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Rye B chromosomes are weakly transcribed and might alter the transcriptional activity of A chromosome sequences

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Abstract

B chromosomes (Bs) are dispensable components of the genomes of numerous species. To test whether the transcriptome of a host is influenced by Bs, we looked for differences in expression in response to additional Bs. Comparative complementary DNA amplified fragment length polymorphism experiments resulted in the identification of 16 putative B-chromosome-associated transcripts. This comprises 0.7% of the total transcript number and indicates a low activity of Bs. We also provide evidence that B chromosome influences in trans the transcription of A chromosome sequences. The B-specific transcribed sequences B1334, B8149, and B2465 belong to high-copy families with similarity to mobile elements. For all analyzed B-chromosome-derived transcripts, similar A chromosome-encoded sequences were found which supports an A-derived origin of rye B chromosomes.

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References

  • Bachem CWB, vander Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M, Visser RGF (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745–753

    Article  PubMed  CAS  Google Scholar 

  • Bachem CWB, Oomen RJFJ, Visser RGF (1998) Transcript imaging with cDNA-AFLP: a step-by-step protocol. Plant Mol Biol Rep 16:157–173

    Article  CAS  Google Scholar 

  • Bang J-W, Choi HW (1990) Genetic analysis of esterase isozymes in rye (Secale cereale L.). Korean J Genetics 12:87–94

    CAS  Google Scholar 

  • Birchler JA, Riddle NC, Auger DL, Veitia RA (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226

    Article  PubMed  CAS  Google Scholar 

  • Blunden R, Wilkes TJ, Forster JW, Jimenez MM, Sandery MJ, Karp A, Jones RN (1993) Identification of the E3900 family, a 2nd family of rye B chromosome specific repeated sequences. Genome 36:706–711

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Cabrero J, Alche JD, Camacho JPM (1987) Effects of B chromosomes on the activity of nucleolar organizer regions in the grasshopper Eyprepocnemis plorans—activation of a latent nucleolar organizer region on a B chromosome fused to an autosome. Genome 29:116–121

    Google Scholar 

  • Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans 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  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Delgado M, Moraiscecilio L, Neves N, Jones RN, Viegas W (1995) The influence of B chromosomes on rDNA organization in rye interphase nuclei. Chromosome Res 3:487–491

    Article  PubMed  CAS  Google Scholar 

  • Delgado M, Caperta A, Ribeiro T, Viegas W, Jones RN, Morais-Cecilio L (2004) Different numbers of rye B chromosomes induce identical compaction changes in distinct A chromosome domains. Cytogenet Genome Res 106:320–324

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 13:113–122

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Han F, Lamb JC, Yu W, Gao Z, Birchler JA (2007) Centromere function and nondisjunction are independent components of the maize B chromosome accumulation mechanism. Plant Cell 19:524–533

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Kynast RG, Heim U, Hermann H, Jones RN, Forster JW (1996) Molecular cytogenetic characterization of the terminal heterochromatic segment of the B-chromosome of rye (Secale cereale). Chromosoma 105:97–103

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Orford SJ, Timmis JN (2006) In situ hybridization to plant tissues and chromosomes. Methods Mol Biol 326:203–218

    PubMed  CAS  Google Scholar 

  • Ishak B, Jaafar H, Maetz JL, Rumpler Y (1991) Absence of transcriptional activity of the B chromosomes of Apodemus peninsulae during pachytene. Chromosoma 100:278–281

    Article  Google Scholar 

  • Jenkins G, Jones RN (2004) B chromosomes in hybrids of temperate cereals and grasses. Cytogenet Genome Res 106:314–319

    Article  PubMed  CAS  Google Scholar 

  • Jimenez MM, Romera F, Puertas MJ, Jones RN (1994) B chromosomes in inbred lines of rye (Secale cereale L).1. Vigor and fertility. Genetica 92:149–154

    Article  Google Scholar 

  • Jones RN (1995) Tansley review no 85—B chromosomes in plants. New Phytol 131:411–434

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jones RN, Rees H (1982) B chromosomes. London, Academic, p 255

    Google Scholar 

  • Jones RN, Viegas W, Houben A (2008a) A century of B chromosomes in plants: so what? Ann Bot 101:767–775

    Article  PubMed  Google Scholar 

  • Jones RN, Gonzalez-Sanchez M, Gonzalez-Garcia M, Vega JM, Puertas MJ (2008b) Chromosomes with a life of their own. Cytogenet Genome Res 120:265–280

    Article  PubMed  CAS  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. Chromosome Res 15:383–398

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Matzke MA, Aufsatz W, Kanno T, Mette MF, Matzke AJ (2002) Homology-dependent gene silencing and host defense in plants. Adv Genet 46:235–275

    Article  PubMed  CAS  Google Scholar 

  • May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1:e79

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nielsen PS, Kleinhofs A, Olsen OA (1997) Barley elongation factor 1 alpha: genomic organization, DNA sequence, and phylogenetic implications. Genome 40:559–565

    Article  PubMed  CAS  Google Scholar 

  • Ortiz M, Puertas MJ, Jimenez MM, Romera F, Jones RN (1996) B-chromosomes in inbred lines of rye (Secale cereale L). 2. Effects on metaphase I and first pollen mitosis. Genetica 97:65–72

    Article  Google Scholar 

  • Rimpau J, Flavell RB (1975) Characterization of rye B chromosome DNA by DNA–DNA hybridization. Chromosoma 52:207–217

    Article  CAS  Google Scholar 

  • Ruiz-Rejon M, Posse F, Oliver JL (1980) The B-chromosome system of Scilla autumnalis (Liliaceae) - Effects at the isoenzyme level. Chromosoma 79:341–348

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

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

    CAS  Google Scholar 

  • Sanguinetti CJ, Neto ED, Simpson AJG (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Souza ED (2006) Eigenes Protokoll statt DNA-Kit. Protokoll für die Extraktion von DNA aus Blättern. Labor J 7:58

    Google Scholar 

  • 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 113:418–427

    Article  PubMed  CAS  Google Scholar 

  • Teruel M, Cabrero J, Perfectti F, Camacho JP (2007) Nucleolus size variation during meiosis and NOR activity of a B chromosome in the grasshopper Eyprepocnemis plorans. Chromosome Res 15:755–765

    Article  PubMed  CAS  Google Scholar 

  • Timmis JN, Ingle J, Sinclair J, Jones RN (1975) Genomic quality of rye B chromosomes. J Exp Bot 26:367–378

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tsujimoto H, Niwa K (1992) DNA structure of the B chromosome of rye revealed by in situ hybridization using repetitive sequences. Jpn J Genet 67:233–241

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  PubMed  CAS  Google Scholar 

  • Wilkes TM, Francki MG, Langridge P, Karp A, Jones RN, Forster JW (1995) Analysis of rye B chromosome structure using fluorescence in-situ hybridization (FISH). Chromosome Res 3:466–472

    Article  PubMed  CAS  Google Scholar 

  • 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 11:23–35

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are grateful to O. Weiss (IPK, Germany) for excellent technical assistance, as well as R. Pickering and I. Schubert for critically reading the manuscript. We would like to thank M. Puertas (Spain), W. Viegas (Portugal), and R. N. Jones (UK) for providing the valuable plant material. MC and AH were supported by grants of the IPK (Gatersleben) and the DFG (HO1779/10-1).

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Correspondence to Andreas Houben.

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Communicated by L. Comai

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Suppl. Material and Methods

cDNA-amplified fragment length polymorphism (AFLP) analysis and DNA cloning (DOC 29 kb)

Suppl Fig. 1

Southern hybridization of probe B1334 with XbaI-, DraI-, BamHI-, and EcoRI-digested genomic rye DNA from plants with (+B) and without Bs (0B). 1, 2, 3 are the three different rye inbred lines. W—Lindström wheat with (+B) and without Bs (0B). Note identical hybridization patterns of 0B and +B rye and wheat plants with B chromosomes (GIF 238 KB)

High resolution image file (TIFF 7 mb)

Suppl Fig. 2

Southern hybridization of probe rye B2465 with XbaI-, BamHI-, and EcoRI-digested genomic rye DNA from plants with (+B) and without Bs (0B). 1, 2, 3 are the three different rye inbred lines. Note identical hybridization patterns of 0B and +B rye plants (GIF 119 KB)

High resolution image file (TIFF 3.5 mb)

Suppl Fig. 3

Southern hybridization of probe B8149 with XbaI- and DraI-digested genomic rye and wheat DNA from plants with (+B) and without Bs (0B). 1, 2, 3 are three different rye inbred lines. W—Lindström wheat with (+B) and without Bs (0B). Note the highly polymorphic hybridization pattern. Additional B-specific restriction bands are arrowed (GIF 145 KB)

High resolution image file (TIFF 3.4 mb)

Suppl. Fig. 4a

Alignment of B1334-like sequences amplified from cDNA of plants with (+B) and without (0B) B chromosomes. Single-nucleotide polymorphisms are highlighted in red. GenBank sequence AF175285 shows the highest similarity. Sequences B1334-1–9 are sequences obtained via cDNA-AFLP and sequences B1334-10–23 are sequences obtained via RT-PCR (DOC 48.5 kb)

Suppl. Fig. 4b

Alignment of B8149-like sequences amplified from cDNA of plants with (+B) and without (0B) B chromosomes. Single-nucleotide polymorphisms are highlighted in red. Sequences B8149-1–24 are sequences obtained by RT-PCR (DOC 63 kb)

Suppl. Table 1

PCR primers used (DOC 45 kb)

Suppl. Table 2

AFLP adaptor sequences (DOC 26 kb)

Suppl. Table 3

List of AFLP primer sequences (Keygene). Selective nucleotides are highlighted in red. http://wheat.pw.usda.gov/ggpages/keygeneAFLPs.html (DOC 40 kb)

Suppl. Table 4

Primer combinations used for cDNA-AFLP analysis of 0B/+B plants. (DOC 73 kb)

Suppl. Table 5

Total number of cDNA-AFLP bands and of additional bands present in 0B- or +B-positive plants only. *weak, **middle, ***strong intensity of band (DOC 137 kb)

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Carchilan, M., Kumke, K., Mikolajewski, S. et al. Rye B chromosomes are weakly transcribed and might alter the transcriptional activity of A chromosome sequences. Chromosoma 118, 607–616 (2009). https://doi.org/10.1007/s00412-009-0222-8

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