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B chromosomes: from cytogenetics to systems biology

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Abstract

Though hundreds to thousands of reports have described the distribution of B chromosomes among diverse eukaryote groups, a comprehensive theory of their biological role has not yet clearly emerged. B chromosomes are classically understood as a sea of repetitive DNA sequences that are poor in genes and are maintained by a parasitic-drive mechanism during cell division. Recent developments in high-throughput DNA/RNA analyses have increased the resolution of B chromosome biology beyond those of classical and molecular cytogenetic methods; B chromosomes contain many transcriptionally active sequences, including genes, and can modulate the activity of autosomal genes. Furthermore, the most recent knowledge obtained from omics analyses, which is associated with a systemic view, has demonstrated that B chromosomes can influence cell biology in a complex way, possibly favoring their own maintenance and perpetuation.

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References

  • Akbari OS, Antoshechkin I, Hay BA, Ferree PM (2013) Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio. G3 3:1597–1605

    Article  PubMed  PubMed Central  Google Scholar 

  • Andermann P, Ungos J, Raible DW (2002) Neurogenin1 defines zebrafish cranial sensory ganglia precursors. Dev Biol 251:45–58

    Article  CAS  PubMed  Google Scholar 

  • Ballouz S, Verleyen W, Gillis J (2015) Guidance for RNA-seq co-expression network construction and analysis: safety in numbers. Bioinformatics 31:2123–2130

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banaei-Moghaddam AM, Martis MM, Macas J, Gundlach H, Himmelbach A, Altschmied L, Mayer KFX, Houben A (2015) Genes on B chromosomes: old questions revisited with new tools. Biochim Biophys Acta 1849:64–70

    Article  CAS  PubMed  Google Scholar 

  • Baroni S, Lopes CE, Almeida-Toledo LF (2009) Cytogenetic characterization of Metynnis maculatus (Teleostei; Characiformes): the description in Serrasalminae of a small B chromosome bearing inactive NOR-like sequences. Caryologia 62:95–101

    Article  Google Scholar 

  • Barzel B, Sharma A, Bababási A-L (2012) Graph theory properties of cellular networks. In: Walhout M, Vidal M, Dekker J (eds) Handbook of systems biology: concepts and insights, 1st edn. Academic Press, Cambridge, pp. 177–193

    Google Scholar 

  • Bidau CJ (1986) A nucleolar-organizing B chromosome showing segregation-distortion in the grasshopper Dichroplus pratensis (Melanoplinae, Acrididae. Can J Genet Cytol 28:138–148

    Article  Google Scholar 

  • Bidau CJ, Rosato M, Martí DA (2004) FISH detection of ribosomal cistrons and assortment-distortion for X and B chromosomes in Dichroplus pratensis (Acrididae. Cytogenet Genome Res 106:295–301

    Article  CAS  PubMed  Google Scholar 

  • Brockhouse C, Bas JAB, Fereday RM, Strauss NA (1989) Supernumerary chromosomes evolution in the Simulium vernum group (Diptera: Simulidae. Genome 32:516–521

    Article  Google Scholar 

  • Bueno D, Palacios-Gimenez OM, Cabral-de-Mello DC (2013) Chromosomal mapping of repetitive DNAs in Abracris flavolineata reveal possible ancestry for the B chromosome and surprisingly H3 histone spreading. PLoS One 8:e66532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Belknap Press of Harvard University, Cambridge

    Book  Google Scholar 

  • Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome, 1st edn. Elsevier, San Diego, pp. 223–286

    Chapter  Google Scholar 

  • Camacho JP, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos T Roy Soc B 355:163–178

    Article  CAS  Google Scholar 

  • Carchilan M, Delgado M, Ribeiro T, Costa-Nunes P, Caperta A, Morais-Cecilio L, Jones RN, Viegas W, Houben A (2007) Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19:1738–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 118:607–616

    Article  CAS  PubMed  Google Scholar 

  • Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, et al. (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5:e1000618

    Article  PubMed  PubMed Central  Google Scholar 

  • Donald TM, Leach CR, Clough A, Timmis JN (1995) Ribosomal RNA genes and the B chromosome of Brachycome dichromosomatica. Heredity 74:556–561

    Article  CAS  PubMed  Google Scholar 

  • Furusawa M, Ohnishi T, Taira T, Iguchi-Ariga SM, Ariga HJ (2001) AMY-1, a c-Myc-binding protein, is localized in the mitochondria of sperm by association with S-AKAP84, an anchor protein of cAMP-dependent protein kinase. Biol Chem 276:36647–36651

    Article  CAS  Google Scholar 

  • Gall JG, Pardue ML (1969) Formation and detection of RNA-DNA hybrid molecules in cytological preparations. Proc Natl Acad Sci U S A 63:378–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodwin SB, M’barek SB, Dhillon B, Wittenberg AHJ, Crane CF, et al. (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graphodatsky AS, Kukekova AV, Yudkin DV, Trifonov VA, Vorobieva NV, Beklemisheva VR, et al. (2005) The proto-oncogene c-KIT maps to canid B-chromosomes. Chromosom Res 13:113–122

    Article  CAS  Google Scholar 

  • Huang W, Du Y, Zhao X, Jin W (2016) B chromosome contains active genes and impacts the transcription of a chromosomes in maize (Zea mays L.). BMC Plant Biol 16:88

  • Jones RN (1991) B-chromosome drive. Am Nat 137:430–442

    Article  Google Scholar 

  • Jones RN (1995) B chromosomes in plants. New Phytol 131:411–434

    Article  Google Scholar 

  • Jones RN, Rees H (1982) B chromosomes. Academic Press, London

    Google Scholar 

  • Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH (2014) Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–811

    Article  CAS  PubMed  Google Scholar 

  • Klemme S, Banaei-Moghaddam AM, Macas J, Wicker T, Novak P, Houben A (2013) High-copy sequences reveal distinct evolution of the rye B chromosome. New Phytol 199:550–558

    Article  CAS  PubMed  Google Scholar 

  • Lamb JC, Riddle NC, Cheng YM, Theuri J, Birchler JA (2007) Localization and transcription of a retrotransposon-derived element on the maize B chromosome. Chromosom Res 15:383–398

    Article  CAS  Google Scholar 

  • Leach CR, Houben A, Bruce F, Pistrick K, Demidov D, et al. (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaris. Genetics 171:269–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-León M, Neves N, Schwarzacher T, Heslop-Harrison J, Hewitt G, Camacho J (1994) Possible origin of a B chromosome deduced from its DNA composition using double FISH technique. Chromosom Res 2:87–92

    Article  Google Scholar 

  • Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrána J, Doležel J, Grundlach H, Altschmied L, Scholz U, Himmelbach A, Behrens SE, Banaei-Moghaddam AM, Houben A (2016) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to it's a chromosome paralog. New Phytol doi. doi:10.1111/nph.14110

    Google Scholar 

  • Martins C, Cabral-de-Mello DC, Valente GT, Mazzuchelli J, Oliveira SG, Pinhal D (2011) Animal genomes under the focus of cytogenetics. Nova Science Publisher, Hauppauge

    Google Scholar 

  • Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, et al. (2012) Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Nat Ac Sci USA 109:13343–13346

    Article  CAS  Google Scholar 

  • McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD (1998) The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94:363–374

    Article  CAS  PubMed  Google Scholar 

  • Miao VP, Covert SF, Van Etten HD (1991) A fungal gene for antibiotic resistance on a dispensable (“B”) chromosome. Science 254:1773–1776

    Article  CAS  PubMed  Google Scholar 

  • Morris KV, Mattick JS (2014) The rise of regulatory RNA. Nat Rev Genet 15:423–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira NL, Cabral-de-Mello DC, Rocha MF, Loreto V, Martins C, Moura RC (2011) Chromosomal mapping of rDNAs and H3 histone sequences in the grasshopper Rhammatocerus brasiliensis (Acrididae, Gomphocerinae): extensive chromosomal dispersion and co-localization of 5S rDNA/H3 histone clusters in the A complement and B chromosome. Mol Cytogenet 4:24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onoguchi M, Hirabayashi Y, Koseki H, Gotoh Y (2012) A noncoding RNA regulates the neurogenin1 gene locus during mouse neocortical development. Proc Nat Ac Sci USA 109:16939–16944

    Article  CAS  Google Scholar 

  • Pardue ML, Gall JG (1969) Molecular hybridization of radioactive DNA to the DNA of cytological preparations. Proc Natl Acad Sci U S A 64:600–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramos E, Cardoso AL, Brown J, Marques DF, Fantinatti BEA, Cabral-de-Mello DC, Oliveira RA, O'Neill RJ, Martins C (2016) The repetitive DNA element BncDNA, enriched in the B chromosome of the cichlid fish Astatotilapia latifasciata, transcribes a potentially noncoding RNA. Chromosoma (in press)

  • Rinn J, Guttman M (2014) RNA and dynamic nuclear organization. Science 345:1240–1241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruìz-Estévez M, López-León MD, Cabrero J, Camacho JP (2013) Ribosomal DNA is active in different B chromosome variants of the grasshopper Eyprepocnemis plorans. Genetica 141:337–345

    Article  PubMed  Google Scholar 

  • Ruìz-Estévez M, Badisco L, Broeck JV, Perfectti F, Lopez-Leon MD, Cabrero J, Camacho JP (2014) B chromosomes showing active ribosomal RNA genes contribute insignificant amounts of rRNA in the grasshopper Eyprepocnemis plorans. Mol Gen Genomics 289:1209–1216

    Article  Google Scholar 

  • Silva MJJ, Yonenaga-Yassuda Y (2004) B chromosomes in Brazilian rodents. Cytogenet Genome Res 106:257–263

    Article  CAS  PubMed  Google Scholar 

  • Silva DMZA, Pansonato-Alves JC, Utsunomia R, Araya-Jaime C, Ruiz-Ruano FJ, et al. (2014) Delimiting the origin of a B chromosome by fish mapping, chromosome painting and DNA sequence analysis in Astyanax paranae (Teleostei, Characiformes. PLoS One 9:e94896

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva DMZA, Daniel SN, Camacho JP, Utsunomia R, Ruiz-Ruano FJ, Penitente M, Pansonato-Alves JC, Hashimoto DT, Oliveira C, Porto-Foresti F, Foresti F (2016) Origin of B chromosomes in the genus Astyanax (Characiformes, Characidae) and the limits of chromosome painting. Mol Gen Genomics 291:1407–1418

    Article  CAS  Google Scholar 

  • Stitou S, de la Guardia D, Jiménez R, Burgos M (2000) Inactive ribosomal cistrons are spread throughout the B chromosomes of Rattus rattus (Rodentia, Muridae). Implications for their origin and evolution. Chromosom Res 8:305–311

    Article  CAS  Google Scholar 

  • Taira T, Maëda J, Onishi T, Kitaura H, Yoshida S, Kato H, Ikeda M, Tamai K, Iguchi-Ariga SM, Ariga H (1998) AMY-1, a novel C-MYC binding protein that stimulates transcription activity of C-MYC. Genes Cells 3:549–565

    Article  CAS  PubMed  Google Scholar 

  • Teruel M, Cabrero J, Perfectti F, Camacho JPM (2010) B chromosome ancestry revealed by histone genes in the migratory locust. Chromosoma 119:217–225

    Article  CAS  PubMed  Google Scholar 

  • Trifonov VA, Dementyeva PV, Larkin DM, O’Brien PC, Perelman PL, Yang F, et al. (2013) Transcription of a protein-coding gene on B chromosomes of the Siberian roe deer (Capreolus pygargus. BMC Biol 11:90

    Article  PubMed  PubMed Central  Google Scholar 

  • Utsunomia R, Silva DMZA, Ruiz-Ruano FJ, Araya-Jaime C, Pansonato-Alves JC, Scacchetti PC, et al. (2016) Uncovering the ancestry of B chromosomes in Moenkhausia sanctaefilomenae (Teleostei, Characidae). PLoS One 11:e0150573

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 31:2061–2072

    Article  CAS  PubMed  Google Scholar 

  • van Vugt JJFA, de Nooijer S, Stouthamer R, de Jong H (2005) NOR activity and repeat sequences of the paternal sex ratio chromosome of the parasitoid wasp Trichogramma kaykai. Chromosoma 114:410–419

    Article  PubMed  Google Scholar 

  • Wilson EB (1907) The supernumerary chromosomes of Hemiptera. Science 26:870–871

    Article  Google Scholar 

  • Wittenberg AHJ, van der Lee TAJ, Ben M'Barek S, Ware SB, Goodwin SB, et al. (2009) Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One 4:e5863

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu KJ, Grandori C, Amacker M, Simon-Vermot N, Polack A, Lingner J, Dalla-Favera R (1999) Direct activation of TERT transcription by c-MYC. Nat Genet 21:220–224

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, et al. (2011) B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet 7:e1002203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yudkin DV, Trifonov VA, Kukekova AV, Vorobieva NV, Rubtsova NV, Yang F, et al. (2007) Mapping of KIT adjacent sequences on canid autosomes and B chromosomes. Cytogenet Genome Res 116:100–103

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

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

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Correspondence to Cesar Martins.

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The authors declare that they have no competing interests.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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

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

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This article is related to the 21st International Chromosome Conference (Foz do Iguaçu, Brazil, July 10–13, 2016).

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Valente, G.T., Nakajima, R.T., Fantinatti, B.E.A. et al. B chromosomes: from cytogenetics to systems biology. Chromosoma 126, 73–81 (2017). https://doi.org/10.1007/s00412-016-0613-6

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