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Random BAC FISH of monocot plants reveals differential distribution of repetitive DNA elements in small and large chromosome species

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Abstract

BAC FISH (fluorescence in situ hybridization using bacterial artificial chromosome probes) is a useful cytogenetic technique for physical mapping, chromosome marker screening, and comparative genomics. As a large genomic fragment with repetitive sequences is inserted in each BAC clone, random BAC FISH without adding competitive DNA can unveil complex chromosome organization of the repetitive elements in plants. Here we performed the comparative analysis of the random BAC FISH in monocot plants including species having small chromosomes (rice and asparagus) and those having large chromosomes (hexaploid wheat, onion, and spider lily) in order to understand a whole view of the repetitive element organization in Poales and Asparagales monocots. More unique and less dense dispersed signals of BAC FISH were observed in species with smaller chromosomes in both the Poales and Asparagales species. In the case of large-chromosome species, 75–85% of the BAC clones were detected as dispersed repetitive FISH signals along entire chromosomes. The BAC FISH of Lycoris did not even show localized repetitive patterns (e.g., centromeric localization) of signals.

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Abbreviations

BAC:

Bacterial artificial chromosome

FISH:

Fluorescence in situ hybridization

FITC:

Fluorescein isothiocyanate

PFGE:

Pulsed field gel electrophoresis

References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–218

    Article  CAS  Google Scholar 

  • Bennett MD, Leitch IJ, Price HJ, Johnston JS (2003) Comparisons with Caenorhabditis (approximately 100 Mb) and Drosophila (approximately 175 Mb) using flow cytometry show genome size in Arabidopsis to be approximately 157 Mb and thus approximately 25% larger than the Arabidopsis genome initiative estimate of approximately 125 Mb. Ann Bot 91:547–557

    Article  PubMed  CAS  Google Scholar 

  • Do GS, Seo BB, Yamamoto M, Suzuki G, Mukai Y (2001) Identification and chromosomal location of tandemly repeated DNA sequences in Allium cepa. Genes Genet Syst 76:53–60

    Article  PubMed  CAS  Google Scholar 

  • Do GS, Suzuki G, Mukai Y (2004) Genomic organization of a novel root alliinase gene, ALL1, in onion. Gene 325:17–24

    Article  PubMed  CAS  Google Scholar 

  • Fukui K-N, Suzuki G, Lagudah ES, Rahman S, Appels R, Yamamoto M, Mukai Y (2001) Physical arrangement of retrotransposon-related repeats in centromeric regions of wheat. Plant Cell Physiol 42:189–196

    Article  PubMed  CAS  Google Scholar 

  • Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF (2006) Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res 16:1252–1261

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Schubert I (2003) DNA and proteins of plant centromeres. Curr Opin Plant Biol 6:554–560

    Article  PubMed  CAS  Google Scholar 

  • Hudakova S, Michalek W, Presting GG, ten Hoopen R, dos Santos K, Jasencakova Z, Schubert I (2001) Sequence organization of barley centromeres. Nucleic Acids Res 29:5029–5035

    Article  PubMed  CAS  Google Scholar 

  • International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800

    Article  Google Scholar 

  • Ito T, Suzuki G, Ochiai T, Nakada M, Kameya T, Kanno A (2005) Genomic organization of the AODEF gene in Asparagus officinalis L. Genes Genet Syst 80:95–103

    Article  PubMed  CAS  Google Scholar 

  • Jakse J, Meyer JD, Suzuki G, McCallum J, Cheung F, Town CD, Havey MJ (2008) Pilot sequencing of onion genomic DNA reveals fragments of transposable elements, low gene densities, and significant gene enrichment after methyl filtration. Mol Genet Genomics 280:287–292

    Article  PubMed  CAS  Google Scholar 

  • Jiang J, Gill BS, Wang G-L, Ronald PC, Ward DC (1995) Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491

    Article  PubMed  CAS  Google Scholar 

  • Kuhl JC, Cheung F, Yuan Q, Martin W, Zewdie Y, McCallum J, Catanach A, Rutherford P, Sink KC, Jenderek M, Prince JP, Town CD, Havey MJ (2004) A unique set of 11, 008 onion expressed sequence tags reveals expressed sequence and genomic differences between the monocot orders Asparagales and Poales. Plant Cell 16:114–125

    Article  PubMed  Google Scholar 

  • Kuhl JC, Havey MJ, Martin WJ, Cheung F, Yuan Q, Landherr L, Hu Y, Leebens-Mack J, Town CD, Sink KC (2005) Comparative genomic analyses in Asparagus. Genome 48:1052–1060

    Article  PubMed  CAS  Google Scholar 

  • Kurita S (1986) Variation and evolution in the karyotype of Lycoris, Amaryllidaceae I. General karyomorphological characteristics of the genus. Cytologia 51:803–815

    Article  Google Scholar 

  • Kurita S (1987) Variation and evolution on the karyotype of Lycoris, Amaryllidaceae II. Karyotype analysis of ten taxa among which seven are native in China. Cytologia 52:19–40

    Article  Google Scholar 

  • Lysak M, Fransz P, Schubert I (1998) Cytogenetic analysis of Arabidopsis. In: Salinas J, Sanchez-Serrano JJ (eds) Arabidopsis protocols, 2nd edn. Humana Press, Totowa, pp 173–186

    Google Scholar 

  • Miller JT, Dong F, Jackson SA, Song J, Jiang J (1998) Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics 150:1615–1623

    PubMed  CAS  Google Scholar 

  • Mukai Y, Endo TR, Gill BS (1990) Physical mapping of the 5S rDNA multigene family in common wheat. J Hered 81:290–295

    CAS  Google Scholar 

  • Neumann P, Koblízková A, Navrátilová A, Macas J (2006) Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics 173:1047–1056

    Article  PubMed  CAS  Google Scholar 

  • Pich U, Schubert I (1998) Terminal heterochromatin and alternative telomeric sequences in Allium cepa. Chromosom Res 6:315–321

    Article  CAS  Google Scholar 

  • Pich U, Fuchs J, Schubert I (1996) How do Alliaceae stabilize their chromosome ends in the absence of TTTAGGG sequences? Chromosom Res 4:207–213

    Article  CAS  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269

    Article  PubMed  CAS  Google Scholar 

  • Presting GG, Malysheva L, Fuchs J, Schubert I (1998) A Ty3/gypsy retrotransposon-like sequence localizes to the centromeric regions of cereal chromosomes. Plant J 16:721–728

    Article  PubMed  CAS  Google Scholar 

  • Ramakrishna W, Dubcovsky J, Park YJ, Busso C, Emberton J, SanMiguel P, Bennetzen JL (2002) Different types and rates of genome evolution detected by comparative sequence analysis of orthologous segments from four cereal genomes. Genetics 162:1389–1400

    PubMed  CAS  Google Scholar 

  • SanMiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82:37–44

    Article  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  PubMed  CAS  Google Scholar 

  • 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 10:908–915

    Article  PubMed  CAS  Google Scholar 

  • Suzuki G, Mukai Y (2004) Plant BAC libraries as tools for molecular cytogenetics. In: Williams CR (ed) Focus on genome research. Nova Science, New York, pp 195–210

    Google Scholar 

  • Suzuki G, Watanabe M, Toriyama K, Isogai A, Hinata K (1997) Direct cloning of the Brassica S locus by using a P1-derived artificial chromosome (PAC) vector. Gene 199:133–137

    Article  PubMed  CAS  Google Scholar 

  • Suzuki G, Ura A, Saito N, Do G, So BB, Yamamoto M, Mukai Y (2001) BAC FISH analysis in Allium cepa. Genes Genet Syst 76:251–255

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Li W, Fellers J, Friebe B, Gill BS (2004) BAC-FISH in wheat identifies chromosome landmarks consisting of different types of transposable elements. Chromosoma 112:288–299

    Article  PubMed  CAS  Google Scholar 

  • Zhou S, Bechner MC, Place M, Churas CP, Pape L, Leong SA, Runnheim R, Forrest DK, Goldstein S, Livny M, Schwartz DC (2007) Validation of rice genome sequence by optical mapping. BMC Genomics 8:278

    Article  PubMed  Google Scholar 

  • Zonneveld BJ, Leitch IJ, Bennett MD (2005) First nuclear DNA amounts in more than 300 angiosperms. Ann Bot 96:229–244

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) and the Japan Society for the Promotion of Science (JSPS), KAKENHI (18075003, 20780240, 23113001 and 23113006 to G.S., 20380014 to A.K., 22580004 and 19380194 to Y.M.).

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Author notes

  1. Akie Kikuchi-Taura

    Present address: Department of Cerebrovascular Disease, National Cardiovascular Center, Suita, Osaka, 565-8565, Japan

  2. Asami Tsuru

    Present address: Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, 630-0192, Japan

  3. Takuro Ito

    Present address: Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata, 997-0052, Japan

Authors and Affiliations

  1. Division of Natural Science, Osaka Kyoiku University, 4-698-1 Asahigaoka, Kashiwara, Osaka, 582-8582, Japan

    Go Suzuki, Yuka Ogaki, Nozomi Hokimoto, Lin Xiao, Akie Kikuchi-Taura, Chiaki Harada, Ryozo Okayama, Asami Tsuru, Misa Onishi, Naoko Saito, Geum Sook Do, Sun Hee Lee & Yasuhiko Mukai

  2. Graduate School of Life Sciences, Tohoku University, Sendai, 980-8577, Japan

    Takuro Ito & Akira Kanno

  3. Faculty of Health Sciences for Welfare, Kansai University of Welfare Sciences, Kashiwara, Osaka, 582-0026, Japan

    Maki Yamamoto

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  1. Go Suzuki
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Corresponding author

Correspondence to Go Suzuki.

Additional information

Communicated by K. Toriyama.

Electronic supplementary material

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Online Resource 1

Representative results of PFGE analysis of NotI-digested BAC clones in rice, asparagus, and spider lily (Lycoris). BAC-vector (pBeloBAC11) fragments are indicated by asterisks. Other fragments represent the BAC inserts.

Supplementary material 1 (DOC 347 kb)

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Suzuki, G., Ogaki, Y., Hokimoto, N. et al. Random BAC FISH of monocot plants reveals differential distribution of repetitive DNA elements in small and large chromosome species. Plant Cell Rep 31, 621–628 (2012). https://doi.org/10.1007/s00299-011-1178-8

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  • DOI: https://doi.org/10.1007/s00299-011-1178-8

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