Satellite DNA sequences consist of tandemly arranged repetitive units up to thousands nucleotides long in head-to-tail orientation. The evolutionary processes by which satellites arise and evolve include unequal crossing over, gene conversion, transposition and extra chromosomal circular DNA formation. Large blocks of satellite DNA are often observed in heterochromatic regions of chromosomes and are a typical component of centromeric and telomeric regions. Satellite-rich loci may show specific banding patterns and facilitate chromosome identification and analysis of structural chromosome changes. Unlike many other genomes, nuclear genomes of banana (Musa spp.) are poor in satellite DNA and the information on this class of DNA remains limited. The banana cultivars are seed sterile clones originating mostly from natural intra-specific crosses within M. acuminata (A genome) and inter-specific crosses between M. acuminata and M. balbisiana (B genome). Previous studies revealed the closely related nature of the A and B genomes, including similarities in repetitive DNA. In this study we focused on two main banana DNA satellites, which were previously identified in silico. Their genomic organization and molecular diversity was analyzed in a set of nineteen Musa accessions, including representatives of A, B and S (M. schizocarpa) genomes and their inter-specific hybrids. The two DNA satellites showed a high level of sequence conservation within, and a high homology between Musa species. FISH with probes for the satellite DNA sequences, rRNA genes and a single-copy BAC clone 2G17 resulted in characteristic chromosome banding patterns in M. acuminata and M. balbisiana which may aid in determining genomic constitution in interspecific hybrids. In addition to improving the knowledge on Musa satellite DNA, our study increases the number of cytogenetic markers and the number of individual chromosomes, which can be identified in Musa.

Institute of Experimental Botany Centre of the Region Haná for Biotechnological and Agricultural Research Olomouc Czech Republic

Zobrazit více v PubMed

Bennetzen JL, Kellog EA (1997) Do plants have a one-way ticket to genomic obesity? Plant Cell 9: 1509–1514. PubMed PMC

Ingham LD, Hanna WW, Baier JW, Hannah LC (1993) Origin of the main class of repetitive DNA within selected Pennisetum species. Mol Gen Genet 238: 350–356. PubMed

Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev 80: 227–250. PubMed

Kubis S, Schmidt T, Heslop-Harrison JS (1998) Repetitive DNA elements as a major component of plant genomes. Ann Bot 82: 45–55.

Charlesworth B, Sniegowski PE, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 37: 215–220. PubMed

Elder JF Jr, Turner BJ (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 70: 297–320. PubMed

Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, et al. (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14: 1691–1704. PubMed PMC

Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5: 435–445. PubMed

Tek AL, Jiang J (2004) The centromere regions of potato chromosomes contain megabase-sized tandem arrays of telomere-similar sequence. Chromosoma 113: 77–83. PubMed

Macas J, Požárková D, Navrátilová A, Nouzová M, Neumann P (2000) Two new families of tandem repeats isolated from genus Vicia using genomic self-priming PCR. Mol Gen Genet 263: 741–751. PubMed

Willard HF (1991) Evolution of alpha satellite. Curr Opin Genet Dev 1: 509–514. PubMed

Navrátilová A, Koblížková A, Macas J (2008) Survey of extrachromosomal circular DNA derived from plant satellite repeats. BMC Plant Biol 8: 90. PubMed PMC

Hřibová E, Neumann P, Matsumoto T, Roux N, Macas J, et al. (2010) Repetitive part of the banana (Musa acuminata) genome investigated by low-depth 454 sequencing. BMC Plant Biol 10: 204. PubMed PMC

Macas J, Neumann P, Navrátilová A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula . BMC Genomics 8: 427. PubMed PMC

Macas J, Kejnovský E, Neumann P, Novák P, Koblížková A, et al. (2011) Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silene latifolia . PLoS One 6: e27335. PubMed PMC

Schmidt T, Heslop-Harrison JS (1998) Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends Plant Sci 3: 195–199.

Zatloukalová P, Hřibová E, Kubaláková M, Suchánková P, Šimková H, et al. (2011) Integration of genetic and physical maps of chickpea (Cicer arietinum L.) genome using flow-sorted chromosomes. Chromosome Res 19: 729–739. PubMed

Han YH, Zhang ZH, Liu JH, Lu JY, Huang SW, et al. (2008) Distribution of the tandem repeat sequences and karyotyping in cucumber (Cucumis sativus L.) by fluorescence in situ hybridization. Cytogenet Genome Res 122: 80–88. PubMed

Macas J, Navrátilová A, Koblížková A (2006) Sequence homogenization and chromosomal localization of VicTR-B satellites differ between closely related Vicia species. Chromosoma 115: 437–447. PubMed

Navrátilová A, Neumann P, Macas J (2003) Karyotype analysis of four Vicia species using in situ hybridization with repetitive sequences. Ann Bot 91: 921–926. PubMed PMC

Sharma S, Raina SN (2005) Organization and evolution of highly repeated satellite DNA in plant chromosomes. Cytogenet Genome Res. 109: 15–26. PubMed

Kopecký D, Havránková M, Loureiro J, Castro S, Lukaszewski AJ, et al. (2010) Physical distribution of homoeologous recombination in individual chromosomes of Festuca pratensis in Lolium multiflorum. Cytogenet Genome Res. 120: 370–383. PubMed

Kopecký D, Lukaszewski AJ, Doležel J (2008) Cytogenetics of Festulolium (Festuca×Lolium hybrids). Cytogenet Genome Res. 120: 370–383. PubMed

Simmonds NW, Shepherd K (1955) The taxonomy and origins of the cultivated bananas. J Linn Soc Bot 55: 302–312.

Bartoš J, Alkhimova O, Doleželová M, De Langhe E, Doležel J (2005) Nuclear genome size and genomic distribution of ribosomal DNA in Musa and Ensete (Musaceae): taxonomic implications. Cytogenet Genome Res 109: 50–57. PubMed

Doležel J, Doleželová M, Novák FJ (1994) Flow cytometric estimation of nuclear DNA amount in diploid bananas (Musa acuminata and Musa balbisiana). Biol Plant 36: 351–357.

D’Hont A, Paget-Goy A, Escoute J, Carreel F (2000) The interspecific genome structure of cultivated banana, Musa spp. revealed by genomic DNA in situ hybridization. Theor Appl Genet 100: 177–183.

Osuji JO, Harrison G, Crouch J, Heslop-Harrison JS (1997) Identification of the genomic constitution of Musa L. lines (bananas, plantains and hybrids) using molecular cytogenetics. Ann Bot 80: 787–793.

Doleželová M, Valárik M, Swennen R, Horry JP, Doležel J (1998) Physical mapping of the 18S–25S and 5S ribosomal RNA genes in diploid bananas. Biol Plant 41: 497–505.

Hřibová E, Doleželová M, Doležel J (2008) Localization of BAC clones on mitotic chromosomes of Musa acuminata using fluorescence in situ hybridization. Biol Plant 52: 445–452.

Valárik M, Šimková H, Hřibová E, Šafář J, Doleželová M, et al. (2002) Isolation, characterization and chromosome localization of repetitive DNA sequences in bananas (Musa spp.). Chromosome Res 10: 89–100. PubMed

Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7: 175–184.

Otto F (1990) DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Crissman HA, Darzynkiewicz Z, editors. Methods in Cell Biology. Academic Press, New York, Vol. 33. Pp. 105–110. PubMed

Doležel J, Bartoš J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry A 51: 127–128. PubMed

D’Hont A, Denoeud F, Aury JM, Baurens FC, Carreel F, et al. (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488: 213–217. PubMed

Sonnhammer ELL, Durbin R (1995) A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167: GC1–GC10. PubMed

Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5: 233–241. PubMed

Huan X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9: 868–877. PubMed PMC

Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511–518. PubMed PMC

Galtier N, Gouy M, Gautier C (1996) SeaView and Phylo_win, two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12: 543–548. PubMed

Eckert AJ, Liechty JD, Tearse BR, Pande B, Neale DB (2010) DnaSAM: Software to perform neutrality testing for large datasets with complex null models. Mol Ecol Resour 10: 542–545. PubMed

Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188–1190. PubMed PMC

Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254–267. PubMed

Dechyeva D, Gindullis F, Schmidt T (2003) Divergence of satellite DNA and interspersion of dispersed repeats in the genome of the wild beet Beta procumbens . Chromosome Res 11: 3–21. PubMed

King K, Jobst J, Hemleben V (1995) Differential homogenization and amplification of two satellite DNAs in the genus Cucurbita (Cucurbitaceae). J Mol Evol 41: 996–1005. PubMed

Dover GA, Strachan T, Coen ES (1982) Molecular drive. Science 218: 1069. PubMed

Baldwin BG, Sanderson MJ, Porter MJ, Wojciechowski MF, Campbell CS, et al. (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann Mo Bot Gard 82: 247–277.

Dover G (2002) Molecular drive. Trends Genet 18: 587–589. PubMed

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

International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon . Nature 463: 763–768. PubMed

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

Galasso I, Schmidt T, Pignone D, Heslop-Harrison JS (1995) 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 91: 928–935. PubMed

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

Jiang J, Birchler JA, Parrott WA, Dawe RK (2003) A molecular view of plant centromeres. Trends Plant Sci 8: 570–574. PubMed

Macas J, Neumann P, Novák P, Jiang J (2010) Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinformatics 26: 2101–2108. PubMed

Torres GA, Gong Z, Iovene M, Hirsch CD, Buell CR, et al. (2011) Organization and evolution of subtelomeric satellite repeats in the potato genome. G3: Genes, Genomes, Genetics 1: 85–92. PubMed PMC

Hřibová E, Doleželová M, Town CD, Macas J, Doležel J (2007) Isolation and characterization of the highly repeated fraction of the banana genome. Cytogenet Genome Res 119: 268–274. PubMed

Bao W, Zhang W, Yang Q, Zhang Y, Han B, et al. (2006) Diversity of centromeric repeats in two closely related wild rice species, Oryza officinalis and Oryza rhizomatis . Mol Genet Genomics 275: 421–430. PubMed

Gindullis F, Desel C, Galasso I, Schmidt T (2001) The large-scale organization of the centromeric region in Beta species. Genome Res 11: 253–265. PubMed PMC

Kumekawa N, Ohmido N, Fukui K, Ohtsubo E, Ohtsubo H (2001) A new gypsy-type retrotransposon, RIRE7: preferential insertion into the tandem repeat sequence TrsD in pericentromeric heterochromatin regions of rice chromosomes. Mol Genet Genomics 265: 480–488. PubMed

Neumann P, Navrátilová A, Koblížková A, Kejnovský E, Hřibová E, et al. (2011) Plant centromeric retrotransposons: a structural and cytogenetic perspective. Mob DNA 2: 4. PubMed PMC

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. PubMed

Kubis SE, Heslop-Harrison JS, Desel C, Schmidt T (1998) The genomic organization of non-LTR retrotransposons (LINEs) from three Beta species and five other angiosperms. Plant Mol Biol 36: 821–31. PubMed

Kumar A, Bennetzen JL (1999) Plant retrotransposons. Annu Rev Genet 33: 479–532. PubMed

Schmidt T, Kubis S, Heslop-Harrison JS (1995) Analysis and chromosomal localisation of retrotransposons in sugar beet (Beta vulgaris) LINES and Ty1-copia- like elements as major components of the genome. Chromosome Res 3: 335–45. PubMed

Christelová P, Valárik M, Hřibová E, De Langhe E, Doležel J (2011) A multi gene sequence- based phylogeny of the Musaceae (banana) family. BMC Evol Biol 11: 103. PubMed PMC

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

Cai X, Xu SS (2007) Meiosis-driven genome variation in plants. Curr Genomics 8: 151–161. PubMed PMC

Dodds KS, Simmonds NW (1948) Sterility and parthenocarpy in diploid hybrids of Musa . Heredity 2: 101–117. PubMed

Shepherd K (1999) Cytogenetics of the genus Musa. IPGRI-INIBAP. Pp.160.

Wilson GB (1946) Cytological studies in the Musae. II. Meiosis in some diploid clones. Genetics 31: 475–482. PubMed

De Langhe E, Hřibová E, Carpentier S, Doležel J, Swennen R (2010) Did backcrossing contribute to the origin of hybrid edible bananas? Ann Bot 106: 849–857. PubMed PMC

Tek AL, Song JQ, Macas J, Jiang J (2005) Sobo, a recently amplified satellite repeat of potato, and its implications for the origin of tandemly repeated sequences. Genetics 170: 1231–1238. PubMed PMC

Urgaković D, Plohl M (2002) Variation in satellite DNA profiles-causes and effects. EMBO J 21: 5955–5959. PubMed PMC

Advances in the Molecular Cytogenetics of Bananas, Family Musaceae

Telomere-to-telomere gapless chromosomes of banana using nanopore sequencing

Chromosome Painting in Cultivated Bananas and Their Wild Relatives (Musa spp.) Reveals Differences in Chromosome Structure

Chromosome Painting Facilitates Anchoring Reference Genome Sequence to Chromosomes In Situ and Integrated Karyotyping in Banana (Musa Spp.)

Molecular and Cytogenetic Study of East African Highland Banana

Centromeric and non-centromeric satellite DNA organisation differs in holocentric Rhynchospora species

DArT whole genome profiling provides insights on the evolution and taxonomy of edible Banana (Musa spp.)

Molecular and Cytogenetic Characterization of Wild Musa Species

Genome-wide analysis of repeat diversity across the family Musaceae