Skip to main content
Log in

Gene content and density in banana (Musa acuminata) as revealed by genomic sequencing of BAC clones

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

The complete sequence of Musa acuminata bacterial artificial chromosome (BAC) clones is presented and, consequently, the first analysis of the banana genome organization. One clone (MuH9) is 82,723 bp long with an overall G+C content of 38.2%. Twelve putative protein-coding sequences were identified, representing a gene density of one per 6.9 kb, which is slightly less than that previously reported for Arabidopsis but similar to rice. One coding sequence was identified as a partial M. acuminata malate synthase, while the remaining sequences showed a similarity to predicted or hypothetical proteins identified in genome sequence data. A second BAC clone (MuG9) is 73,268 bp long with an overall G+C content of 38.5%. Only seven putative coding regions were discovered, representing a gene density of only one gene per 10.5 kb, which is strikingly lower than that of the first BAC. One coding sequence showed significant homology to the soybean ribonucleotide reductase (large subunit). A transition point between coding regions and repeated sequences was found at approximately 45 kb, separating the coding upstream BAC end from its downstream end that mainly contained transposon-like sequences and regions similar to known repetitive sequences of M. acuminata. This gene organization resembles Gramineae genome sequences, where genes are clustered in gene-rich regions separated by gene-poor DNA containing abundant transposons.

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

Access this article

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
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    PubMed  Google Scholar 

  • Balint-Kurti PJ, Clendennen SK, Doleželová M, Valárik M, Doležel J, Beetham PR, May GD (2000) Identification and chromosomal localization of the monkey retrotransposon in Musa sp. Mol Gen Genet 263:908–915

    Article  CAS  PubMed  Google Scholar 

  • Barakat A, Carels N, Bernardi G (1997) The distribution of genes in the genomes of Gramineae. Proc Natl Acad Sci USA 94:6857–6861

    CAS  PubMed  Google Scholar 

  • Barakat A, Matassi G, Bernardi G (1998) Distribution of genes in the genome of Arabidopsis thaliana and its implications for the genome organization in plants. Proc Natl Acad Sci USA 95:10044–10049

    Article  CAS  PubMed  Google Scholar 

  • Baurens FC, Noyer JL, Lanaud C, Lagoda P (1997) Copia-like elements in banana. J Genet Breed 51:135–142

    CAS  Google Scholar 

  • Becraft PW (1998) Receptor kinases in plant development. Trends Plant Sci 3:384–388

    Article  Google Scholar 

  • Bevan M, Mayer K, White O, Eisen J, Preuss D, Bureau T, Salzberg S, Mewes H-M (2001) Sequence and analysis of the Arabidopsis genome. Curr Opin Plant Biol 4:105–110

    Article  CAS  PubMed  Google Scholar 

  • Bodenteich A, Chissoe S, Wang YF, Roe BA (1993) Shot-gun cloning as the strategy of choice to generate templates for high-throughput dideoxynucleotide sequencing. In: Venter JC (ed) Automated DNA sequencing and analysis techniques, Academic Press, London, pp 42–50

  • Brooks SA, Huang L, Gill BS, Fellers JP (2002) Analysis of 106 kb of contiguous DNA sequence from the D genome of wheat reveals high gene density and a complex arrangement of genes related to disease resistance. Genome 45:963–972

    Article  CAS  PubMed  Google Scholar 

  • Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268:78–94

    Article  CAS  PubMed  Google Scholar 

  • Denham TP, Haberle SG, Lentfer C, Fullagar R, Field J, Therin M, Porch N, Winsborough B (2003) Origins of agriculture at Kuk Swamp in the highlands of New Guinea. Science 301:189–193

    Article  CAS  PubMed  Google Scholar 

  • Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, Jia P, Zhang Y, Zhao Q, Ying K, Yu S, Tang Y, Weng Q, Zhang L, Lu Y, Mu J, Lu Y, Zhang LS, Yu Z, Fan D, Liu X, Lu T, Li C, Wu Y, Sun T, Lei H, Li T, Yin HH, Cai Z, Ren S, Lu G, Gu W, Zhu G, Tu Y, Jia J, Zhang Y, Chen J, Kang H, Chen X, Shao C, Sun Y, Hu Q, Zhang X, Zhang W, Wang L, Ding C, Sheng H, Gu J, Chen S, Ni L, Zhu F, Chen W, Lan L, Lai Y, Cheng Z, Gu M, Jiang J, Li J, Hong G, Xue Y, Han B (2002) Sequence and analysis of rice chromosome 4. Nature 420:316–319

    Article  CAS  PubMed  Google Scholar 

  • Fu HH, Park WK, Yan XH, Zheng ZW, Shen BZ, Dooner HK (2001) The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome. Proc Natl Acad Sci USA 98:8903–8908

    CAS  PubMed  Google Scholar 

  • Gewolb J (2001) DNA sequencers to go Banana’s? Science 293:585–586

    CAS  PubMed  Google Scholar 

  • Gish W, States DJ (1993) Identification of protein coding regions by database similarity search. Nat Genet 3:266–272

    CAS  PubMed  Google Scholar 

  • Gowen S (1995) Bananas and Plantains. Chapman and Hall, London

  • Harper G, Osuji JO, Heslop-Harrison JS, Hull R (1999) Integration of banana streak badnavirus into the Musa genome: molecular and cytogenetic evidence. Virology 255:207–213

    CAS  PubMed  Google Scholar 

  • Huang AHC, Trelease RN, Moore TS (1983) Plant peroxisomes. Academic Press, New York

  • Jentoft JE, Katz RA (1989) What is the role of the cys-his motif in retroviral nucleocapsid (NC) proteins? Bioessays 11:176–181

    PubMed  Google Scholar 

  • Jurka J (2000) Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 9:418–420

    Article  Google Scholar 

  • Jurka J, Klonowski P, Dagman V, Pelton P (1996) censor— a program for identification and elimination of repetitive elements from DNA sequences. Comput Chem 20:119–122

    CAS  PubMed  Google Scholar 

  • Keller B, Feuillet C (2000) Colinearity and gene density in grasses. Trends Plant Sci 5:246–251

    CAS  PubMed  Google Scholar 

  • Liu H, Sachidanandam R, Stein L (2001) Comparative genomics between rice and Arabidopsis shows scant co linearity in gene order. Genome Res 11:2020–2026

    Article  CAS  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) trnascan-se: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    CAS  PubMed  Google Scholar 

  • Lukashin AV, Borodovsky M (1998) genemark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115

    CAS  PubMed  Google Scholar 

  • Lysák M, Doleželova M, Horry JP, Swennen R, Doležel J (1999) Flow cytometric analysis of nuclear DNA content in Musa. Theor Appl Genet 98:1344–1350

    Article  CAS  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    CAS  PubMed  Google Scholar 

  • Mulder NJ, Apweiler R, Attwood TK, Bairoch A, Barrell D, Bateman A, Binns D, Biswas M, Bradley P, Bork P, Bucher P, Copley RR, Courcelle E, Das U, Durbin R, Falquet L, Fleischmann W, Griffiths-Jones S, Haft D, Harte N, Hulo N, Kahn D, Kanapin A, Krestyaninova M, Lopez R, Letunic I, Lonsdale D, Silventoinen V, Orchard SE, Pagni M, Peyruc D, Ponting CP, Selengut JD, Servant F, Sigrist CJA, Vaughan R, Zdobnov EM (2003) The interpro database 2003 brings increased coverage and new features. Nucleic Acids Res 31:315–318

    Article  CAS  PubMed  Google Scholar 

  • Ndowora T, Dahal G, LaFleur D, Harper G, Hull R, Olszewski NE, Lockhart B (1999) Evidence that badnavirus infection in Musa can originate from integrated pararetroviral sequences. Virology 255:214–220

    CAS  PubMed  Google Scholar 

  • Parniske M, Hammond-Kosack KE, Golstein C, Thomas CM, Jones DA, Harrison K, Wulff BBH, Jones JDG (1997) Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91:821–832

    CAS  PubMed  Google Scholar 

  • Pua EC, Chandramouli S, Han P, Liu P (2003) Malate synthase gene expression during fruit ripening of Cavendish banana (Musa acuminata cv. Williams). J Exp Bot 54:309–316

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna W, Emberton J, SanMiguel P, Ogden M, Llaca V, Messing J, Bennetzen JL (2002) Comparative sequence analysis of the sorghum rph region and the maize rp1 resistance gene complex. Plant Physiol 130:1728–1738

    Article  CAS  PubMed  Google Scholar 

  • Reichard P (1988) Interactions between deoxyribonucleotide and DNA synthesis. Annu Rev Biochem 57:349–374

    CAS  PubMed  Google Scholar 

  • Robinson JC (1996) Bananas and plantains. CAB Int, Wallingford

  • Roe BA, Crabtree JS, Khan AS (1996) DNA isolation and sequencing. John Wiley and Sons, New York

  • Salamov A, Solovyev V (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res10:516–522

    Google Scholar 

  • Salse J, Piegu B, Cooke R, Delseny M (2002) Synteny between Arabidopsis thaliana and rice at the genome level: a tool to identify conservation in the ongoing rice genome sequencing project. Nucleic Acids Res 30:2316–2328

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Matsumoto T, Yamamoto K, Sakata K, Baba T, Katayose Y, Wu J, Niimura Y, Cheng Z, Nagamura Y, Antonio BA, Kanamori H, Hosokawa S, Masukawa M, Arikawa K, Chiden Y, Hayashi M, Okamoto M, Ando T, Aoki H, Arita K, Hamada M, Harada C, Hijishita S, Honda M, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, Ito S, Ito T, Ito Y, Ito Y, Iwabuchi A, Kamiya K, Karasawa W, Katagiri S, Kikuta A, Kobayashi N, Kono I, Machita K, Maehara T, Mizuno H, Mizubayashi T, Mukai Y, Nagasaki H, Nakashima M, Nakama Y, Nakamichi Y, Nakamura M, Namiki N, Negishi M, Ohta I, Ono N, Saji S, Sakai K, Shibata M, Shimokawa T, Shomura A, Song J, Takazaki Y, Terasawa K, Tsuji K, Waki K, Yamagata H, Yamane H, Yoshiki S, Yoshihara R, Yukawa K, Zhong H, Iwama H, Endo T, Ito H, Ho Hahn J, Kim HI, Eun MY, Yano M, Jiang J, Gojobori T (2002) The genome sequence and structure of rice chromosome 1. Nature 420:312–315

    Article  CAS  PubMed  Google Scholar 

  • Sauge-Merle S, Falcone S, Fontecave M (1999) An active ribonucleotide reductase from Arabidopsis thaliana. Eur J Biochem 266:62–69

    Article  CAS  PubMed  Google Scholar 

  • Simmonds NW (1966) Bananas, 2nd edn. Longmans, London

  • Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, Van der Lee T, Bleeker M, Onstenk J, de Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P (1998) Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068

    CAS  Google Scholar 

  • Teo CH, Tan SH, Othman YR, Schwarzacher T (2002) The cloning of Ty1-copia-like retrotransposons from 10 varieties of banana (Musa sp.). J Biochem Mol Biol Biophys 6:193–201

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • The Rice Chromosome 10 Sequencing Consortium (2003) In-depth view of structure, activity and evolution of rice chromosome 10. Science 300:1566–1569

    Article  PubMed  Google Scholar 

  • Valárik M, Simková H, Hribová E, Safár J, Doleželová M, Doležel J (2002) Isolation, characterization and chromosome localization of repetitive DNA sequences in banana (Musa spp.). Chromos Res 10:89–100

    Article  Google Scholar 

  • Walbot V, Petrov DA (2001) Gene galaxies in the maize genome. Proc Natl Acad Sci USA 98:8163–8164

    Article  CAS  PubMed  Google Scholar 

  • Walker-Simmons MK (1998) Protein kinases in seeds. Seed Sci Res 8:193–200

    CAS  Google Scholar 

  • Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394

    CAS  PubMed  Google Scholar 

  • Yada T, Takagi T, Totoki Y, Sakaki Y, Takaeda Y (2003) digit: a novel gene finding program by combining gene-finders. Pac Symp Biocomput 2003:375–387

    Google Scholar 

  • Yu J, Hu S, Wang J, Wong G, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M, Liu J, Sun J, Tang J, Chen Y, Huang X, Lin W, Ye C, Tong W, Cong L, Geng J, Han Y, Li L, Li W, Hu G, Huang X, Li W, Li J, Liu Z, Li L, Liu J, Qi Q, Liu J, Li L, Li T, Wang X, Lu H, Wu T, Zhu M, Ni P, Han H, Dong W, Ren X, Feng X, Cui P, Li X, Wang H, Xu X, Zhai W, Xu Z, Zhang J, He S, Zhang J, Xu J, Zhang K, Zheng X, Dong J, Zeng W, Tao L, Ye J, Tan J, Ren X, Chen X, He J, Liu D, Tian W, Tian C, Xia H, Bao Q, Li G, Gao H, Cao T, Wang J, Zhao W, Li P, Chen W, Wang X, Zhang Y, Hu J, Wang J, Liu S, Yang J, Zhang G, Xiong Y, Li Z, Mao L, Zhou C, Zhu Z, Chen R, Hao B, Zheng W, Chen S, Guo W, Li G, Liu S, Tao M, Wang J, Zhu L, Yuan L, Yang H (2002) A draft sequence of the Rice genome (Oryza sativa L. ssp indica). Science 296:79–92

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Jaroslav Dolezel (Institute of Experimental Botany, Olomouc, Czech Republic) for providing a set of 96 BAC clones for this study and to Phillip SanMiguel (Purdue University, West Lafayette, USA) for initial help with retroelement analysis. Access to the Syngenta Musa EST database maintained at MIPS (Munich, Germany) is acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Aert.

Additional information

Communicated by J.S. Heslop-Harrison

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aert, R., Sági, L. & Volckaert, G. Gene content and density in banana (Musa acuminata) as revealed by genomic sequencing of BAC clones. Theor Appl Genet 109, 129–139 (2004). https://doi.org/10.1007/s00122-004-1603-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1603-2

Keywords

Navigation