Chromosoma

, Volume 126, Issue 2, pp 313–323 | Cite as

The repetitive DNA element BncDNA, enriched in the B chromosome of the cichlid fish Astatotilapia latifasciata, transcribes a potentially noncoding RNA

  • Érica Ramos
  • Adauto L. Cardoso
  • Judith Brown
  • Diego F. Marques
  • Bruno E. A. Fantinatti
  • Diogo C. Cabral-de-Mello
  • Rogério A. Oliveira
  • Rachel J. O’Neill
  • Cesar Martins
Research Article
First Online:
Received:
Revised:
Accepted:

Abstract

Supernumerary chromosomes have been studied in many species of eukaryotes, including the cichlid fish, Astatotilapia latifasciata. However, there are many unanswered questions about the maintenance, inheritance, and functional aspects of supernumerary chromosomes. The cichlid family has been highlighted as a model for evolutionary studies, including those that focus on mechanisms of chromosome evolution. Individuals of A. latifasciata are known to carry up to two B heterochromatic isochromosomes that are enriched in repetitive DNA and contain few intact gene sequences. We isolated and characterized a transcriptionally active repeated DNA, called B chromosome noncoding DNA (BncDNA), highly represented across all B chromosomes of A. latifasciata. BncDNA transcripts are differentially processed among six different tissues, including the production of smaller transcripts, indicating transcriptional variation may be linked to B chromosome presence and sexual phenotype. The transcript lengths and lack of similarity with known protein/gene sequences indicate BncRNA might represent a novel long noncoding RNA family (lncRNA). The potential for interaction between BncRNA and known miRNAs were computationally predicted, resulting in the identification of possible binding of this sequence in upregulated miRNAs related to the presence of B chromosomes. In conclusion, Bnc is a transcriptionally active repetitive DNA enriched in B chromosomes with potential action over B chromosome maintenance in somatic cells and meiotic drive in gametic cells.

Keywords

Cytogenomics Repetitive element Evolution Supernumerary chromosome 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by grants from São Paulo Research Foundation (13/04533-3, 10/17212-2, 12/20959-8, 13/01688-6), National Council for Scientific and Technological Development (474684/2013-0, 301728/2011-9), and São Paulo State University (0045/021/13-PROPe/CDC).

Compliance with ethical standards

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

412_2016_601_MOESM1_ESM.pdf (5.3 mb)
ESM 1 (PDF 5465 kb)

References

  1. Ahnert SE, Fink TMA, Zinovyev A (2008) How much non-coding DNA do eukaryotes require? J Theor Biol 252:587–592PubMedCrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedCrossRefGoogle Scholar
  3. Banaei-Moghaddam AM, Meier K, Karimi-Ashtiyani R, Houben A (2013) Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell 25:2536–44PubMedPubMedCentralCrossRefGoogle Scholar
  4. Basu S, Müller F, Sanges R (2013) Examples of sequence conservation analyses capture a subset of mouse long non-coding RNAs sharing homology with fish conserved genomic elements. BMC Bioinformatics 14:S14PubMedPubMedCentralGoogle Scholar
  5. Bougourd SM, Jones RN (1997) B chromosomes: a physiological enigma. New Phytol 137:43–54CrossRefGoogle Scholar
  6. Brockdorff N, Ashworth A, Kay GF, McCabe VM, Norris DP, Cooper PJ, Swift S, Rastan S (1992) The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 71:515–526PubMedCrossRefGoogle Scholar
  7. Brodsky LI, Ivanov VV, YaL K d, Leontovich AM, Nikolaev VK, Feranchuk SI, Drachev VA (1995) GeneBee-NET: internet-based server for analyzing biopolymers structure. Biokhimiia 60:923–928Google Scholar
  8. Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, Willard HF (1992) The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71:527–542PubMedCrossRefGoogle Scholar
  9. 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, e66532PubMedPubMedCentralCrossRefGoogle Scholar
  10. Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Belknap Press of Harvard University, CambridgeCrossRefGoogle Scholar
  11. 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 20:279–292PubMedCrossRefGoogle Scholar
  12. Camacho JP (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286CrossRefGoogle Scholar
  13. Camacho JP, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos T Roy Soc B 355:163–178CrossRefGoogle Scholar
  14. Cao J, Shen Y, Zhu L, Xu Y, Zhou Y, Wu Z, Li Y, Yan X, Zhu X (2012) miR-129-3p controls cilia assembly by regulating CP110 and actin dynamics. Nat Cell Biol 14:697–706PubMedCrossRefGoogle Scholar
  15. Carchilan M, Kumke K, Mikolajewski S, Houben A (2009) Rye B chromosomes are weakly transcribed and might alter the transcriptional activity of A chromosome sequences. Chromosoma 118:607–616PubMedCrossRefGoogle Scholar
  16. Carlson W (2009) The B chromosome of maize, in: Bennetzen JL, Hake S (Eds.), Maize handbook—Volume II: genetics and genomics, Springer, pp. 459–480Google Scholar
  17. Carone DM, Longo MS, Ferreri GC, Hall L, Harris M, Shook N, Bulazel KV, Carone BR, Obergfell C, O’Neill MJ (2009) A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 118:113–125PubMedCrossRefGoogle Scholar
  18. Carvalho AB (2002) Origin and evolution of the Drosophila Y chromosome. Curr Opin Genet Dev 12:664–668PubMedCrossRefGoogle Scholar
  19. Coolen M, Katz S, Bally-Cuif L (2013) mir-9: a versatile regulator of neurogenesis. Front Cell Neurosci 7:220PubMedPubMedCentralCrossRefGoogle Scholar
  20. Ebert MS, Neilson JR, Sharp PA (2007) MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 4:721–726PubMedCrossRefGoogle Scholar
  21. Eddy SR (2001) Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2:919–929PubMedCrossRefGoogle Scholar
  22. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS (2003) MicroRNA targets in Drosophila. Genome Biol 5:R1PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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 139:1273–1282PubMedCrossRefGoogle Scholar
  24. Feldberg E, Bertollo LAC (1984) Discordance in chromosome number among somatic and gonadal tissue cells of Gymnogeonhagus balzani. Braz J Genet 8:639–645Google Scholar
  25. Feldberg E, Porto JIR, Brinn MNA, Mendonça MNC, Benzaquem DC (2004) B-chromosomes in Amazonian cichlid species. Cytogenet Genome Res 106:195–198PubMedCrossRefGoogle Scholar
  26. Finn RD, Clements J, Eddy SR (2011) HMMER Web Server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37PubMedPubMedCentralCrossRefGoogle Scholar
  27. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M (2014) The Pfam protein families database. Nucleic Acids Res 42:D222–D230PubMedCrossRefGoogle Scholar
  28. Gong C, Maquat LE (2011) lncRNAs transactive STAU1-mediated mRNA decay by duplexing with 3′ UTR via Alu elements. Nature 470:284–288PubMedPubMedCentralCrossRefGoogle Scholar
  29. Graphodatsky AS, Kukekova AV, Yudkin DV, Trifonov VA, Vorobieva NV, Beklemisheva VR, Perelman PL, Graphodatskaya DA, Trut LN, Yang F, Ferguson-Smith MA, Acland GM, Aguirre GD (2005) The proto-oncogene C-KIT maps to canid B-chromosomes. Chromosome Res 13:113–122PubMedCrossRefGoogle Scholar
  30. Griffiths-Jones S (2004) The microRNA registry. Nucleic Acids Res 32:D109–D111PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gupta RA, Shah N, Wang KC, Jeewon K, Horlings HM, Wong DJ, Tsai M-C, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076PubMedPubMedCentralCrossRefGoogle Scholar
  32. Han P, Li W, Lin C-H, Yang J, Shang C, Nurnberg ST, Jin KK, Xu W, Lin C-Y, Lin C-J, Xiong Y, Chien H-C, Zhou B, Ashley E, Bernstein D, Chen P-S, Chen H-SV, Quertermous T, Chang C-P (2014) A long noncoding RNA protects the heart from pathological hypertrophy. Nature 514:102–106PubMedPubMedCentralCrossRefGoogle Scholar
  33. He LP, Ling FY, Zheng XZ, Wang W, Kuang RP (2000) The effect of B chromosome on the reproduction of Drosophila albomicans. Yi Chuan Xue Bao 27:114–120PubMedGoogle Scholar
  34. Houben A, Banaei-Moghaddam AM, Klemme S (2013) Biology and evolution of B chromosomes. In: Leitch IJ (ed) Plant genome diversity, vol 2. Berlin, Springer, pp 149–165CrossRefGoogle Scholar
  35. Johnson R, Guigó R (2014) The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs. RNA 20:959–976PubMedPubMedCentralCrossRefGoogle Scholar
  36. Jones RN (1991) B-chromosome drive. Am Nat 137:430–442CrossRefGoogle Scholar
  37. Jones R, Rees H (1982) B chromosomes. Academic Press, LondonGoogle Scholar
  38. Jones RN, Gonzalez-Sanchez M, Gonzalez-Garcia M, Vega JM, Puertas MJ (2008) Chromosomes with a life of their own. Cytogenet Genome Res 120:265–280PubMedCrossRefGoogle Scholar
  39. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467PubMedCrossRefGoogle Scholar
  40. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316:1484–1488PubMedCrossRefGoogle Scholar
  41. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kelley D, Rinn J (2012) Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Gen Biol 13:R107CrossRefGoogle Scholar
  43. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of accessibility in microRNA target recognition. Nature Genet 39:1278–1284PubMedCrossRefGoogle Scholar
  44. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–98PubMedCrossRefGoogle Scholar
  45. 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 142:112–120PubMedCrossRefGoogle Scholar
  46. Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359PubMedPubMedCentralCrossRefGoogle Scholar
  47. Laurent GS, Wahlestedt C, Kapranov P (2015) The landscape of long noncoding RNA classification. Trends in Genet 31:239–251CrossRefGoogle Scholar
  48. Leach CR, Houben A, Field B, Pistrick K, Demidov D, Timmis JN (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaries. Genetics 171:269–278PubMedPubMedCentralCrossRefGoogle Scholar
  49. Leucci E, Patella F, Waage J, Holmstrøm K, Lindow M, Porse B (2013) microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci Rep 3:2535PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lin HZ, Lin WD, Lin CY, Peng SF, Cheng YM (2014) Characterization of maize B-chromosome-related transcripts isolated via cDNA-AFLP. Chromosoma 123:597–607PubMedCrossRefGoogle Scholar
  51. Lorenz R, Bernhart SH, Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL (2011) ViennaRNA package 2.0. Algorithm Mol Biol 6:26CrossRefGoogle Scholar
  52. Martins-Santos IC, Portela-Castro ALB, Julio HF Jr (1995) Chromosome analysis of 5 species of the Cichlidae family (Pisces, Perciformes) from the Paraná River. Cytologia 60:223–231CrossRefGoogle Scholar
  53. 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 109:13343–13346PubMedPubMedCentralCrossRefGoogle Scholar
  54. Mattick JS, Makunin V (2006) Non-coding RNA. Hum Mol Genet 15:R17–R29PubMedCrossRefGoogle Scholar
  55. McHugh CA, Chen CK, Chow A, Surka CF, Tran C, McDonel P, Pandya-Jones A, Blanco M, Burghard C, Moradian A, Sweredoski MJ, Shishkin AA, Su J, Lander ES, Hess S, Plath K, Guttman M (2015) The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 521:232–236PubMedPubMedCentralCrossRefGoogle Scholar
  56. Miao VP, Covert SF, VanEtten HD (1991) A fungal gene for antibiotic resistance on a dispensable (“B”) Chromosome. Science 254:1773–1776PubMedCrossRefGoogle Scholar
  57. Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 32:1372–1379PubMedGoogle Scholar
  58. Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2014) Rfam 12.0: updates to the RNA families database. Nucleic Acids Res 43:D130–D137PubMedPubMedCentralCrossRefGoogle Scholar
  59. Neo DM, Moreira-Filho O, Camacho JMP (2000) Altitudinal variation for B chromosome frequency in the characid fish Astyanax scabripinnis. Heredity 85:136–141PubMedCrossRefGoogle Scholar
  60. Nokkala S, Grozeva S, Kuznetsova V, Maryañska-Nadachowska A (2003) The origin of the achiasmatic XY sex chromosome system in Cacopsylla peregrina (Frst.) (Psylloidea, Homoptera). Genetica 119:327–32PubMedCrossRefGoogle Scholar
  61. Palestis BG, Trivers R, Burt A, Jones RN (2004) The distribution of B chromosomes across species. Cytogenet Genome Res 106:151–158PubMedCrossRefGoogle Scholar
  62. Pang KC, Frith MC, Mattick JS (2006) Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends in Genet 22:1–5CrossRefGoogle Scholar
  63. Pang KC, Dinger ME, Mercer TR, Malquori L, Grimmond SM, Chen W, Mattick JS (2009) Genome-wide identification of long noncoding RNAs in CD8+ T cells. J Immunol 182:7738–7748PubMedCrossRefGoogle Scholar
  64. Pickard MR, Williams GT (2014) Regulation of apoptosis by long non-coding RNA GAS5 in breast cancer cells: implications for chemotherapy. Breast Cancer Res Tr 145:359–370CrossRefGoogle Scholar
  65. Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A 83:2934–2938PubMedPubMedCentralCrossRefGoogle Scholar
  66. Poletto AB, Ferreira IA, Martins C (2010a) The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genet 11:1PubMedPubMedCentralCrossRefGoogle Scholar
  67. Poletto AB, Ferreira IA, Cabral-de-Mello DC, Nakajima RT, Mazzuchelli J, Ribeiro HB, Venere PC, Nirchio M, Kocher TD, Martins C (2010b) Chromosome differentiation patterns during cichlid fish evolution. BMC Genet 11:50PubMedPubMedCentralCrossRefGoogle Scholar
  68. Quek XC, Thomson DW, Maag JL, Bartonicek N, Signal B, Clark MB, Gloss BS, Dinger ME (2014) lncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs. Nucleic Acids Res 43:D168–D173PubMedPubMedCentralCrossRefGoogle Scholar
  69. Rajicic M, Adnadevic T, Stamenkovic G, Blagojevic J, Vujosevic M (2015) Screening of B chromosomes for presence of two genes in yellow-necked mice, Apodemus flavicollis (Mammalia, Rodentia). Genetika 47:311–321CrossRefGoogle Scholar
  70. Ruiz-Estévez M, López-León MD, Cabrero J, Camacho JPM (2012) B chromosome ribosomal DNA is functional in the Grasshopper Eyprepocnemis plorans. PLoS One 7, e36600PubMedPubMedCentralCrossRefGoogle Scholar
  71. Sambrook J, Russel DW (2001) Molecular cloning. A laboratory manual (3rd ed) Cold Spring, New YorkGoogle Scholar
  72. Sandelin A, Bailey P, Bruce S, Engström PG, Klos JM, Wasserman WW, Ericson J, Lenhard B (2004) Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 5:99PubMedPubMedCentralCrossRefGoogle Scholar
  73. Simon P (2003) Q-gene: processing quantitative real-time RT-PCR data. Bioinformatics 19:1439–1440PubMedCrossRefGoogle Scholar
  74. Skelton P (2001) A complete guide to the freshwater fishes of Southern Africa (2th) New Holland publishing, South AfricaGoogle Scholar
  75. Smit AFA, Hubley R, Green P (2013–2015) RepeatMasker Open-4.0. <http://www.repeatmasker.org>
  76. Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7:S10PubMedPubMedCentralCrossRefGoogle Scholar
  77. Standaert L, Adriaens C, Radaelli E, Keymeulen AV, Blanpain C, Hirose T, Nakagawa S, Marine J-C (2014) The long noncoding RNA Neat1is required for mammary gland development and lactation. RNA 20:1844–1849PubMedPubMedCentralCrossRefGoogle Scholar
  78. The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212CrossRefGoogle Scholar
  79. Tian E, Borset M, Sawyer JR, Brede G, Vatsveen TK, Hov H, Waage A, Barlogie B, Shaughnessy JD Jr, Epstein J, Sundan A (2015) Allelic mutations in noncoding genomic sequences construct novel transcription factor binding sites that promote gene overexpression. Genes Chromosomes Cancer 54:692–701PubMedCrossRefGoogle Scholar
  80. Treangen TJ, Salzberg SL (2011) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46PubMedPubMedCentralGoogle Scholar
  81. 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 6:90CrossRefGoogle Scholar
  82. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147:1537–1550PubMedPubMedCentralCrossRefGoogle Scholar
  83. Valente GT, Conte MA, Fantinatti BEA, Cabral-de-Mello DC, Carvalho RF, Vicari MR, Kocher TD, Martins C (2014) Origin and evolution of B chromosomes in the cichlid fish Astatotilapia latifasciata based on integrated genomic analyses. Mol Biol Evol 31:2061–2072PubMedCrossRefGoogle Scholar
  84. Vicente VE, Moreira-Filho O, Camacho JPM (1996) Sex-ratio distortion associated with the presence of a B chromosome in Astyanax scabripinnis (Teleostei Characidae). Cytogenet Cell Genet 74:70–75PubMedCrossRefGoogle Scholar
  85. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914PubMedPubMedCentralCrossRefGoogle Scholar
  86. White MJD (1973) Animal cytology and evolution. Cambridge University Press, LondonGoogle Scholar
  87. Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23:1494–1504PubMedPubMedCentralCrossRefGoogle Scholar
  88. Yao H, Ma R, Yang L, Hu G, Chen X, Duan M, Kook Y, Niu F, Liao K, Fu M, Hu G, Kolattukudy P, Buch S (2014) MIR-9 promotes microglial activation by targeting MCPIP1. Nat Commun 5:4386PubMedPubMedCentralGoogle Scholar
  89. Yoon J-H, Abdelmohsen K, Gorospe M (2014) Functional interactions among microRNAs and long noncoding RNAs. Semin Cell Dev Biol 34:9–14PubMedCrossRefGoogle Scholar
  90. 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, e1002203PubMedPubMedCentralCrossRefGoogle Scholar
  91. Zhou Q, Zhu H, Huang Q, Li Z, Zhang G, Roy SW, Vicoso B, Xuan Z, Ruan J, Zhang Y, Zhao R, Ye C, Zhang X, Wang J, Wang W, Bachtrog D (2012) Deciphering neo-sex and B chromosome evolution by the draft genome of Drosophila albomicans. BMC Genomics 13:109PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Érica Ramos
    • 1
  • Adauto L. Cardoso
    • 1
  • Judith Brown
    • 2
  • Diego F. Marques
    • 1
  • Bruno E. A. Fantinatti
    • 1
  • Diogo C. Cabral-de-Mello
    • 3
  • Rogério A. Oliveira
    • 4
  • Rachel J. O’Neill
    • 5
  • Cesar Martins
    • 1
  1. 1.Department of Morphology, Institute of BiosciencesSao Paulo State UniversityBotucatuBrazil
  2. 2.Allied Health Sciences Department and Institute for Systems GenomicsUniversity of ConnecticutStorrsUSA
  3. 3.Department of Biology, Institute of BiosciencesSao Paulo State UniversityRio ClaroBrazil
  4. 4.Department of Biostatistics, Institute of BiosciencesSao Paulo State UniversityBotucatuBrazil
  5. 5.Department of Molecular and Cell Biology and Institute for Systems GenomicsUniversity of ConnecticutStorrsUSA

Personalised recommendations