Intra-genomic GC heterogeneity in sauropsids: Evolutionary insights from cDNA mapping and GC3 profiling in snake

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Matsubara, Kazumi ^a,g   Kuraku, Shigehiro ^b,c   Tarui, Hiroshi ^c,h   Nishimura, Osamu ^c,d   Nishida, Chizuko ^e   Agata, Kiyokazu ^d   Kumazawa, Yoshinori ^a   Matsuda, Yoichi ^f  

^a NAGOYA CITY UNIVERSITY   (Japan)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

^f NAGOYA UNIVERSITY   (Japan)

^g UNIVERSITY OF CANBERRA   (Australia)

^h RIKEN YOKOHAMA INSTITUTE   (Japan)

Author keywords

GC content; Lepidosauria; Macrochromosome; Microchromosome; Snake

Indexed keywords

COMPLEMENTARY DNA; CYTOSINE; GUANINE;

AMNIOTE; ARCHOSAUR; ARTICLE; CHICKEN; CHROMOSOME SIZE; CODON; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOGENETICS; DNA BASE COMPOSITION; EVOLUTION; EXON; EXPRESSED SEQUENCE TAG; FLUORESCENCE IN SITU HYBRIDIZATION; GC RICH SEQUENCE; GENE LOCATION; GENE MAPPING; GENETIC CONSERVATION; GENETIC HETEROGENEITY; GENETIC VARIABILITY; LAST COMMON ANCESTOR; LEPIDOSAUR; MICROCHROMOSOME; MOLECULAR CLONING; NEIGHBOR JOINING METHOD; NONHUMAN; NUCLEIC ACID ANALYSIS; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHYLOGENETIC TREE; SAUROPSID; SEQUENCE ALIGNMENT; SNAKE; SPECIES DIFFERENCE;

ANIMALS; BASE COMPOSITION; CHROMOSOME MAPPING; CHROMOSOMES; CODON; CYTOGENETIC ANALYSIS; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENOME; IN SITU HYBRIDIZATION, FLUORESCENCE; SNAKES; SPECIES SPECIFICITY;

AMNIOTA; AMPHISBAENIA; ANOLIS; ARCHOSAURIA; AVES; CROCODYLIDAE (ALL CROCODILES); ELAPHE QUADRIVIRGATA; LEPIDOSAURIA; RATTUS; REPTILIA; SAUROPSIDA; SERPENTES; SPHENODON PUNCTATUS; SQUAMATA; TESTUDINES;

EID: 84868549817     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-604     Document Type: Article

References (75)

1. Zardoya R, Meyer A. Complete mitochondrial genome suggests diapsid affinities of turtles. Proc Natl Acad Sci USA 1998, 95:14226-14231. 10.1073/pnas.95.24.14226, 24355, 9826682.
2. Hedges SB, Poling LL. A molecular phylogeny of reptiles. Science 1999, 283:998-1001. 10.1126/science.283.5404.998, 9974396.
3. Kumazawa Y, Nishida M. Complete mitochondrial DNA sequences of the green turtle and blue-tailed mole skink: statistical evidence for archosaurian affinity of turtles. Mol Biol Evol 1999, 16:784-792. 10.1093/oxfordjournals.molbev.a026163, 10368956.
4. Cao Y, Sorenson MD, Kumazawa Y, Mindell DP, Hasegawa M. Phylogenetic position of turtles among amniotes: evidence from mitochondrial and nuclear genes. Gene 2000, 259:139-148. 10.1016/S0378-1119(00)00425-X, 11163971.
5. Rest JS, Ast JC, Austin CC, Waddell PJ, Tibbetts EA, Hay JM, Mindell DP. Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol Phylogenet Evol 2003, 29:289-297. 10.1016/S1055-7903(03)00108-8, 13678684.
6. Iwabe N, Hara Y, Kumazawa Y, Shibamoto K, Saito Y, Miyata T, Katoh K. Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. Mol Biol Evol 2005, 22:810-813. 10.1093/molbev/msi075, 15625185.
7. Kumazawa Y. Mitochondrial genomes from major lizard families suggest their phylogenetic relationships and ancient radiations. Gene 2007, 388:19-26. 10.1016/j.gene.2006.09.026, 17118581.
8. Benton MJ, Donoghue PCJ. Paleontological evidence to date the tree of life. Mol Biol Evol 2007, 24:26-53.
9. Shedlock AM, Edwards SV. Amniotes (Amniota). The timetree of life 2009, 375-379. New York: Oxford University Press, Hedges SB, Kumar S.
10. Beçak W, Beçak ML, Nazareth HRS, Ohno S. Close karyological kinship between the reptilian suborder Serpentes and the class Aves. Chromosoma 1964, 15:606-617. 10.1007/BF00319994, 14333153.
11. Bickham JW, Baker RJ. Chromosome homology and evolution of emydid turtles. Chromosoma 1976, 54:201-219. 10.1007/BF00293451, 1248339.
12. Bickham JW, Bull JJ, Legler JM. Karyotypes and evolutionary relationships of trinychoid turtles. Cytologia 1983, 48:177-183.
13. Norris TB, Rickards GK, Daugherty CH. Chromosomes of tuatara, Sphenodon, a chromosome heteromorphism and an archaic reptilian karyotype. Cytogenet Genome Res 2004, 105:93-99. 10.1159/000078014, 15218263.
14. Takagi N, Sasaki M. A phylogenetic study of bird karyotypes. Chromosoma 1974, 46:91-120. 10.1007/BF00332341, 4134896.
15. Belterman RHR, de Boer LEM. A karyological study of 55 species of birds, including karyotypes of 39 species new to cytology. Genetica 1984, 65:39-82.
16. Shetty S, Griffin DK, Graves JAM. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 1999, 7:289-295. 10.1023/A:1009278914829, 10461874.
17. Nishida-Umehara C, Tsuda Y, Ishijima J, Ando J, Fujiwara A, Matsuda Y, Griffin DK. The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosome Res 2007, 15:721-734. 10.1007/s10577-007-1157-7, 17605112.
18. Cohen MM, Gans C. The chromosomes of the order Crocodylia. Cytogenetics 1970, 9:81-105. 10.1159/000130080, 5461083.
19. Kawagoshi T, Nishida C, Ota H, Kumazawa Y, Endo H, Matsuda Y. Molecular structures of centromeric heterochromatin and karyotypic evolution in the Siamese crocodile (Crocodylus siamensis) (Crocodylidae, Crocodylia). Chromosome Res 2008, 16:1119-1132. 10.1007/s10577-008-1263-1, 18941916.
20. International Chicken Genome Sequencing Consortium (ICGSC) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432:695-716. 10.1038/nature03154, 15592404, International Chicken Genome Sequencing Consortium (ICGSC).
21. Kuraku S, Ishijima J, Nishida-Umehara C, Agata K, Kuratani S, Yoichi M. cDNA-based gene mapping and GC3 profiling in the soft-shelled turtle suggest a chromosomal size-dependent GC bias shared by sauropsids. Chromosome Res 2006, 14:187-202. 10.1007/s10577-006-1035-8, 16544192.
22. Costantini M, Filippo MD, Auletta F, Bernardi G. Isochore pattern and gene distribution in the chicken genome. Gene 2007, 400:9-15. 10.1016/j.gene.2007.05.025, 17629634.
23. McQueen HA, Siriaco G, Bird AP. Chicken microchromosomes are hyperacetylated, early replicating, and gene rich. Genome Res 1998, 8:621-630. 310741, 9647637.
24. Smith J, Bruley CK, Paton IR, Dunn I, Jones CT, Windsor D, Morrice DR, Law AS, Masabanda J, Sazanov A, Waddington D, Fries R, Burt DW. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim Genet 2000, 31:96-103. 10.1046/j.1365-2052.2000.00565.x, 10782207.
25. Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I. Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res 2001, 9:569-584. 10.1023/A:1012447318535, 11721954.
26. Axelsson E, Webster MT, Smith NG, Burt DW, Ellegren H. Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res 2005, 15:120-125. 10.1101/gr.3021305, 540272, 15590944.
27. Federico C, Cantarella CD, Scavo C, Saccone S, Bed'Hom B, Bernardi G. Avian genomes: different karyotypes but a similar distribution of the GC-richest chromosome regions at interphase. Chromosome Res 2005, 13:785-793. 10.1007/s10577-005-1012-7, 16331410.
28. Shedlock AM, Botka CW, Zhao S, Shetty J, Zhang T, Liu JS, Deschavanne PJ, Edwards SV. Phylogenomics of nonavian reptiles and the structure of the ancestral amniote genome. Proc Natl Acad Sci USA 2007, 104:2767-2772. 10.1073/pnas.0606204104, 1815256, 17307883.
29. Janes DE, Organ CL, Fujita MK, Shedlock AM, Edwards SV. Genome evolution in Reptilia, the sister groups of mammals. Annu Rev Genomics Hum Genet 2010, 11:239-264. 10.1146/annurev-genom-082509-141646, 20590429.
30. Belle EM, Smith N, Eyre-Walker A. Analysis of the phylogenetic distribution of isochores in vertebrates and a test of the thermal stability hypothesis. J Mol Evol 2002, 55:356-363. 10.1007/s00239-002-2333-1, 12187388.
31. Hamada K, Horiike T, Ota H, Mizuno K, Shinozawa T. Presence of isochore structures in reptile genomes suggested by the relationship between GC content of intron regions and those of coding regions. Genes Genet Syst 2003, 78:195-198. 10.1266/ggs.78.195, 12773820.
32. Chojnowski JL, Franklin J, Katsu Y, Iguchi T, Guillette LJ, Kimball RT, Braun EL. Patterns of vertebrate isochore evolution revealed by comparison of expressed mammalian, avian, and crocodilian genes. J Mol Evol 2007, 65:259-266. 10.1007/s00239-007-9003-2, 17674077.
33. Chojnowski JL, Braun EL. Turtle isochore structure is intermediate between amphibians and other amniotes. Integr Comp Biol 2008, 48:454-462. 10.1093/icb/icn062, 21669806.
34. Elhaik E, Landan G, Graur D. Can GC content at third-codon positions be used as a proxy for isochore composition?. Mol Biol Evol 2009, 26:1829-1833. 10.1093/molbev/msp100, 19443854.
35. Clay OK, Bernardi G. GC3 of genes can be used as a proxy for isochore base composition: A reply to Elhaik et al. Mol Biol Evol 2011, 28:21-23. 10.1093/molbev/msq222, 20817719.
36. Romiguier J, Ranwez V, Douzery EJP, Galtier N. Contrasting GC-content dynamics across 33 mammalian genomes: Relationship with life-history traits and chromosome sizes. Genome Res 2010, 20:1001-1009. 10.1101/gr.104372.109, 2909565, 20530252.
37. Fujita MK, Edwards SV, Ponting CP. The Anolis lizard genome: an amniote genome without isochores. Genome Biol Evol in press.
38. Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K, Isobe T, Ando J, Fujiwara A, Hirao Y, Nishimura O, Ishijima J, Hayashi A, Saito T, Murakami T, Murakami Y, Kuratani S, Agata K. Highly conserved linkage homology between birds and turtles: Bird and turtle chromosomes are precise counterparts of each other. Chromosome Res 2005, 13:601-615. 10.1007/s10577-005-0986-5, 16170625.
39. Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, Ray DA, Boissinot S, Shedlock AM, Botka C, Castoe TA, Colbourne JK, Fujita MK, Moreno RG, Ten Hallers BF, Haussler D, Heger A, Heiman D, Janes DE, Johnson J, de Jong PJ, Koriabine MY, Lara M, Novick PA, Organ CL, Peach SE, Poe S, Pollock DD, de Queiroz K, Sanger T, Searle S, Smith JD, Smith Z, Swofford R, Turner-Maier J, Wade J, Young S, Zadissa A, Edwards SV, Glenn TC, Schneider CJ, Losos JB, Lander ES, Breen M, Ponting CP, Lindblad-Toh K. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 2011, 477:587-591. 10.1038/nature10390, 3184186, 21881562.
40. Beçak W, Beçak ML. Cytotaxonomy and chromosomal evolution in Serpentes. Cytogenetics 1969, 8:247-262. 10.1159/000130037, 5381335.
41. Singh L. Evolution of karyotypes in snakes. Chromosoma 1972, 38:185-236. 10.1007/BF00326193, 5066447.
42. Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, Matsuda Y. Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci USA 2006, 103:18190-18195. 10.1073/pnas.0605274103, 1838728, 17110446.
43. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
44. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
45. Katoh K, Kuma K, Toh H, Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33:511-518. 10.1093/nar/gki198, 548345, 15661851.
46. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704. 10.1080/10635150390235520, 14530136.
47. Matsuda Y, Chapman VM. Application of fluorescence in situ hybridization in genome analysis of the mouse. Electrophoresis 1995, 16:261-272. 10.1002/elps.1150160142, 7774567.
48. Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JG, Korf I, Lapp H, Lehväslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E. The Bioperl toolkit: Perl modules for the life sciences. Genome Res 2002, 12:1611-1618. 10.1101/gr.361602, 187536, 12368254.
49. Castoe TA, de Koning AJ, Hall KT, Yokoyama KD, Gu W, Smith EN, Feschotte C, Uetz P, Ray DA, Dobry J, Bogden R, Mackessy SP, Bronikowski AM, Warren WC, Secor SM, Pollock DD. Sequencing the genome of the Burmese python (Python molurus bivittatus) as a model for studying extreme adaptations in snakes. Genome Biol 2011, 12:406. URL: http://www.ncbi.nlm.nih.gov/Traces/wgs/?val=AEQU, 10.1186/gb-2011-12-7-406, 3218823, 21801464.
50. Wise2 - Intelligent algorithms for DNA searches URL: http://www.ebi.ac.uk/Tools/Wise2/index.html.
51. Hubbard T, Andrews D, Caccamo M, Cameron G, Chen Y, Clamp M, Clarke L, Coates G, Cox T, Cunningham F, Curwen V, Cutts T, Down T, Durbin R, Fernandez-Suarez XM, Gilbert J, Hammond M, Herrero J, Hotz H, Howe K, Iyer V, Jekosch K, Kahari A, Kasprzyk A, Keefe D, Keenan S, Kokocinsci F, London D, Longden I, McVicker G, Melsopp C, Meidl P, Potter S, Proctor G, Rae M, Rios D, Schuster M, Searle S, Severin J, Slater G, Smedley D, Smith J, Spooner W, Stabenau A, Stalker J, Storey R, Trevanion S, Ureta-Vidal A, Vogel J, White S, Woodwark C, Birney E. Ensembl 2005. Nucleic Acids Res 2005, 33:D447-453. URL: http://www.ensembl.org/, 10.1093/nar/gki378, 540092, 15608235.
52. NCBI Entrez Gene URL: http://www.ncbi.nlm.nih.gov/gene/.
53. Al-Shahrour F, Dîaz-Uriarte R, Dopazo J. FatiGO: a web tool for finding significant associations of Gene Ontology terms with groups of genes. Bioinformatics 2004, 20:578-580. URL: http://babelomics.bioinfo.cipf.es/functional.html, 10.1093/bioinformatics/btg455, 14990455.
54. Shibusawa M, Nishibori M, Nishida-Umehara C, Tsudzuki M, Masabanda J, Griffin DK, Matsuda Y. Karyotypic evolution in the Galliformes: an examination of the process of karyotypic evolution by comparison of the molecular cytogenetic findings with the molecular phylogeny. Cytogenet Genome Res 2004, 106:111-119. 10.1159/000078570, 15218250.
55. Holmquist GP. Chromosome bands, their chromatin flavors, and their functional features. Am J Hum Genet 1992, 51:17-37. 1682890, 1609794.
56. Saccone S, De Sario A, Della Valle G, Bernardi G. The highest gene concentrations in the human genome are in telomeric bands of metaphase chromosomes. Proc Natl Acad Sci USA 1992, 89:4913-4917. 10.1073/pnas.89.11.4913, 49198, 1594593.
57. Saccone S, De Sario A, Wiegant J, Raap AK, Della Valle G, Bernardi G. Correlations between isochores and chromosomal bands in the human genome. Proc Natl Acad Sci USA 1993, 90:11929-11933. 10.1073/pnas.90.24.11929, 48098, 8265650.
58. Saccone S, Cacciò S, Kusuda J, Andreozzi L, Bernardi G. Identification of the gene-richest bands in human chromosomes. Gene 1996, 174:85-94. 10.1016/0378-1119(96)00392-7, 8863733.
59. Nabholz B, Künstner A, Wang R, Jarvis ED, Ellegren H. Dynamic evolution of base composition: causes and consequences in avian phylogenomics. Mol Biol Evol 2011, 28:2197-2210. 10.1093/molbev/msr047, 3144382, 21393604.
60. Bucciarelli G, Di Filippo M, Costagliola D, Alvarez-Valin F, Bernardi G, Bernardi G. Environmental genomics: a tale of two fishes. Mol Biol Evol 2009, 26:1235-1243. 10.1093/molbev/msp041, 19270014.
61. Kasai F, O'Brien PC, Ferguson-Smith MA. Reassessment of genome size in turtle and crocodile based on chromosome measurement by flow karyotyping: close similarity to chicken. Biol Lett 2012, 8:631-635. 10.1098/rsbl.2012.0141, 22491763.
62. Benirschke K, Hsu TC. Chromosome atlas: fish, amphibians, reptiles and birds volume 1 1971, New York: Springer.
63. Burt DW. Origin and evolution of avian microchromosomes. Cytogenet Genome Res 2002, 96:97-112. 10.1159/000063018, 12438785.
64. Nakatani Y, Takeda H, Kohara Y, Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res 2007, 17:1254-1265. 10.1101/gr.6316407, 1950894, 17652425.
65. Duret L, Eyre-Walker A, Galtier N. A new perspective on isochore evolution. Gene 2006, 385:71-74.
66. Duret L, Galtier N. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 2009, 10:285-311. 10.1146/annurev-genom-082908-150001, 19630562.
67. Meunier J, Duret L. Recombination drives the evolution of GC-content in the human genome. Mol Biol Evol 2004, 21:984-990. 10.1093/molbev/msh070, 14963104.
68. Costantini M, Cammarano R, Bernardi G. The evolution of isochore patterns in vertebrate genomes. BMC Genomics 2009, 10:146. 10.1186/1471-2164-10-146, 2678159, 19344507.
69. Costantini M, Clay O, Auletta F, Bernardi1 G. An isochore map of human chromosomes. Genome Res 2006, 16:536-541. 10.1101/gr.4910606, 1457033, 16597586.
70. Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, Hosoya S, Suetake H, Naruse K, Brenner S, Suzuki Y, Venkatesh B. Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals. Genome Biol Evol 2011, 3:424-442. 10.1093/gbe/evr041, 21551351.
71. Backström N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, Bolund E, Webster MT, Ost T, Schneider M, Kempenaers B, Ellegren H. The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 2010, 20:485-495. 10.1101/gr.101410.109, 2847751, 20357052.
72. Hildebrand F, Meyer A, Eyre-Walker A. Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 2010, 6:e1001107. 10.1371/journal.pgen.1001107, 2936529, 20838593.
73. Bajic VB, Tan SL, Christoffels A, Schönbach C, Lipovich L, Yang L, Hofmann O, Kruger A, Hide W, Kai C, Kawai J, Hume DA, Carninci P, Hayashizaki Y. Mice and men: their promoter properties. PLoS Genet 2006, 2:e54. 10.1371/journal.pgen.0020054, 1449896, 16683032.
74. D'Onofrio G, Ghosh TC, Saccone S. Different functional classes of genes are characterized by different compositional properties. FEBS Lett 2007, 581:5819-5824. 10.1016/j.febslet.2007.11.052, 18037382.
75. Ren L, Gao G, Zhao D, Ding M, Luo J, Deng H. Developmental stage related patterns of codon usage and genomic GC content: searching for evolutionary fingerprints with models of stem cell differentiation. Genome Biol 2007, 8:R35. 10.1186/gb-2007-8-3-r35, 1868930, 17349061.