Origin and evolution of B chromosomes in the cichlid fish astatotilapia latifasciata based on integrated genomic analyses

Molecular Biology and Evolution

Volumn 31, Issue 8, 2014, Pages 2061-2072

  Valente, Guilherme T ^a   Conte, Matthew A ^b   Fantinatti, Bruno E A ^a   Cabral De Mello, Diogo C ^a   Carvalho, Robson F ^a   Vicari, Marcelo R ^c   Kocher, Thomas D ^b   Martins, Cesar ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b Bldg 142   (United States)

^c STATE UNIVERSITY OF PONTA GROSSA   (Brazil)

Author keywords

chromosome evolution; genome evolution; next generation sequencing; supernumerary chromosome

Indexed keywords

ARTICLE; ASTATOTILAPIA LATIFASCIATA; AUTOSOME; CELL CYCLE PROGRESSION; CENTROMERE; CICHLID; CONTROLLED STUDY; DNA SEQUENCE; EUKARYOTE; GENE INSERTION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENOMICS; IN SITU HYBRIDIZATION; KARYOTYPE; KARYOTYPING; MICROTUBULE ORGANIZING CENTER; MOLECULAR EVOLUTION; NONHUMAN; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; SUPERNUMERARY CHROMOSOME; TRANSPOSON; ANIMAL; CHEMICAL STRUCTURE; CHROMOSOME; CLASSIFICATION; GENE DUPLICATION; GENETICS; HIGH THROUGHPUT SEQUENCING; PROCEDURES;

FISH PROTEIN;

ANIMALS; CHROMOSOMES; CICHLIDS; EVOLUTION, MOLECULAR; FISH PROTEINS; GENE DUPLICATION; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; KARYOTYPE; MODELS, MOLECULAR; SEQUENCE ANALYSIS, DNA;

EID: 84904994769     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msu148     Document Type: Article

References (67)

1. Alfenito MR, Birchler JA. 1993. Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589-597
2. Banaei-Moghaddam AM, Meier K, Karimi-Ashtiyani R, Houben A. 2013. Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell 25:2536-2544
3. Banaei-Moghaddam AM, Schubert V, Kumke K, Weib O, Klemme S, Nagaki K, Macas J, González-Sánchez M, Heredia V, Gómez-Revilla D, et al. 2012. Nondisjunction in favor of a chromosome: The mechanism of rye B chromosome drive during pollen mitosis. Plant Cell 24:4124-4134
4. Betrán E, Thornton K, LongM. 2002. Retroposed new genes out of the X in Drosophila. Genome Res. 12:1854-1859
5. Bischoff JR, Anderson L, Zhu Y, Mossie K, Ng L, Souza B, Schryver B, Flanagan P, Clairvoyant F, Ginthe C, et al. 1998. A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17:3052-3065
6. Brosius J. 1999. RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238: 115-134
7. Bueno D, Palacios-Gimenez OM, Cabral-De-Mello DC. 2013. Chromosomal mapping of repetitive DNAs in the grasshopper Abracris flavolineata reveal possible ancestry of the B chromosome and H3 histone spreading. PLoS One 8:e66532
8. Burt A, Trivers R. 2006. Genes in conflict: The biology of selfish genetic elements. Cambridge: Belknap Press of Harvard University
9. Cabral-De-Mello DC, Valente GT, Nakajima RT, Martins C. 2012. Genomic organization and comparative chromosome mapping of the U1 snRNA gene in cichlid fish, with an emphasis in Oreochromis niloticus. Chromosome Res. 20:279-292
10. Camacho JP. 2005. B chromosomes. In: Gregory TR, editor. The evolution of the genome. San Diego (CA): Elsevier. p. 223-286
11. Camacho JP, Sharbel TF, Beukeboom LW. 2000. B-chromosome evolution. Philos Trans R Soc Lond B. 355:163-178
12. Cnaani A, Kocher TD. 2008. Sex-linked markers and microsatellite locus duplication in the cichlid species Oreochromis tanganicae. Biol Lett. 4: 700-703
13. Cnaani A, Lee BY, Zilberman N, Ozouf-Costaz C, Hulata G, Ron M, D'Hont A, Baroiller JF, D'Cotta H, Penman DJ, et al. 2008. Genetics of sex determination in tilapiine species. Sex Dev. 1:43-54
14. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. 2005. "Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. ". Bioinformatics 21: 3674-3676
15. Darling AC, Mau B, Blattner FR, Perna NT. 2004. Mauve: Multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14:1394-403
16. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214
17. Edgar RC. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797
18. Fantinatti BEA, Mazzuchelli J, Valente GT, Cabral-De-Mello DC, Martins C. 2011. Genomic content and new insights on the origin of the B chromosome of the cichlid fish Astatotilapia latifasciata. Genetica 139:1273-1282
19. Ferenz NP, Gable A, Wadsworth P. 2010. Mitotic functions of kinesin-5. Semin Cell Dev Biol. 21:255-259
20. Fu J, Bian M, Jiang Q, Zhang C. 2007. Roles of aurora kinases in mitosis and tumorigenesis. Mol Cancer Res. 5:1-10
21. Goldman N, Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 11: 725-736
22. Gómez-López S, Lerner RG, Petritsch C. 2014. Asymmetric cell division of stem and progenitor cells during homeostasis and cancer. Cell Mol Life Sci. 71:575-597
23. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 27:221-224
24. Guerra MS. 1986. Reviewing the chromosome nomenclature of Leval et al. Braz J Genet. 9:741-743
25. Guindon S, Gascuel O. 2003. PhyML: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704
26. Hauf S, Waizenegger IC, Peters JM. 2001. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293: 1320-1323
27. Houben A, Banaei-Moghaddam AM, Klemme S. 2013. Biology and evolution of B chromosomes. In: Leitch IJ, editor. Plant genome diversity, Vol. 2. Berlin (Germany): Springer. p. 149-165
28. Houben A, Verlin D, Leach CR, Timmis JN. 2001. The genomic complexity of micro B chromosomes of Brachycome dichromosomatica. Chromosoma 110:451-459
29. Jones RN. 1991. B-chromosome drive. Am Nat. 137:430-442
30. Jones RN, Gonzalez-Sanchez M, Gonzalez-Garcia M, Vega JM, Puertas MJ. 2008. Chromosomes with a life of their own. Cytogenet Genome Res. 120:265-280
31. Jones RN, Houben A 2003. B chromosomes in plants: Escapes from the A chromosome genome? Trends Plant Sci. 8:417-423
32. Jones RN, Puertas MJ. 1993. The B chromosomes of rye (Secale cereale L. ). In: Dhir KK, Sareen TS, editors. Frontiers in plant science research. Delhi (India): Bhagwati Enterprises. p. 81-112
33. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D. 2009. Circos: An information aesthetic for comparative genomics. Genome Res. 19:1639-1645
34. Kuroiwa A, Terai Y, Kobayashi N, YoshiDa K, Suzuki M, Nakanishi A, MatsuDa Y, Watanabe M, OkaDa N. 2014. Construction of chromosome markers from the Lake Victoria cichlid Paralabidochromis chilotes and their application to comparative mapping. Cytogenet Genome Res. 142:112-120
35. Langmead B, Salzberg S. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9:357-359
36. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079
37. Macarulla T, Ramos FJ, Tabernero J. 2008. Aurora kinase family: A new target for anticancer drug. Recent Pat Anticancer Drug Discov. 3: 114-122
38. Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Šimková H, et al. 2012. Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Natl Acad Sci U S A. 109:13343-13346
39. Maruska KP, Fernald RD. 2010. Reproductive status regulates expression of sex steroid and GnRH receptors in the olfactory bulb. Behav Brain Res. 213:208-217
40. Mestriner CA, Galetti PM Jr, Valentini SR, Ruiz IR, Abel LD, Moreira-Filho O, Camacho JP. 2000. Structural and functional evidence that a B chromosome in the characid fish Astyanax scabripinnis is an isochromosome. Heredity 85:1-9
41. Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 2010 Nov 14; New Orleans, LA. p 1-8
42. Nagaraju G, Hartlerode A, Kwok A, Chandramouly G, Scully R. 2009. XRCC2 and XRCC3 regulate the balance between short-And longtract gene conversions between sister chromatids. Mol Cell Biol. 29: 4283-4294
43. Nguyen P, Sýkorová M, Šíchová J, Kůta V, Dalíková M, Č apková Frydrychová R, Neven LG, Sahara K, Marec F. 2013. Neo-sex chromosomes and adaptive potential in tortricid pests. Proc Natl Acad Sci U S A. 110:6931-6936
44. O'Quin CT, Drilea AC, Conte MA, Kocher TD. 2013. Mapping of pigmentation QTL on an anchored genome assembly of the cichlid fish, Metriaclima zebra. BMC Genomics 14:287
45. Palestis BG, Trivers R, Burt A, Jones RN. 2004. The distribution of B chromosomes across species. Cytogenet Genome Res. 106: 151-158
46. Peng SF, Lin YP, Lin BY. 2005. Characterization of AFLP sequences from regions of maize B chromosome defined by 12 B-10L translocations. Genetics 169:375-388
47. Pinkel D, Straume T, Gray JW. 1986. Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A. 83:2934-2938
48. Poletto AB, Ferreira IA, Cabral-De-Mello DC, Nakajima RT, Mazzuchelli J, Ribeiro HB, Venere PC, Nirchio M, Kocher TD, Martins C. 2010. Chromosome differentiation patterns during cichlid fish evolution. BMC Genet. 11:50
49. Poletto AB, Ferreira IA, Martins C. 2010. The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genet. 11:1
50. PosaDa D. 2008. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 25:1253-1256
51. Radrizzani M, Vila-Ortiz G, Cafferata EG, Di Tella MC, Gonzalez-Guerrico A, Perandones C, Pivetta OH, Carminatti H, Idoyaga VP, Santa-Coloma TA. 2001. Differential expression of CPD1 during postnatal development in the mouse cerebellum. Brain Res. 907: 162-174
52. Rambaut A 2009. Molecular evolution, phylogenetics and epidemiology: Tracer [Online]. [updated 2009 Nov 30]. Available from: Http://tree. bio. ed. ac. uk/software/tracer/.
53. Rapley J, Nicolàs M, Groen A, Regué L, Bertran MT, Caelles C, Avruch J, Roig J. 2008. The NIMA-family kinase Nek6 phosphorylates the kinesin Eg5 at a novel site necessary for mitotic spindle formation. J Cell Sci. 121:3912-3921
54. Schmidt JC, Arthanari H, Boeszoermenyi A, Dashkevich NM, Wilson-Kubalek EM, Monnier N, Markus M, Oberer M, Milligan RA, Bathe M, et al. 2012. The kinetochore-bound Ska1 complex tracks depolymerizing microtubules and binds to curved protofilaments. Dev Cell. 23:968-980
55. Schweizer D. 1976. Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58:307-324
56. Ser JR, Roberts RB, Kocher TD. 2009. Multiple interacting loci control sex determination in Lake Malawi cichlid fish. Evolution 64: 486-501
57. Shirak A, Grabherr M, Di Palma F, Lindblad-Toh K, Hulata G, Ron M, Kocher TD, Seroussi E. 2010. Identification of repetitive elements in the genome of Oreochromis niloticus: Tilapia repeat masker. Mar Biotechnol. 12:121-125
58. Sumner A. 1972. A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res. 75:304-306
59. Trifonov VA, Dementyeva PV, Larkin DM, O'Brien PC, Perelman PL, Yang F, Ferguson-Smith MA, Graphodatsky AS. 2013. Transcription of a protein-coding gene on B chromosomes of the Siberian roe deer (Capreolus pygargus). BMC Biol. 6:90
60. Walne AJ, Vulliamy T, Kirwan M, Plagnol V, Dokal I. 2013. Constitutional mutations in RTEL1 cause severe dyskeratosis congenita. Am J Hum Genet. 92:448-453
61. Weaver BA, Bonday ZQ, Putkey FR, Kops GJ, Silk AD, Cleveland DW. 2003. Centromere-Associated protein-E is essential for the mammalian mitotic checkpoint to prevent aneuploidy due to single chromosome loss. J Cell Biol. 162:551-563
62. Welburn JPI, Grishchuk EL, Backer CB, Wilson-Kubalek EM, Yates JR 3rd, Cheeseman IM. 2009. The human kinetochore Ska1 complex facilitates microtubule depolymerization-coupled motility. Dev Cell. 16: 374-385
63. Werren JH. 2011. Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc Natl Acad Sci U S A. 108:10863-10870
64. White MJD. 1973. Animal cytology and evolution. London: Cambridge University Press
65. Wilson B. 1907. The supernumerary chromosomes of Hemiptera. Science 26:870-71
66. Winkel K, Alsheimer M, Ollinger R, Benavente R. 2009. Protein SYCP2 provides a link between transverse filaments and lateral elements of mammalian synaptonemal complexes. Chromosoma 118:259-267
67. YoshiDa K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A, Hirai H, Hirai Y, MatsuDa Y, et al. 2011. B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet. 7:e1002203.