Skip to main content
SpringerLink
Log in

Evolution and biology of supernumerary B chromosomes

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

B chromosomes (Bs) are dispensable components of the genome exhibiting non-Mendelian inheritance and have been widely reported on over several thousand eukaryotes, but still remain an evolutionary mystery ever since their first discovery over a century ago [1]. Recent advances in genome analysis have significantly improved our knowledge on the origin and composition of Bs in the last few years. In contrast to the prevalent view that Bs do not harbor genes, recent analysis revealed that Bs of sequenced species are rich in gene-derived sequences. We summarize the latest findings on supernumerary chromosomes with a special focus on the origin, DNA composition, and the non-Mendelian accumulation mechanism of Bs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

As:

Standard chromosomes

Bs:

Supernumerary B chromosomes

FISH:

Fluorescence in situ hybridization

miRNA:

microRNA

NUPT:

Nuclear integrants of plastid DNA

NUMT:

Nuclear integrants of mitochondrial DNA

NORG:

Nuclear integrants of cytoplasmic organellar DNA

SNP:

Single nucleotide polymorphism

References

  1. Wilson EB (1907) The supernumerary chromosomes of Hemiptera. Science 26:870

    Google Scholar 

  2. Pennisi E (2012) Genomics encode project writes eulogy for junk DNA. Science 337(6099):1159–1161

    CAS  PubMed  Google Scholar 

  3. Liehr T, Mrasek K, Kosyakova N, Ogilvie CM, Vermeesch J, Trifonov V, Rubtsov N (2008) Small supernumerary marker chromosomes (sSMC) in humans; are there B chromosomes hidden among them. Mol Cytogenet 1(1):12

    PubMed Central  PubMed  Google Scholar 

  4. Jones N, Houben A (2003) B chromosomes in plants: escapees from the A chromosome genome? Trends Plant Sci 8(9):417–423

    CAS  PubMed  Google Scholar 

  5. Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond B 355(1394):163–178

    CAS  Google Scholar 

  6. Houben A, Banaei Moghaddam AM, Klemme S (2013) Biology and evolution of B chromosomes. In: Leich IK (ed) Plant genome diversity physical structure behaviour and evolution of plant genomes. Springer, Wien, pp 149–166

    Google Scholar 

  7. Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, CA, pp 223–285

    Google Scholar 

  8. Bougourd SM, Jones RN (1997) B chromosomes: a physiological enigma. New Phytol 137(1):43–54

    Google Scholar 

  9. Mendelson D, Zohary D (1972) Behavior and transmission of supernumerary chromosomes in Aegilops speltoides. Heredity 29 (Dec):329–339

    Google Scholar 

  10. Ohta S (1996) Mechanisms of B-chromosome accumulation in Aegilops mutica Boiss. Genes Genet Syst 71(1):23–29

    Google Scholar 

  11. Nur U (1969) Mitotic instability leading to an accumulation of B chromosomes in grasshoppers. Chromosoma 27(1):1–19. doi:10.1007/Bf00326108

    CAS  PubMed  Google Scholar 

  12. Houben A, Thompson N, Ahne R, Leach CR, Verlin D, Timmis JN (1999) A monophyletic origin of the B chromosomes of Brachycome dichromosomatica (Asteraceae). Plant Syst Evol 219(1–2):127–135

    CAS  Google Scholar 

  13. Parker JS, Jones GH, Edgar LA, Whitehouse C (1991) The population cytogenetics of Crepis capillaris. 4. The Distribution of B-chromosomes in British populations. Heredity 66:211–218

    Google Scholar 

  14. Bougourd SM, Parker JS (1979) B-chromosome system of Allium schoenoprasum 2 Stability, inheritance and phenotypic effects. Chromosoma 75(3):369–383. doi:10.1007/Bf00293478

    Google Scholar 

  15. Belyayev A, Raskina O (2013) Chromosome evolution in marginal populations of Aegilops speltoides: causes and consequences. Ann Bot 111(4):531–538. doi:10.1093/Aob/Mct023

    CAS  PubMed  Google Scholar 

  16. Bakkali M, Cabrero J, Lopez-Leon MD, Perfectti F, Camacho JPM (1999) The B chromosome polymorphism of the grasshopper Eyprepocnemis plorans in north Africa. I. B variants and frequency. Heredity 83:428–434

    PubMed  Google Scholar 

  17. Marques A, Banaei-Moghaddam AM, Klemme S, Blattner FR, Niwa K, Guerra M, Houben A (2013) B chromosomes of rye are highly conserved and accompanied the development of early agriculture. Ann Bot 112(3):527–534

    Google Scholar 

  18. Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinforma 11:378. doi:1471-2105-11-378

    Google Scholar 

  19. Mayer KF, Martis M, Hedley PE, Simkova H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubalakova M, Suchankova P, Murat F, Felder M, Nussbaumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Dolezel J, Waugh R, Stein N (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23(4):1249–1263

    CAS  PubMed Central  PubMed  Google Scholar 

  20. Lamb JC, Riddle NC, Cheng YM, Theuri J, Birchler JA (2007) Localization and transcription of a retrotransposon-derived element on the maize B chromosome. Chromosome Res 15(3):383–398

    CAS  PubMed  Google Scholar 

  21. Houben A, Verlin D, Leach CR, Timmis JN (2001) The genomic complexity of micro B chromosomes of Brachycome dichromosomatica. Chromosoma 110(7):451–459

    CAS  PubMed  Google Scholar 

  22. Dhar MK, Friebe B, Koul AK, Gill BS (2002) Origin of an apparent B chromosome by mutation, chromosome fragmentation and specific DNA sequence amplification. Chromosoma 111(5):332–340

    CAS  PubMed  Google Scholar 

  23. Gonzalez-Sanchez M, Chiavarino M, Jimenez G, Manzanero S, Rosato M, Puertas MJ (2004) The parasitic effects of rye B chromosomes might be beneficial in the long term. Cytogenet Genome Res 106:386–393

    CAS  PubMed  Google Scholar 

  24. Niwa K, Sakamoto S (1996) Detection of B chromosomes in rye collected from Pakistan and China. Hereditas 124(3):211–215

    Google Scholar 

  25. Niwa K, Sakamoto S (1995) Origin of B-chromosomes in cultivated rye. Genome 38(2):307–312

    CAS  PubMed  Google Scholar 

  26. Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Simkova H, Novak P, Neumann P, Kubalakova M, Bauer E, Haseneyer G, Fuchs J, Dolezel J, Stein N, Mayer KF, Houben A (2012) Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Natl Acad Sci USA 109(33):13343–13346

    CAS  PubMed  Google Scholar 

  27. Becker SE, Thomas R, Trifonov VA, Wayne RK, Graphodatsky AS, Breen M (2011) Anchoring the dog to its relatives reveals new evolutionary breakpoints across 11 species of the Canidae and provides new clues for the role of B chromosomes. Chromosome Res 19(6):685–708

    PubMed  Google Scholar 

  28. Wicker T, Mayer KF, Gundlach H, Martis M, Steuernagel B, Scholz U, Simkova H, Kubalakova M, Choulet F, Taudien S, Platzer M, Feuillet C, Fahima T, Budak H, Dolezel J, Keller B, Stein N (2011) Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives. Plant Cell 23(5):1706–1718

    CAS  PubMed Central  PubMed  Google Scholar 

  29. 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. doi:10.1111/nph.12289

    CAS  PubMed  Google Scholar 

  30. Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10(7):908–915. doi:10.1101/Gr.10.7.908

    CAS  PubMed  Google Scholar 

  31. Tomita M, Shinohara K, Morimoto M (2008) Revolver is a new class of transposon-like gene composing the triticeae genome. DNA Res 15(1):49–62

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Ziegler CG, Lamatsch DK, Steinlein C, Engel W, Schartl M, Schmid M (2003) The giant B chromosome of the cyprinid fish Alburnus alburnus harbours a retrotransposon-derived repetitive DNA sequence. Chromosome Res 11(1):23–35

    CAS  PubMed  Google Scholar 

  33. Coleman JJ, Rounsley SD, Rodriguez-Carres M, Kuo A, Wasmann CC, Grimwood J, Schmutz J, Taga M, White GJ, Zhou S, Schwartz DC, Freitag M, Ma LJ, Danchin EG, Henrissat B, Coutinho PM, Nelson DR, Straney D, Napoli CA, Barker BM, Gribskov M, Rep M, Kroken S, Molnar I, Rensing C, Kennell JC, Zamora J, Farman ML, Selker EU, Salamov A, Shapiro H, Pangilinan J, Lindquist E, Lamers C, Grigoriev IV, Geiser DM, Covert SF, Temporini E, Vanetten HD (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet 5(8):e1000618. doi:10.1371/journal.pgen.1000618

    PubMed Central  PubMed  Google Scholar 

  34. Charlesworth D (2008) Plant sex chromosomes. Genome Dyn 4:83–94

    CAS  PubMed  Google Scholar 

  35. Zhu Y, Dai J, Fuerst PG, Voytas DF (2003) Controlling integration specificity of a yeast retrotransposon. Proc Natl Acad Sci USA 100(10):5891–5895. doi:10.1073/pnas.1036705100

    CAS  PubMed  Google Scholar 

  36. Tsukahara S, Kawabe A, Kobayashi A, Ito T, Aizu T, Shin IT, Toyoda A, Fujiyama A, Tarutani Y, Kakutani T (2012) Centromere-targeted de novo integrations of an LTR retrotransposon of Arabidopsis lyrata. Genes Dev 26:705–713. doi:10.1101/gad.183871.111

    CAS  PubMed  Google Scholar 

  37. Kejnovsky E, Vyskot B (2010) Silene latifolia: the classical model to study heteromorphic sex chromosomes. Cytogenet Genome Res 129(1–3):250–262. doi:10.1159/000314285

    CAS  PubMed  Google Scholar 

  38. Alfenito MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135(2):589–597

    CAS  PubMed  Google Scholar 

  39. Stark EA, Connerton I, Bennett ST, Barnes SR, Parker JS, Forster JW (1996) Molecular analysis of the structure of the maize B-chromosome. Chromosome Res 4(1):15–23

    CAS  PubMed  Google Scholar 

  40. Sandery MJ, Forster JW, Blunden R, Jones RN (1990) Identification of a family of repeated sequences on the rye B-chromosome. Genome 33(6):908–913

    CAS  Google Scholar 

  41. Langdon T, Seago C, Jones RN, Ougham H, Thomas H, Forster JW, Jenkins G (2000) De novo evolution of satellite DNA on the rye B chromosome. Genetics 154(2):869–884

    CAS  PubMed  Google Scholar 

  42. Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191(4227):528–535

    CAS  PubMed  Google Scholar 

  43. Devos KM, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojc P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85(6–7):673–680

    CAS  PubMed  Google Scholar 

  44. Zhou Q, Zhu HM, Huang QF, Zhao L, Zhang GJ, Roy SW, Vicoso B, Xuan ZL, Ruan J, Zhang Y, Zhao RP, Ye C, Zhang XQ, Wang J, Wang W, Bachtrog D (2012) Deciphering neo-sex and B chromosome evolution by the draft genome of Drosophila albomicans. Bmc Genomics 13:109. doi:10.1186/1471-2164-13-109

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Sheppard AE, Ayliffe MA, Blatch L, Day A, Delaney SK, Khairul-Fahmy N, Li Y, Madesis P, Pryor AJ, Timmis JN (2008) Transfer of plastid DNA to the nucleus is elevated during male gametogenesis in tobacco. Plant Physiol 148(1):328–336. doi:10.1104/pp.108.119107

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Wang D, Lloyd AH, Timmis JN (2012) Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants. Proc Natl Acad Sci USA 109(7):2444–2448. pii: 1117890109

    CAS  PubMed  Google Scholar 

  47. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123 U116

    CAS  PubMed  Google Scholar 

  48. Sheppard AE, Timmis JN (2009) Instability of plastid DNA in the nuclear genome. PLoS Genet 5(1):e1000323. doi:10.1371/journal.pgen.1000323

    PubMed Central  PubMed  Google Scholar 

  49. Jones RN, Rees H (1982) B chromosomes, 1st edn. Academic Press, London, New York

    Google Scholar 

  50. Jones RN (1995) Tansley Review No 85, B chromosomes in plants. New Phytol 131:411–434

    Google Scholar 

  51. Carlson W (2009) The B chromosome of maize. In: Bennetzen JL, Hake S (eds) Maize Handbook. Genetics and Genomics, vol II. Springer, Heidelberg, pp 459–480

  52. Holmes DS, Bougourd SM (1991) B-Cchromosome selection in Allium schoenoprasum. 2. experimental populations. Heredity 67:117–122

    Google Scholar 

  53. Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A, Hirai H, Hirai Y, Matsuda Y, Okada N (2011) B Chromosomes have a functional effect on female sex determination in lake Victoria cichlid fishes. Plos Genetics 7(8):e1002203. doi:10.1371/journal.pgen.1002203

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Jackson RC, Newmark P (1960) Effects of supernumerary chromosomes on production of pigment in Haplopappus gracilis. Science 132(3436):1316–1317

    CAS  PubMed  Google Scholar 

  55. Dover GA, Riley R (1972) Prevention of pairing of homoeologous meiotic chromosomes of wheat by an activity of supernumerary chromosomes of Aegilops. Nature 240(5377):159

    Google Scholar 

  56. Kousaka R, Endo TR (2012) Effect of a rye B chromosome and its segments on homoeologous pairing in hybrids between common wheat and Aegilops variabilis. Genes Genet Syst 87(1):1–7 pii: JST.JSTAGE/ggs/87.1

    PubMed  Google Scholar 

  57. Staub RW (1987) Leaf striping correlated with the presence of B-chromosomes in maize. J Hered 78(2):71–74

    Google Scholar 

  58. Dherawat A, Sadanaga K (1973) Cytogenetics of a crown rust-resistant hexaploid Oat with 42 + 2 fragment chromosomes. Crop Sci 13(6):591–594

    Google Scholar 

  59. Fox DP, Hewitt GM, Hall DJ (1974) DNA-replication and RNA transcription of euchromatic and heterochromatic chromosome regions during grasshopper meiosis. Chromosoma 45(1):43–62

    CAS  PubMed  Google Scholar 

  60. Ishak B, Jaafar H, Maetz JL, Rumpler Y (1991) Absence of transcriptional activity of the B-chromosomes of Apodemus peninsulae during pachytene. Chromosoma 100(4):278–281. doi:10.1007/Bf00344162

    Google Scholar 

  61. Teruel M, Cabrero J, Perfectti F, Camacho JPM (2010) B chromosome ancestry revealed by histone genes in the migratory locust. Chromosoma 119(2):217–225. doi:10.1007/s00412-009-0251-3

    CAS  PubMed  Google Scholar 

  62. 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. doi:10.1186/1471-2156-11-1

    PubMed Central  PubMed  Google Scholar 

  63. Houben A, Leach CR, Verlin D, Rofe R, Timmis JN (1997) A repetitive DNA sequence common to the different B chromosomes of the genus Brachycome. Chromosoma 106(8):513–519

    CAS  PubMed  Google Scholar 

  64. Donald TM, Leach CR, Clough A, Timmis JN (1995) Ribosomal RNA genes and the B chromosome of Brachycome dichromosomatica. Heredity 74(5):556–561

    CAS  PubMed  Google Scholar 

  65. 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 capillaris. Genetics 171:269–278

    CAS  PubMed  Google Scholar 

  66. Banaei-Moghaddam AM, Meier K, Karimi-Ashtiyani R, Houben A (2013) Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell (in press)

  67. Green DM (1988) Cytogenetics of the endemic New Zealand frog, Leiopelma hochstetteri - Extraordinary supernumerary chromosome variation and a unique sex chromosome system. Chromosoma 97(1):55–70

    Google Scholar 

  68. Brockhouse C, Bass JAB, Feraday RM, Straus NA (1989) Supernumerary chromosome evolution in the Simulium vernum Group (Diptera, Simuliidae). Genome 32(4):516–521

    Google Scholar 

  69. Tanic N, Vujosevic M, Dedovic-Tanic N, Dimitrijevic B (2005) Differential gene expression in yellow-necked mice Apodemus flavicollis (Rodentia, Mammalia) with and without B chromosomes. Chromosoma 113(8):418–427

    CAS  PubMed  Google Scholar 

  70. Graphodatsky AS, Kukekova AV, Yudkin DV, Trifonov VA, Vorobieva NV, Beklemisheva VR, Perelman PL, Graphodatskaya DA, Trut LN, Yang FT, Ferguson-Smith MA, Acland GM, Aguirre GD (2005) The proto-oncogene C-KIT maps to canid B-chromosomes. Chromosome Res 13(2):113–122

    CAS  PubMed  Google Scholar 

  71. Yudkin DV, Trifonov VA, Kukekova AV, Vorobieva NV, Rubtsova NV, Yang F, Acland GM, Ferguson-Smith MA, Graphodatsky AS (2007) Mapping of KIT adjacent sequences on canid autosomes and B chromosomes. Cytogenet Genome Res 116(1–2):100–103. doi:10.1159/000097424

    CAS  PubMed  Google Scholar 

  72. Covert SF, Enkerli J, Miao VP, VanEtten HD (1996) A gene for maackiain detoxification from a dispensable chromosome of Nectria haematococca. Mol Gen Genet: MGG 251(4):397–406

    CAS  PubMed  Google Scholar 

  73. Han Y, Liu X, Benny U, Kistler HC, VanEtten HD (2001) Genes determining pathogenicity to pea are clustered on a supernumerary chromosome in the fungal plant pathogen Nectria haematococca. Plant J 25(3):305–314

    CAS  PubMed  Google Scholar 

  74. Covert SF (1998) Supernumerary chromosomes in filamentous fungi. Curr Genet 33(5):311–319

    CAS  PubMed  Google Scholar 

  75. VanEtten H, Funnell-Baerg D, Wasmann C, McCluskey K (1994) Location of pathogenicity genes on dispensable chromosomes in Nectria haematococca MPVI. Antonie van Leeuwenhoek 65(3):263–267

    CAS  PubMed  Google Scholar 

  76. Funnell DL, VanEtten HD (2002) Pisatin demethylase genes are on dispensable chromosomes while genes for pathogenicity on carrot and ripe tomato are on other chromosomes in Nectria haematococca. Mol Plant Microbe In 15(8):840–846. doi:10.1094/Mpmi.2002.15.8.840

    CAS  Google Scholar 

  77. Funnell DL, Matthews PS, VanEtten HD (2002) Identification of new pisatin demethylase genes (PDA5 and PDA7) in Nectria haematococca and non-Mendelian segregation of pisatin demethylating ability and virulence on pea due to loss of chromosomal elements. Fungal Genet Biol 37(2):121–133. doi:10.1016/S1087-1845(02)00503-0

    CAS  PubMed  Google Scholar 

  78. Rodriguez-Carres A, White G, Tsuchiya D, Taga M, VanEtten HD (2008) The supernumerary chromosome of Nectria haematococca that carries pea-pathogenicity-related genes also carries a trait for pea rhizosphere competitiveness. Appl Environ Microbiol 74(12):3849–3856. doi:10.1128/Aem.00351-08

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Green DM (1990) Muller`s rachet and the evolution of supernumerary chromosomes. Genome 33:818–824

    Google Scholar 

  80. Ruiz-Estevez M, Lopez-Leon MD, Cabrero J, Camacho JPM (2012) B-Chromosome Ribosomal DNA Is Functional in the Grasshopper Eyprepocnemis plorans. PLoS ONE 7(5):e36600. doi:10.1371/journal.pone.0036600

    CAS  PubMed Central  PubMed  Google Scholar 

  81. 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(5):607–616. doi:10.1007/s00412-009-0222-8

    CAS  PubMed  Google Scholar 

  82. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8(4):272–285

    CAS  PubMed  Google Scholar 

  83. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6(11):836–846

    CAS  PubMed  Google Scholar 

  84. Misteli T (2007) Beyond the sequence: cellular organization of genome function. Cell 128(4):787–800

    CAS  PubMed  Google Scholar 

  85. Lemos B, Araripe LO, Hartl DL (2008) Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. Science 319(5859):91–93

    CAS  PubMed  Google Scholar 

  86. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155

    CAS  PubMed  Google Scholar 

  87. Guo L, Lu ZH (2010) The fate of miRNA* strand through evolutionary analysis: Implication for degradation as merely carrier strand or potential regulatory molecule? PLoS ONE 5(6):e11387. doi:10.1371/journal.pone.0011387

    PubMed Central  PubMed  Google Scholar 

  88. Prestel M, Feller C, Becker PB (2010) Dosage compensation and the global re-balancing of aneuploid genomes. Genome Biol 11(8):216. doi:10.1186/gb-2010-11-8-216

    PubMed Central  PubMed  Google Scholar 

  89. 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(6):1738–1749

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Dalakouras A, Wassenegger M (2013) Revisiting RNA-directed DNA methylation. RNA Biol (in press)

  91. Filipowicz W, Jaskiewicz L, Kolb FA, Pillai RS (2005) Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15(3):331–341. doi:10.1016/j.sbi.2005.05.006

    CAS  PubMed  Google Scholar 

  92. Pink RC, Wicks K, Caley DP, Punch EK, Jacobs L, Carter DR (2011) Pseudogenes: pseudo-functional or key regulators in health and disease? RNA 17(5):792–798. doi:10.1261/rna.2658311

    CAS  PubMed  Google Scholar 

  93. Gordon DJ, Resio B, Pellman D (2012) Causes and consequences of aneuploidy in cancer. Nat Rev 13(3):189–203. doi:10.1038/nrg3123

    CAS  Google Scholar 

  94. Kimura M, Kayano H (1961) The maintenance of supernumerary chromosomes in wild populations of Lillium callosum by preferential segregation. Genetics 46:1699–1712

    CAS  PubMed  Google Scholar 

  95. Burt A, Trivers R (2006) Genes in conflict : The biology of selfish genetic elements. Belknap, Cambridge

    Google Scholar 

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

    Google Scholar 

  97. Roman H (1948) Selective fertilization in maize. Genetics 33(1):122

    CAS  PubMed  Google Scholar 

  98. Carlson WR (1969) Factors affecting preferential fertilization in maize. Genetics 62(3):543–554

    CAS  PubMed  Google Scholar 

  99. Rusche ML, Mogensen HL, Shi L, Keim P, Rougier M, Chaboud A, Dumas C (1997) B chromosome behavior in maize pollen as determined by a molecular probe. Genetics 147(4):1915–1921

    CAS  PubMed  Google Scholar 

  100. Carlson WR, Roseman RR (1992) A new property of the maize B-chromosome. Genetics 131(1):211–223

    CAS  PubMed  Google Scholar 

  101. Gonzalez-Sanchez M, Gonzalez-Gonzalez E, Molina F, Chiavarino AM, Rosato M, Puertas MJ (2003) One gene determines maize B chromosome accumulation by preferential fertilisation; another gene(s) determines their meiotic loss. Heredity 90(2):122–129

    CAS  PubMed  Google Scholar 

  102. Carlson WR (2007) Locating a site on the maize B chromosome that controls preferential fertilization. Genome 50(6):578–587

    CAS  PubMed  Google Scholar 

  103. Hasegawa N (1934) A cytological study on 8-chromosome rye. Cytologia 6:68–77

    Google Scholar 

  104. Hakansson A (1948) Behaviour of accessory rye chromosomes in the embryo sac. Hereditas 34:35–59

    Google Scholar 

  105. Endo TR, Nasuda S, Jones N, Dou Q, Akahori A, Wakimoto M, Tanaka H, Niwa K, Tsujimoto H (2008) Dissection of rye B chromosomes, and nondisjunction properties of the dissected segments in a common wheat background. Genes Genet Syst 83(1):23–30

    PubMed  Google Scholar 

  106. Müntzing A (1948) Cytological studies of extra fragment chromosomes in rye. V. A new fragment type arisen by deletion. Hereditas 34:435–442

    Google Scholar 

  107. Håkanson A (1959) Behaviour of different small accessry rye chromosomes at pollen mitosis. Hereditas 45:623–631

    Google Scholar 

  108. Lima-de-Faria A (1962) Genetic interaction in rye expressed at chromosome phenotype. Genetics 47:1455–1462

    CAS  PubMed  Google Scholar 

  109. Banaei-Moghaddam AM, Schubert V, Kumke K, Weibeta O, Klemme S, Nagaki K, Macas J, Gonzalez-Sanchez M, Heredia V, Gomez-Revilla D, Gonzalez-Garcia M, Vega JM, Puertas MJ, Houben A (2012) Nondisjunction in favor of a chromosome: the mechanism of rye B chromosome drive during pollen mitosis. Plant Cell. doi:10.1105/tpc.112.105270

    PubMed Central  PubMed  Google Scholar 

  110. Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting Shugoshin. Nature 455(7210):251–255. doi:10.1038/nature07217

    CAS  PubMed  Google Scholar 

  111. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294(5551):2539–2542

    CAS  PubMed  Google Scholar 

  112. Twell D (2010) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod. doi:10.1007/s00497-010-0157-5

    PubMed  Google Scholar 

  113. Niwa K, Horiuchi G, Hirai Y (1997) Production and characterization of common wheat with B chromosomes of rye from Korea. Hereditas 126(2):139–146

    Google Scholar 

  114. Müntzing A (1970) Chromosomal variation in the Lindström strain of wheat carrying accessory chromosomes in rye. Hereditas 66:279–286

    Google Scholar 

  115. Lindström J (1965) Transfer to wheat of accessory chromosomes from rye. Hereditas 54:149–155

    Google Scholar 

  116. Kishikawa H, Suzuki A (1982) Cytological study on hypo-pentaploid Triticale with four B chromosomes of rye. Jpn J Genet 57:17–24

    Google Scholar 

  117. Puertas MJ, Romera F, Delapena A (1985) Comparison of B-chromosome effects on Secale cereale and Secale vavilovii. Heredity 55 (Oct):229–234

    Google Scholar 

  118. Matthews RB, Jones RN (1983) Dynamics of the B chromosome polymorphism in rye II. Estimates of parameters. Heredity 50:119–137

    Google Scholar 

  119. Romera F, Jimenez MM, Puertas MJ (1991) Factors controlling the dynamics of the B-chromosome polymorphism in Korean rye. Heredity 67:189–195

    Google Scholar 

  120. Rutishauser A, Rothlisberger E (1966) Boosting mechanism of B-chromosomes in Crepis capilaris. Chromosomes Today 1:28–30

    Google Scholar 

  121. Hewitt GM (1976) Meiotic drive for B-chromosomes in the primary oocytes of Myrmeleotettix maculatus (Orthopera: Acrididae). Chromosoma 56(4):381–391

    CAS  PubMed  Google Scholar 

  122. Houben A, Kumke K, Nagaki K, Hause G (2011) CENH3 distribution and differential chromatin modifications during pollen development in rye (Secale cereale L.). Chromosome Res 19(4):471–480. doi:10.1007/s10577-011-9207-6

    CAS  PubMed  Google Scholar 

  123. Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32(4):391–409

    CAS  PubMed  Google Scholar 

  124. Carlson WR (1978) B-chromosome of corn. Annu Rev Genet 12:5–23

    CAS  PubMed  Google Scholar 

  125. Lamb JC, Han F, Auger DL, Birchler J (2006) A trans-acting factor required for non-disjunction of the B chromosome is located distal to the TB-4Lb breakpoint on the B chromosome. Maize Genet Cooper Newsl 80:51–54

    Google Scholar 

  126. Carlson WR (2006) Unstable inheritance of maize B-type chromosomes that lack centric heterochromatin. Genome 49(5):420–431

    CAS  PubMed  Google Scholar 

  127. Han FP, Lamb JC, Yu WC, Gao Z, Birchler JA (2007) Centromere function and nondisjunction are independent components of the maize B chromosome accumulation mechanism. Plant Cell 19(2):524–533. doi:10.1105/tpc.106.049577

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371(6494):215–220. doi:10.1038/371215a0

    CAS  PubMed  Google Scholar 

  129. Mroczek RJ, Melo JR, Luce AC, Hiatt EN, Dawe RK (2006) The maize Ab10 meiotic drive system maps to supernumerary sequences in a large complex haplotype. Genetics 174(1):145–154

    CAS  PubMed  Google Scholar 

  130. Frank SA (2000) Polymorphism of attack and defense. Trends Ecol Evol 15(4):167–171

    PubMed  Google Scholar 

  131. Fishman L, Saunders A (2008) Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322(5907):1559–1562. doi:10.1126/science.1161406

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the DFG Germany (HO 1779/14-1) and the IPK. We would like to thank Juan Pedro M. Camacho (Granada, Spain), Nikolay B. Rubtsov (Novosibirsk, Russia) and Andre Marques (Gatersleben, Germany) for providing photomicrographs.

Author information

Authors and Affiliations

  1. Chromosome Structure and Function Laboratory, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Corrensstrasse 3, 06466, Gatersleben, Germany

    Andreas Houben, Ali Mohammad Banaei-Moghaddam & Sonja Klemme

  2. School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, SA, 5005, Australia

    Jeremy N. Timmis

Authors
  1. Andreas Houben
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Mohammad Banaei-Moghaddam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sonja Klemme
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeremy N. Timmis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Houben.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Houben, A., Banaei-Moghaddam, A.M., Klemme, S. et al. Evolution and biology of supernumerary B chromosomes. Cell. Mol. Life Sci. 71, 467–478 (2014). https://doi.org/10.1007/s00018-013-1437-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-013-1437-7

Keywords

Search

Navigation