The ITS1-5.8S-ITS2 sequence region in the Musaceae: structure, diversity and use in molecular phylogeny

. 2011 Mar 22 ; 6 (3) : e17863. [epub] 20110322

Jazyk angličtina Země Spojené státy americké Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21445344

Genes coding for 45S ribosomal RNA are organized in tandem arrays of up to several thousand copies and contain 18S, 5.8S and 26S rRNA units separated by internal transcribed spacers ITS1 and ITS2. While the rRNA units are evolutionary conserved, ITS show high level of interspecific divergence and have been used frequently in genetic diversity and phylogenetic studies. In this work we report on the structure and diversity of the ITS region in 87 representatives of the family Musaceae. We provide the first detailed information on ITS sequence diversity in the genus Musa and describe the presence of more than one type of ITS sequence within individual species. Both Sanger sequencing of amplified ITS regions and whole genome 454 sequencing lead to similar phylogenetic inferences. We show that it is necessary to identify putative pseudogenic ITS sequences, which may have negative effect on phylogenetic reconstruction at lower taxonomic levels. Phylogenetic reconstruction based on ITS sequence showed that the genus Musa is divided into two distinct clades--Callimusa and Australimusa and Eumusa and Rhodochlamys. Most of the intraspecific banana hybrids analyzed contain conserved parental ITS sequences, indicating incomplete concerted evolution of rDNA loci. Independent evolution of parental rDNA in hybrids enables determination of genomic constitution of hybrids using ITS. The observation of only one type of ITS sequence in some of the presumed interspecific hybrid clones warrants further study to confirm their hybrid origin and to unravel processes leading to evolution of their genomes.

Zobrazit více v PubMed

Gilbert W. Origin of life: the RNA world. Nature. 1986:319–618.

Rogers SO, Bendich AJ. Ribosomal RNA genes in plants: variability in copy number and in intergenic spacer. Plant Mol Biol. 1987;9:509–520. PubMed

Hillis DM, Dixon MT. Ribosomal DNA – molecular evolution and phylogenetic inference. Q Rev Biol. 1991;66:410–453. PubMed

Hershkovitz MA, Zimmer EA. Conservation patterns in angiosperm ITS2 sequences. Nucleic Acids Res. 1996;24:2857–2867. PubMed PMC

Jobes DV, Thien LB. A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequence. Plant Mol Biol Rep. 1997;15:326–334.

Coleman AW. Pan-eukaryote ITS2 homologies revealed by RNA secondary structure. Nucleic Acids Res. 2007;35:3322–3329. PubMed PMC

Schultz J, Stefanie M, Gerlach D, Muller T, Wolf M. A common core of secondary structure of the internal transcribed spacer 2 (ITS2) throughout the Eukaryota. RNA. 2007;11:361–364. PubMed PMC

Wolf M, Achtziger M, Schultz J, Dandekar T. Homology modeling revealed more than 20,000 rRNA internal transcribed spacer 2 (ITS2) secondary structures. Bioinformatics. 2005;11:1616–1623. PubMed PMC

Harpke D, Peterson A. 5.8S motifs for the identification of pseudogenic ITS regions. Botany. 2008a;86:300–305. PubMed

Harpke D, Peterson A. Extensive 5.8S nrDNA polymorphism in Mammillaria (Cactaceae) with special reference to the identification of pseudogenic internal transcribed spacer region. J Plant Res. 2008b;121:261–270. PubMed

Ochieng JW, Henry RJ, Baverstock PR, Steane DA, Shepherd M. Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs. Mol Phylogenet Evol. 2007;44:752–764. PubMed

Xiao L-Q, Möller M, Zhu H. High nrDNA ITS polymorphism in the ancient extant seed plant Cycas: Incomplete concerted evolution and the origin of pseudogenes. Mol Phylogenet Evol. 2010;55:168–177. PubMed

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

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

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

Wendel JF, Schnabel A, Seelanan T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci U S A. 1995;92:280–284. PubMed PMC

Alvarez I, Wendel JF. Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol. 2003;29:417–434. PubMed

Kovařík A, Matyášek R, Lim KY, Skalická K, Koukalová B, et al. Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biol J Linn Soc. 2004;82:615–625.

Francisco-Ortega J, Barber JC, Santos-Guerra A, Febles-Hernández R, Jansen RR. Origin and evolution of the endemic genera of Gonosperminae (Asteraceae: Anthemideae) from the Canary Islands: Evidence from nucleotide sequences of the internal transcribed spacers of the nuclear ribosomal DNA. Am J Bot. 2001;88:161–169. PubMed

Renner SS, Schaefer H, Kocyan A. Phylogenetics of Cucumis (Cucurbitaceae): Cucumber (C. sativus) belongs in an Asian/Australian clade far from melon (C. melo). BMC Evol Biol. 2007;7:58. Available: http://www.biomedcentral.com/1471-2148/7/58. Accessed 2010 Aug 12. PubMed PMC

Pettengill JB, Neel MC. Phylogenetic patterns and conservation among North American members of the genus Agalinis (Orobanchaceae). BMC Evol Biol. 2008;8:264. Available: http://www.biomedcentral.com/1471-2148/8/264. Accessed 2010 Aug 12. PubMed PMC

Sun K, Chen X, Ma R, Li C, Wang Q, et al. Molecular phylogenetics of Hippophae L. (Elaegnaceae) based on the internal transcribed spacer (ITS) sequence of nrDNA. Plant Syst Evol. 2002;235:121–134.

Liu QL, Ge S, Tang HB, Zhang XL, Zhu GF, et al. Phylogenetic relationships in Elymus (Poaceae : Triticeae) based on the nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. New Phytol. 2006;170:411–4206. PubMed

Wang QD, Zhang T, Wang JB. Phylogenetic relationships and hybrid origin of Potamogeton species (Potamogetonaceae) distributed in China: insight from the nuclear ribosomal internal transcribed spacer sequence (ITS). Plant Syst Evol. 2007;267:65–78.

O'Kane SL, Schaal BA, Al-Shehbaz IA. The origin of Arabidopsis suecica as indicated by nuclear rDNA sequences. Syst Bot. 1996;21:559–566.

Popp M, Oxelman B. Inferring the history of the polyploid Silene aegaea (Caryophyllacea) using plastid and homeologous nuclear DNA sequences. Mol Phylogenet Evol. 2001;20:474–481. PubMed

Bennet RI, Smith AG. Use of a genomic clone for ribosomal RNA from Brassica oleracea in RFLP analysis of Brassica species. Plant Mol Biol. 1991;16:685–688. PubMed

Barkman TJ, Simpson BB. Hybrid origin and parentage of Dendrochilum acuiferum (Orchidaceae) infered in a phylogenetic context using nuclear and plastid DNA sequence data. Syst Bot. 2002;27:209–220.

Volkov RA, Komarova NY, Hemleben V. Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodivers. 2007;5:261–276.

Dadejová M, Lim KY, Součková-Skalická K, Matyášek R, Grandbastien M-A, et al. Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol. 2007;174:658–668. PubMed

Kovařík A, Pires JC, Leitch AR, Lim KY, Sherwood AM, et al. Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics. 2005;169:931–944. PubMed PMC

Lim KY, Matyášek R, Kovařík A, Leitch A. Genome evolution in allotetraploid Nicotiana. Biol J Linn Soc. 2004;82:599–606.

Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V. Elimination and rearrangement of parental rDNA in the allopolyploid Nicotiana tabacum. Mol Biol Evol. 1999;16:311–320. PubMed

Mayol M, Rosselló JA. Why nuclear ribosomal DNA spacers (ITS) tell us different stories in Quercus. Mol Phylogenet Evol. 2001;19:167–176. PubMed

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

Cheesman EE. Classification of the bananas II. The genus Musa L. Kew Bull. 1947;2:106–117.

Gawel NJ, Jarret RL, Whittemore AP. Restriction fragment length polymorphism (RFLP)-based phylogenetic analysis of Musa. Theor Appl Genet. 1992;84:286–290. PubMed

Lanaud C, Tezenas du Montcel H, Jolivot MP, Glaszmann JC, González de León D. Variation of ribosomal gene spacer length among wild and cultivated banana. Heredity. 1992;68:147–156. PubMed

Wong C, Kiew R, Argent G, Set O, Lee SK, et al. Assessment of the validity of the section in Musa (Musaceae) using AFLP. Ann Bot. 2002;90:231–238. PubMed PMC

Ude G, Pillay M, Ogundiwin E, Tenkouano A. Analysis of genetic diversity and sectional relationships in Musa using AFLP markers. Theor Appl Genet. 2002;104:1239–1245. PubMed

Risterucci AM, Hippolyte I, Perrier X, Xia L, Caig V, et al. Development and assesment of Diversity Array technology for high-throughput DNA analysis in Musa. Theor Appl Genet. 2009;119:1093–1103. PubMed

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. PubMed

Hakkinen M. Musa voonii, a new Musa species from northern Borneo and discussion of the section Callimusa in Borneo. Acta Phytotaxon Geobot. 2004;55:79–88.

Hakkinen M. Musa azizii, a new Musa species (Musaceae) from northern Borneo. Acta Phytotaxon Geobot. 2005;56:27–31.

Amorim EP, Vilarinhos AD, Cohen KO, Amorim VBO, dos Santos-Serejo JA, et al. Genetic diversity of carotenoid–rich bananas evaluated by Diversity Arrays Technology. Genet Mol Biol. 2009;32:96–103. PubMed PMC

Buhariwalla HK, Jarret RL, Jayashree B, Crouch JH, Ortiz R. Isolation and characterization of microsatellite markers from Musa balbisiana. Mol Ecol Notes. 2005;5:327–330.

Wang XL, Chiang TY, Roux N, Hao G, Ge XJ. Genetic diversity of wild banana (Musa balbisiana Colla) in China as revealed by AFLP markers. Genet Resour Crop Evol. 2007;54:1125–1132.

Nwakanma DC, Pillay M, Okoli BE, Tenkouano A. PCR-RFLP of the ribosomal DNA internal transcribed spacer (ITS) provides markers for the A and B genomes in Musa L. Theor Appl Genet. 2003;108:154–159. PubMed

Li L-F, Hakkinen M, Yuan Y-M, Hao G, Ge X-J. Molecular phylogeny and systematics of the banana family (Musaceae) inferred from multiple nuclear and chloroplast DNA fragments, with a special reference to the genus Musa. Mol Phylogenet Evol. 2010;57:1–10. PubMed

Liu A-Z, Kress J, Li D-Z. Phylogenetic analyses of the banana family (Musaceae) based on nuclear ribosomal (ITS) and chloroplast (trnL-F) evidence. Taxon. 2010;59:20–28.

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

Bailey CD, Carr TG, Harris SA, Hughes CE. Characterization of angiosperm nrDNA polymorphism, paralogy and pseudogenes. Mol Phylogenet Evol. 2003;29:435–455. PubMed

Kim ST, Sultan SE, Donoghue MJ. Allopolyploid speciation in Persicaria (Polygonaceae): insights from a low-copy nuclear region. Proc Natl Acad Sci U S A. 2008;105:12370–12375. PubMed PMC

Ritz CM, Schmuths H, Wissemann V. Evolution by reticulation: European dogroses originated by multiple hybridization across the genus Rosa. J Hered. 2005;96:4–14. PubMed

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

Wissemann V. Molecular evidence for allopolyploid origin of the Rosa canina complex (Rosaceae, Rosoideae). J Appl Bot. 2002;76:176–178.

Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005;473:376–380. PubMed PMC

Simmond NW. The evolution of the bananas. London: Longmans; 1962. 170

Shepherd K. Observation on Musa taxonomy. 1988. pp. 158–165. In: Identification of Genetic Diversity in the Genus Musa. Proc. Int. Workshop held at Los Banos, Philippines 5–10 September. INIBAP, Montpellier, France.

Simmond NW. Notes on banana taxonomy. Kew Bull. 1960;14:198–212.

Samuel R, Bachmair A, Jobst J, Ehrendorfer F. ITS sequences from nuclear rDNA suggest phylogenetic relationships between Euro-Mediterranean, East Asiatic and North American Quercus (Fagaceae). Plant Syst Evol. 1998;211:129–139.

Manos P, Doyle JJ, Nixon KC. Phylogeny, biogeography and processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Mol Phylogenet Evol. 1999;12:333–349. PubMed

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

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

Šafář J, Noa-Carrazana JC, Vrána J, Bartoš J, Alkhimova O, et al. Creation of a BAC resource to study the structure and evolution of the banana (Musa balbisiana) genome. Genome. 2004;47:1182–1191. PubMed

Meyer M, Briggs AW, Maricic T, Hober B, Hoffner B, et al. From micrograms to picograms: quantitative PCR reduces the material demands of high-throughput sequencing. Nucl Acids Res. 2008;36:e5. doi: 10.1093/nar/gkm1095. PubMed DOI PMC

Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0. 1996–2004. Available: http://www.repeatmasker.org.

Huan X, Madan A. CAP3: A DNA sequence assembly program. Genome Res. 1999;9:868–877. 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. Available: http://www.biomedcentral.com/1471-2164/8/427. Accessed 2010 Sep 10. PubMed PMC

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. PubMed PMC

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

Kumar S, Tamura K, Nei M. MEGA, Molecular Evolutionary Genetics Analysis software for microcomputers. Bioinformatics. 1994;10:189–191. PubMed

Mathews DH, Sabina J, Zuker M, Turner DH. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol. 1999;288:911–940. PubMed

Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003;31:3406–3415. PubMed PMC

Tomlinson PB. Phylogeny of the Scitamineae: Morphological and anatomical considerations. Evolution. 1962;16:192–213.

Kress WJ, Prince LM, Hahn WJ, Zimmer EA. Unraveling the evolution of the families of the Zingiberales using morphological and molecular evidence. Syst Biol. 2001;50:926–944. PubMed

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

Posada D. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 2008;25:1253–1256. PubMed

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696–704. PubMed

Akaike H. A new look at the statistical model identification. IEEE Trans Autom Control. 1974;19:716–723.

Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214. Available: http://www.biomedcentral.com/1471-2148/7/214. Accessed 2010 Sep 10. PubMed PMC

Wuyts J, De Rijk P, Van de Peer Y, Winkelmans T, De Wachter R. The European large subunit ribosomal RNA database. Nucleic Acids Res. 2001;29:175–177. PubMed PMC

Perrier X, Bakry F, Carreel F, Jenny C, Horry J-P, et al. Combining biological approaches to shed light on the evolution of edible bananas. Ethnobotany Research & Applications. 2009;7:199–216.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...