal evolution in Rattini (Muridae, Rodentia). Chromosome Res 19: 709-727 (2011).
4. Brown JD, Mitchell SE, O'Neill RJ: Making a long story short: noncoding RNAs and chromosome change. Heredity 108: 42-49 (2012).
5. Catzeflis FM, Aguilar JP, Jaeger JJ: Muroid rodents: phylogeny and evolution. Trends Ecol Evol 7: 122-126 (1992).
6. Catzeflis FM, Dickerman AW, Michaux J, Kirsch JA: DNA hybridization and rodent phylogeny, in Szalay FS, Novacek MJ, McKenna MC (eds): Mammal Phylogeny, pp 159-172 (Springer-Verlag, New York 1993).
7. Cazaux B, Catalan J, Veyrunes F, Douzery E, Britton-Davidian J: Are ribosomal DNA clusters rearrangement hotspots? A case study in the genus Mus (Rodentia, Muridae). BMC Evol Biol 11: 124 (2011).
8. Chaline J, Mein P, Petter F: Les grandes lignes d'une classification évolutive des Muroidea. Mammalia 41: 245-252 (1977).
9. Chaves R, Louzada S, Meles S, Adega F: Praomys tullbergi genome (chromosome) architecture decoded by the related genomes Mus and Rattus . Chromosome Res 20: 673-683 (2012).
10. Darai E, Kost-Alimova M, Kiss H, Kansoul H, Klein G, Imreh S: Evolutionarily plastic regions at human 3p21.3 coincide with tumor breakpoints identified by the 'elimination test'. Genomics 86: 1-12 (2005).
11. Deaven LL, Vidal-Rioja L, Jett JH, Hsu TC: Chromosomes of Peromyscus (Rodentia, Cricetidae). VI. The genomic size. Cytogenet Cell Genet 19: 241-249 (1977).
12. Dubois JY, Rakotondravony D, Hänni C, Sourrouille P, Catzeflis FM: Molecular evolutionary relationships of three genera of Nesomyinae, endemic rodent taxa from Madagascar. J Mamm Evol 3: 239-260 (1996).
13. Dubois JY, Catzeflis FM, Beintema JJ: The phylogenetic position of 'Acomyinae' (Rodentia, Mammalia) as sister group of a Murinae + Gerbillinae clade: evidence from the nuclear ribonuclease gene. Mol Phylogenet Evol 13: 181-192 (1999).
14. Elder FF: Tandem fusion, centric fusion, and chromosomal evolution in the cotton rat, genus Sigmodon . Cytogenet Cell Genet 26: 199-210 (1980).
15. Engelbrecht A, Dobigny G, Robinson TJ: Further insights into the ancestral murine karyotype: The contribution of the Otomys-Mus comparison using chromosome painting. Cytogenet Genome Res 112: 126-130 (2006).
16. Eymery A, Callanan M, Vourc'h C: The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 53: 259-268 (2009).
17. Fabre PH, Hautier L, Dimitrov D, Douzery EJ: A glimpse on the pattern of rodent diversification: A phylogenetic approach. BMC Evol Biol 12: 88 (2012).
18. Froenicke L, Lyons AL: Hotspots of mammalian chromosome evolution, in: Encyclopedia of Life Sciences (ELS) (John Wiley & Sons, Ltd, Chichester 2008) [http://www.els.net/].
19. Gamperl R, Vistorin G, Rosenkranz W: A comparative analysis of the karyotypes of Cricetus cricetus and Cricetulus griseus . Chromosoma 55: 259-265 (1976).
20. Glasper ER, DeVries AC: Social structure influences effects of pair-housing on wound healing. Brain Behav Immun 19: 61-68 (2005).
21. Greenbaum IF, Baker RJ: Determination of the primitive karyotype for Peromyscus . J Mammal 59: 820-834 (1978).
22. Grewal SI, Jia S: Heterochromatin revisited. Nat Rev Genet 8:35-46 (2007).
23. Hanon EA, Routledge K, Dardente H, Masson-Pévet M, Morgan PJ, Hazlerigg DG: Effect of photoperiod on the thyroid-stimulating hormone neuroendocrine system in the European hamster (Cricetus cricetus). J Neuroendocrinol 22: 51-55 (2010).
24. Hugueney M, Mein P: A comment on the earliest Spalacinae (Rodentia, Muroidea). J Mamm Evol 1: 215-223 (1993).
25. Jacobs LL, Flynn LJ, Downs WR: Neogene rodents of Southern Asia, in Black CC, Dawson MR (eds): Papers on Fossil Rodents in Honor of Albert Elmer Wood. Science, Series No. 33, pp 157-177 (Nat Hist Mus Los Angeles County, Los Angeles 1989).
26. Jansa SA, Goodman SM, Tucker PK: Molecular phylogeny and biogeography of the native rodents of Madagascar (Muridae: Nesomyinae): A test of the single-origin hypothesis. Cladistics 15: 253-270 (1999).
27. John B: The biology of heterochromatin, in Verma RS (ed): Heterochromatin: Molecular and Structural Aspects, pp 1-128 (Cambridge University Press, Cambridge 1988).
28. Kent WJ, Baertsch R, Hinrichs A, Miller W, Haussler D: Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci USA 100: 11484-11489 (2003).
29. Longo MS, Carone DM, NISC Comparative Sequencing Program, Green ED, O'Neill MJ, O'Neill RJ: Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty. BMC Genomics 10: 334 (2009).
30. Louzada S, Paço A, Kubickova S, Adega F, Guedes-Pinto H, et al: Different evolutionary trails in the related genomes Cricetus cricetus and Peromyscus eremicus (Rodentia, Cricetidae) uncovered by orthologous satellite DNA repositioning. Micron 39: 1149-1155 (2008).
31. Matthey R: Chromosomes de Muridae (Microtinae et Cricetinae). Chromosoma 5: 113-138 (1952).
32. Michaux J, Reyes A, Catzeflis F: Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Mol Biol Evol 18: 2017-2031 (2001).
33. Miller GS, Gidley JW: Synopsis of supergeneric groups of rodents. J Wash Acad Sci 8: 431-448 (1911).
34. Mlynarski EE, Obergfell CJ, Rens W, O'Brien PC, Ramsdell CM, et al: Peromyscus maniculatus-Mus musculus chromosome homology map derived from reciprocal cross species chromosome painting. Cytogenet Genome Res 121:288-292 (2008).
35. Murphy WJ, Stanyon R, O'Brien SJ: Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2: 1-8 (2001).
36. Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G, et al: Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309: 613-617 (2005).
37. Musser G, Carleton MD: Superfamily Muroidea, in Wilson DE, Reeder DM (eds): Mammal Species of the World: A Taxonomic and Geographic Reference, ed 3, pp 894-1531 (Johns Hopkins University Press, Baltimore 2005).
38. Nadeau JH, Taylor BA: Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci USA 81: 814-818 (1984).
39. Nilsson S, Helou K, Walentinsson A, Szpirer C, Nerman O, Stahl F: Rat-mouse and rat-human comparative maps based on gene homology and high-resolution zoo-FISH. Genomics 74: 287-298 (2001).
40. Paço A, Adega F, Guedes-Pinto H, Chaves R: Hidden heterochromatin: characterization in the Rodentia species Cricetus cricetus , Peromyscus eremicus (Cricetidae) and Praomys tullbergi (Muridae). Genet Mol Biol 32: 58-68 (2009).
41. Pathak S, Hsu TC, Arrighi FE: Chromosomes of Peromyscus (Rodentia, Cricetidae). IV. The role of heterochromatin in karyotypic evolution. Cytogenet Cell Genet 12: 315-326 (1973).
42. Peacock WJ, Dennis ES, Gerlach WL: DNA sequence changes and speciation. Prog Clin Biol Res 96: 123-142 (1982).
43. Peng Q, Pevzner PA, Tesler G: The fragile breakage versus random breakage models of chromosome evolution. PLoS Comput Biol 2:e14 (2006).
44. Petrović V, Plohl M: Sequence divergence and conservation in organizationally distinct subfamilies of Donax trunculus satellite DNA. Gene 362: 37-43 (2005).
45. Rabbitts P, Impey H, Heppell-Parton A, Langford C, Tease C, et al: Chromosome specific paints from a high resolution flow karyotype of the mouse. Nat Genet 9: 369-375 (1995).
46. Ramsdell CM, Lewandowski AA, Glenn JL, Vrana PB, O'Neill RJ, Dewey MJ: Comparative genome mapping of the deer mouse (Peromyscus maniculatus) reveals greater similarity to rat (Rattus norvegicus) than to the lab mouse (Mus musculus) . BMC Evol Biol 8: 65 (2008).
47. Robinson M, Catzeflis F, Briolay J, Mouchiroud D: Molecular phylogeny of rodents, with special emphasis on murids: evidence from nuclear gene LCAT . Mol Phylogenet Evol 8: 423-434 (1997).
48. Robinson TJ, Ruiz-Herrera A, Froenicke L: Dissecting the mammalian genome-new insights into chromosomal evolution. Trends Genet 22: 297-301 (2006).
49. Romanenko SA, Perelman PL, Serdukova NA, Trifonov VA, Biltueva LS, et al: Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17: 1183-1192 (2006).
50. Romanenko SA, Volobouev VT, Perelman PL, Lebedev VS, Serdukova NA, et al: Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison. Chromosome Res 15: 283-297 (2007).
51. Romanenko SA, Perelman PL, Trifonov VA, Graphodatsky AS: Chromosomal evolution in Rodentia. Heredity (Edinb) 108: 4-16 (2012).
52. Rousselet J, Monti L, Auger-Rozenberg MA, Parker JS, Lemeunier F: Chromosome fission associated with growth of ribosomal DNA in Neodiprion abietis (Hymenoptera: Diprionidae). Proc Biol Sci 267: 1819-1823 (2000).
53. Ruiz-Herrera A, Castresana J, Robinson TJ: Is mammalian evolution driven by regions of genome fragility? Genome Biol 7:R115 (2006).
54. Sankoff D, Deneault M, Turbis P, Allen C: Chromosomal distributions of breakpoints in cancer, infertility, and evolution. Theor Popul Biol 61: 497-501 (2002).
55. Stanyon R, Yang F, Cavagna P, O'Brien PC, Bagga M, et al: Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats. Cytogenet Cell Genet 84: 150-155 (1999).
56. Stanyon R, Yang F, Morescalchi AM, Galleni L: Chromosome painting in the long-tailed field mouse provides insights into the ancestral murid karyotype. Cytogenet Genome Res 105: 406-411 (2004).
57. Steppan SJ, Adkins RM, Anderson J: Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53: 533-553 (2004).
58. Swofford DL: PAUP ∗ : Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4. (Sinauer Associates, Sunderland 2003).
59. The Committee for Standardization of Chromosomes of Peromyscus : Standardized karyotype of deer mice, Peromyscus (Rodentia). Cytogenet Cell Genet 19: 38-43 (1977).
60. van Wolfswinkel JC, Ketting RF: The role of small non-coding RNAs in genome stability and chromatin organization. J Cell Sci 123: 1825-1839 (2010).
61. Veyrunes F, Catalan J, Sicard B, Robinson TJ, Duplantier JM, et al: Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Muridae; Mus ). Chromosome Res 12: 369-382 (2004).
62. Veyrunes F, Dobigny G, Fengtang Y, O'Brien PC, Catalan J, et al: Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse. Proc Biol Sci 273: 2925-2934 (2006).
63. Wienberg J, Stanyon R, Nash WG, O'Brien PC, Yang F, et al: Conservation of humans vs. feline genome organization revealed by reciprocal chromosome painting. Cytogenet Cell Genet 77: 211-217 (1997).
64. Yang F, O'Brien PC, Wienberg J, Ferguson-Smith MA: A reappraisal of the tandem fusion theory of karyotype evolution in the Indian muntjac using chromosome painting. Chromosome Res 5: 109-117 (1997).
65. Yang F, O'Brien PC, Ferguson-Smith MA: Comparative chromosome map of the laboratory mouse and Chinese hamster defined by reciprocal chromosome painting. Chromosome Res 8: 219-227 (2000).
66. Yunis JJ, Yasmineh WG: Heterochromatin, satellite DNA, and cell function. Structural DNA of eucaryotes may support and protect genes and aid in speciation. Science 174: 1200-1209 (1971).