Repetitive part of the banana (Musa acuminata) genome investigated by low-depth 454 sequencing
Language English Country England, Great Britain Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
20846365
PubMed Central
PMC2956553
DOI
10.1186/1471-2229-10-204
PII: 1471-2229-10-204
Knihovny.cz E-resources
- MeSH
- Musa genetics MeSH
- DNA, Plant genetics MeSH
- Genome, Plant * MeSH
- Microsatellite Repeats * MeSH
- Retroelements * MeSH
- Sequence Analysis, DNA MeSH
- DNA Transposable Elements * MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Plant MeSH
- Retroelements * MeSH
- DNA Transposable Elements * MeSH
BACKGROUND: Bananas and plantains (Musa spp.) are grown in more than a hundred tropical and subtropical countries and provide staple food for hundreds of millions of people. They are seed-sterile crops propagated clonally and this makes them vulnerable to a rapid spread of devastating diseases and at the same time hampers breeding improved cultivars. Although the socio-economic importance of bananas and plantains cannot be overestimated, they remain outside the focus of major research programs. This slows down the study of nuclear genome and the development of molecular tools to facilitate banana improvement. RESULTS: In this work, we report on the first thorough characterization of the repeat component of the banana (M. acuminata cv. 'Calcutta 4') genome. Analysis of almost 100 Mb of sequence data (0.15× genome coverage) permitted partial sequence reconstruction and characterization of repetitive DNA, making up about 30% of the genome. The results showed that the banana repeats are predominantly made of various types of Ty1/copia and Ty3/gypsy retroelements representing 16 and 7% of the genome respectively. On the other hand, DNA transposons were found to be rare. In addition to new families of transposable elements, two new satellite repeats were discovered and found useful as cytogenetic markers. To help in banana sequence annotation, a specific Musa repeat database was created, and its utility was demonstrated by analyzing the repeat composition of 62 genomic BAC clones. CONCLUSION: A low-depth 454 sequencing of banana nuclear genome provided the largest amount of DNA sequence data available until now for Musa and permitted reconstruction of most of the major types of DNA repeats. The information obtained in this study improves the knowledge of the long-range organization of banana chromosomes, and provides sequence resources needed for repeat masking and annotation during the Musa genome sequencing project. It also provides sequence data for isolation of DNA markers to be used in genetic diversity studies and in marker-assisted selection.
See more in PubMed
Food and Agriculture Organization (FAO) http://faostat.fao.org/
Simonds NW, Shepherd K. The taxonomy and origins of the cultivated bananas. J Linn Soc Bot. 1955;55:302–312. doi: 10.1111/j.1095-8339.1955.tb00015.x. DOI
Doležel J, Doleželová M, Novák FJ. Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata and M. balbisiana) Biol Plantarum. 1994;36:351–357. doi: 10.1007/BF02920930. DOI
Bartoš J, Alkhimova O, Doleželová M, De Langhe E, Doležel J. Nuclear genome size and genomic distribution of ribosomal DNA in Musa and Ensete (Musaceae): taxonomic implications. Cytogenet Genome Res. 2005;109:50–57. doi: 10.1159/000082381. PubMed DOI
Hřibová E, Doleželová M, Town CD, Macas J, Doležel J. Isolation and characterization of the highly repeated fraction of the banana genome. Cytogenet Genome Res. 2007;119:268–274. doi: 10.1159/000112073. PubMed DOI
Valárik M, Šimková H, Hřibová E, Safář J, Doleželová M, Doležel J. Isolation, characterization and chromosome localization of repetitive DNA sequences in bananas (Musa spp.) Chromosome Res. 2002;10:89–100. doi: 10.1023/A:1014945730035. PubMed DOI
Baurens FC, Noyer JL, Lanaud C, Lagoda PJL. A repetitive sequence family of banana (Musa sp.) shows homology to Copia-like elements. J Genet Breed. 1997;51:135–142.
Teo CH, Tan SH, Othman YR, Schwarzacher T. The cloning of Ty 1 -copia -like retrotransposons from 10 varieties of banana (Musa Sp.) J Biochem Mol Biol Biophys. 2002;6:193–201. doi: 10.1080/10258140290022329. PubMed DOI
Baurens FC, Noyer JL, Lanaud C, Lagoda PJL. Use of competitive PCR to essay copy number of repetitive elements in banana. Mol Gen Genet. 1996;253:57–64. doi: 10.1007/s004380050296. PubMed DOI
Baurens FC, Noyer JL, Lanaud C, Lagoda PJL. Assessment of a species-specific element (Brep 1) in banana. Theor Appl Genet. 1997;95:922–931. doi: 10.1007/s001220050643. DOI
Balint-Kurti PJ, Clendennen SK, Doleželová M, Valárik M, Doležel J, Beetham PR, May GD. Identification and chromosomal localization of the monkey retrotransposon in Musa sp. Mol Gen Genet. 2000;263:908–915. doi: 10.1007/s004380000265. PubMed DOI
Cheung F, Town CD. A BAC end view of the Musa acuminata genome. BMC Plant Biol. 2007;7:29. doi: 10.1186/1471-2229-7-29. PubMed DOI PMC
Global Musa Genomics Consortium (GMGC) http://www.musagenomics.org/
Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu PG, Begley RF, Rothberg JM. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005;473:376–380. PubMed PMC
Macas J, Neumann P, Navrátilová A. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics. 2007;8:427. doi: 10.1186/1471-2164-8-427. PubMed DOI PMC
Swaminathan K, Varala K, Hudson ME. Global repeat discovery and estimation of genomic copy number in a large, complex genome using a high-throughput 454 sequence survey. BMC Genomics. 2007;8:132. doi: 10.1186/1471-2164-8-132. PubMed DOI PMC
Aert R, Sagi L, Volckaer G. Gene content and density in banana (Musa acuminata) as revealed by genomic sequencing of BAC clones. Theor Appl Genet. 2004;109:129–139. doi: 10.1007/s00122-004-1603-2. PubMed DOI
Azhar M, Heslop-Harrison JS. Genomes, diversity and resistance gene analogues in Musa species. Cytogenet Genome Res. 2008;121:59–66. doi: 10.1159/000124383. PubMed DOI
Vilarinhos AD, Piffanelli P, Lagoda P, Thibivilliers S, Sabau X, Carreel F, DHont A. Construction and characterization of a bacterial artificial chromosome library of banana (Musa acuminata Colla) Theor Appl Genet. 2003;106:1102–1106. PubMed
Pillay M, Ssebuliba R, Hartman J, Vuylsteke D, Talengera D, Tushemereirwe W. Conventional breeding strategies to enhance the sustainability of Musa biodiversity conservation for endemic cultivars. African Crop Science Journal. 2004;12:59–65.
Moens T, Sandoval Fernandez JA, Escalant JV, De Waele D. Evaluation of the progeny from a cross between 'Pisang Berlin' and M. acuminata spp. burmannicoides 'Calcutta 4' for evidence of segregation with respect to resistance to black leaf streak disease and nematodes. Infomusa. 2002;11:20–22.
Bartoš J, Paux E, Kofler R, Havránková M, Kopecký D, Suchánková P, Šafář J, Šimková H, Town CD, Lelley T, Feuillet C, Doležel J. A first survey of the rye (Secale cereale) genome composition through BAC end sequencing of the short arm of chromosome 1R. BMC Plant Biol. 2008;8:95. doi: 10.1186/1471-2229-8-95. PubMed DOI PMC
International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature. 2005;436:793–800. doi: 10.1038/nature03895. PubMed DOI
Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao QZ, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R. High quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS ONE. 2007;2(12):e1326. doi: 10.1371/journal.pone.0001326. PubMed DOI PMC
Marin I, Llorens C. Ty3/Gypsy retrotransposons: Description of a new Arabidopsis thaliana elements and evolutionary perspectives derived from comparative genomics data. Mol Biol Evol. 2000;17:1040–1049. PubMed
Havecker ER, Gao X, Voytas DF. The Sireviruses, a plant-specific lineage of the Ty1/copia retrotransposons, interact with a family of proteins related to dynein light chain 8. Plant Physiol. 2005;139:857–868. doi: 10.1104/pp.105.065680. PubMed DOI PMC
Wicker T, Keller B. Genome-wide comparative analysis of copia retrotransposon in triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res. 2007;17:1072–1081. doi: 10.1101/gr.6214107. PubMed DOI PMC
Grandbastien M-A, Spielmann A, Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989;337:376–380. doi: 10.1038/337376a0. PubMed DOI
White SE, Habera LF, Wessler SR. Retrotransposons in the flanking region of normal plant genes: A role for copia-like elements in the evolution of gene structure and expression. Proc Natl Acad Sci USA. 1994;91:11792–11796. doi: 10.1073/pnas.91.25.11792. PubMed DOI PMC
Gorinsek B, Gubensek F, Kordis D. Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol. 2004;21:781–798. doi: 10.1093/molbev/msh057. PubMed DOI
Kordis D. A genomic perspective on the chromodomain-containing retrotransposons: Chromoviruses. Gene. 2005;347:161–173. doi: 10.1016/j.gene.2004.12.017. PubMed DOI
Llorens C, Fares MA, Moya A. Relationships of gag-pol diversity between Ty3/Gypsy and Retroviridae LTR retroelements and the three kings hypothesis. BMC Evol Biol. 2008;8:276. doi: 10.1186/1471-2148-8-276. PubMed DOI PMC
Schmidt T. LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol Biol. 1999;40:903–910. doi: 10.1023/A:1006212929794. PubMed DOI
Rubin E, Lithwick G, Levy AA. Structure and evolution of the hAT transposon superfamily. Genetics. 2001;158:949–957. PubMed PMC
Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR, Yu Y, Wei F, Fuks G, Soderlund CA, Mayer KF, Wing RA. Sequence composition and genome organization of maize. Proc Natl Acad Sci USA. 2004;101:14349–14354. doi: 10.1073/pnas.0406163101. PubMed DOI PMC
Raap AK, Florijn RJ, Blonden LJ, Wiegant J, Vaandrager JW, Vrolijk H, den Dunnen J, Tanke HJ, Ommen GJ. Fiber FISH as a DNA mapping tool. Methods. 1996;9:67–73. doi: 10.1006/meth.1996.0009. PubMed DOI
Pedersen C, Linde-Laursen I. The relationship between physical and genetic distances at the Hor1 and Hor2 loci of barley estimated by two-colour fluorescent in situ hybridization. Theor Appl Genet. 1995;91:941–946. doi: 10.1007/BF00223904. PubMed DOI
Teo CH, Schwarzacher T. Tandem repeats and Musa chromosome organisation. Unpublished. GenBank code: AM909712 - AM909714.
Galasso I, Schmidt T, Pignone D, Heslop-Harrison JS. The molecular cytogenetics of Vigna unguiculata (L.) Walp: the physical organization and characterization of 18s-5.8s-25s rRNA genes, 5s rRNA genes, telomere-like sequences, and a family of centromeric repetitive DNA sequences. Theor Appl Genet. 1995;91:928–935. doi: 10.1007/BF00223902. PubMed DOI
Han YH, Zhang ZH, Liu JH, Lu JY, Huang SW, Jin WW. Distribution of the tandem repeat sequences and karyotyping in cucumber (Cucumis sativus L.) by fluorescence in situ hybridization. Cytogenet Genome Res. 2008;122:80–88. doi: 10.1159/000151320. PubMed DOI
Jiang J, Birchler JA, Parrott WA, Dawe RK. A molecular view of plant centromeres. Trends Plant Sci. 2003;8:570–574. doi: 10.1016/j.tplants.2003.10.011. PubMed DOI
Nagaki K, Tsujimoto H, Sasakuma T. A novel repetitive sequence of sugar cane, SCEN family, locating on centromeric regions. Chromosome Res. 1998;6:295–302. doi: 10.1023/A:1009270824142. PubMed DOI
Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C. Characterizing the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J. 2006;48:463–747. doi: 10.1111/j.1365-313X.2006.02891.x. PubMed DOI
Laboratory of Molecular Cytogenetics and Cytomnetry (IEB, Czech Republic) http://olomouc.ueb.cas.cz/banana-sequencing-data
Macas J, Pech J, Novák P. PROFREP: a web server for repeat detection in genomic sequences based on 454 sequencing data. http://w3lamc.umbr.cas.cz/profrep/public/
Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA. Preparation of megabase-size DNA from plant nuclei. Plant J. 1995;7:175–184. doi: 10.1046/j.1365-313X.1995.07010175.x. DOI
Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J. TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics. 2003;19:651–652. doi: 10.1093/bioinformatics/btg034. PubMed DOI
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC
Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 2003;31:383–387. doi: 10.1093/nar/gkg087. PubMed DOI PMC
Sonnhammer ELL, Durbin R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene. 1995;167:GC1–GC10. doi: 10.1016/0378-1119(95)00714-8. PubMed DOI
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. PubMed DOI PMC
Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27:573–580. doi: 10.1093/nar/27.2.573. PubMed DOI PMC
Sobreira TJP, Durham AM, Gruber A. TRAP:automated classification, quantification and annotation of tandemly repeated sequences. Bioinformatics. 2006;22:361–362. doi: 10.1093/bioinformatics/bti809. PubMed DOI
Paux E, Faure S, Choulet F, Roger D, Gauthier V, Martinant JP, Sourdille P, Balfourier F, Le Paslier M-C, Chauveau A, Cakir M, Gandon B, Feuillet C. Insertion site-based polymorphism markers open new perspectives for genome saturation and marker-assisted selection in wheat. Plant Biotechnol J. 2010;8:196–210. doi: 10.1111/j.1467-7652.2009.00477.x. PubMed DOI
Staden R. The Staden sequence analysis package. Mol Biotechnol. 1996;5:233–241. doi: 10.1007/BF02900361. PubMed DOI
Doleželová M, Valárik M, Swennen R, Horry JP, Doležel J. Physical mapping of the 18S-25S and 5S ribosomal RNA genes in diploid bananas. Biol Plantarum. 1998;41:497–505. doi: 10.1023/A:1001880030275. DOI
Advances in the Molecular Cytogenetics of Bananas, Family Musaceae
TE-greedy-nester: structure-based detection of LTR retrotransposons and their nesting
Molecular and Cytogenetic Study of East African Highland Banana
Genome-wide analysis of repeat diversity across the family Musaceae
Molecular analysis and genomic organization of major DNA satellites in banana (Musa spp.)
Plant centromeric retrotransposons: a structural and cytogenetic perspective