Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula

. 2007 Nov 21 ; 8 () : 427. [epub] 20071121

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid18031571

BACKGROUND: Extraordinary size variation of higher plant nuclear genomes is in large part caused by differences in accumulation of repetitive DNA. This makes repetitive DNA of great interest for studying the molecular mechanisms shaping architecture and function of complex plant genomes. However, due to methodological constraints of conventional cloning and sequencing, a global description of repeat composition is available for only a very limited number of higher plants. In order to provide further data required for investigating evolutionary patterns of repeated DNA within and between species, we used a novel approach based on massive parallel sequencing which allowed a comprehensive repeat characterization in our model species, garden pea (Pisum sativum). RESULTS: Analysis of 33.3 Mb sequence data resulted in quantification and partial sequence reconstruction of major repeat families occurring in the pea genome with at least thousands of copies. Our results showed that the pea genome is dominated by LTR-retrotransposons, estimated at 140,000 copies/1C. Ty3/gypsy elements are less diverse and accumulated to higher copy numbers than Ty1/copia. This is in part due to a large population of Ogre-like retrotransposons which alone make up over 20% of the genome. In addition to numerous types of mobile elements, we have discovered a set of novel satellite repeats and two additional variants of telomeric sequences. Comparative genome analysis revealed that there are only a few repeat sequences conserved between pea and soybean genomes. On the other hand, all major families of pea mobile elements are well represented in M. truncatula. CONCLUSION: We have demonstrated that even in a species with a relatively large genome like pea, where a single 454-sequencing run provided only 0.77% coverage, the generated sequences were sufficient to reconstruct and analyze major repeat families corresponding to a total of 35-48% of the genome. These data provide a starting point for further investigations of legume plant genomes based on their global comparative analysis and for the development of more sophisticated approaches for data mining.

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Shapiro JA, von Sternberg R. Why repetitive DNA is essential to genome function. Biol Rev. 2005;80:227–250. doi: 10.1017/S1464793104006657. PubMed DOI

Bennetzen JL. Patterns in grass genome evolution. Curr Opin Plant Biol. 2007;10:176–181. doi: 10.1016/j.pbi.2007.01.010. PubMed DOI

Morgante M, De Paoli E, Radovic S. Transposable elements and the plant pan-genomes. Curr Opin Plant Biol. 2007;10:149–155. doi: 10.1016/j.pbi.2007.02.001. PubMed DOI

Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 2007;8:272–285. doi: 10.1038/nrg2072. PubMed DOI

Flavell RB, Bennett MD, Smith JB, Smith DB. Genome size and proportion of repeated nucleotide-sequence dna in plants. Biochem Genet. 1974;12:257–269. doi: 10.1007/BF00485947. PubMed DOI

Murray MG, Peters DL, Thompson WF. Ancient repeated sequences in the pea and mung bean genomes and implications for genome evolution. J Mol Evol. 1981;17:31–42. doi: 10.1007/BF01792422. DOI

Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O. Doubling genome size without polyploidization: Dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 2006;16:1262–1269. doi: 10.1101/gr.5290206. PubMed DOI PMC

Neumann P, Koblizkova A, Navratilova A, Macas J. Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics. 2006;173:1047–1056. doi: 10.1534/genetics.106.056259. PubMed DOI PMC

Hawkins JS, Kim H, Nason JD, Wing RA, Wendel JF. Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 2006;16:1252–1261. doi: 10.1101/gr.5282906. PubMed DOI PMC

Macas J, Pozarkova D, Navratilova A, Nouzova M, Neumann P. Two new families of tandem repeats isolated from genus Vicia using genomic self-priming PCR. Mol Gen Genet. 2000;263:741–751. doi: 10.1007/s004380000245. PubMed DOI

Dechyeva D, Schmidt T. Molecular organization of terminal repetitive DNA in Beta species. Chromosome Res. 2006;14:881–897. doi: 10.1007/s10577-006-1096-8. PubMed DOI

Manetti ME, Rossi M, Costa APP, Clausen AM, Van Sluys MA. Radiation of the Tnt1 retrotransposon superfamily in three Solanaceae genera. BMC Evol Biol. 2007;7 PubMed PMC

Nouzova M, Neumann P, Navratilova A, Galbraith DW, Macas J. Microarray-based survey of repetitive genomic sequences in Vicia spp. Plant Mol Biol. 2001;45:229–244. doi: 10.1023/A:1006408119740. PubMed DOI

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;437:376–380. PubMed PMC

Smith MG, Gianoulis TA, Pukatzki S, Mekalanos JJ, Ornston LN, Gerstein M, Snyder M. New insights into Acinetobacter baumannii pathogenesis revealed by high-density pyrosequencing and transposon mutagenesis. Genes Dev. 2007;21:601–614. doi: 10.1101/gad.1510307. PubMed DOI PMC

Noonan JP, Coop G, Kudaravalli S, Smith D, Krause J, Alessi J, Chen F, Platt D, Paabo S, Pritchard JK, Rubin EM. Sequencing and analysis of Neanderthal genomic DNA. Science. 2006;314:1113–1118. doi: 10.1126/science.1131412. PubMed DOI PMC

Cheung F, Haas BJ, Goldberg SM, May GD, Xiao Y, Town CD. Sequencing Medicago truncatula expressed sequenced tags using 454 Life Sciences technology. BMC Genomics. 2006;7:272. doi: 10.1186/1471-2164-7-272. PubMed DOI PMC

Plant DNA C-values database

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 PubMed PMC

Neumann P, Nouzova M, Macas J. Molecular and cytogenetic analysis of repetitive DNA in pea (Pisum sativum L.) Genome. 2001;44:716–728. doi: 10.1139/gen-44-4-716. PubMed DOI

Neumann P, Pozarkova D, Macas J. Highly abundant pea LTR retrotransposon Ogre is constitutively transcribed and partially spliced. Plant Mol Biol. 2003;53:399–410. doi: 10.1023/B:PLAN.0000006945.77043.ce. PubMed DOI

Macas J, Neumann P, Pozarkova D. Zaba: a novel miniature transposable element present in genomes of legume plants. Mol Genet Genomics. 2003;269:624–631. doi: 10.1007/s00438-003-0869-4. PubMed DOI

Macas J, Koblizkova A, Neumann P. Characterization of Stowaway MITEs in pea (Pisum sativum L.) and identification of their potential master elements. Genome. 2005;48:831–839. PubMed

Neumann P, Pozarkova D, Koblizkova A, Macas J. PIGY, a new plant envelope-class LTR retrotransposon. Mol Genet Genomics. 2005;273:43–53. doi: 10.1007/s00438-004-1092-7. PubMed DOI

Pertea G, Huang XQ, 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

Macas J, Neumann P. Ogre elements – A distinct group of plant Ty3/gypsy-like retrotransposons. Gene. 2007;390:108–116. doi: 10.1016/j.gene.2006.08.007. PubMed DOI

Chavanne F, Zhang DX, Liaud MF, Cerff R. Structure and evolution of Cyclops: a novel giant retrotransposon of the Ty3/Gypsy family highly amplified in pea and other legume species. Plant Mol Biol. 1998;37:363–375. doi: 10.1023/A:1005969626142. PubMed DOI

Lee D, Ellis THN, Turner L, Hellens RP, Cleary WG. A copia-like element in Pisum demonstrates the uses of dispersed repeated sequences in genetic-analysis. Plant Mol Biol. 1990;15:707–722. doi: 10.1007/BF00016121. PubMed DOI

Laten HM, Havecker ER, Farmer LM, Voytas DF. SIRE1, an endogenous retrovirus family from Glycine max, is highly homogenous and evolutionarily young. Mol Biol Evol. 2003;20:1222–1230. doi: 10.1093/molbev/msg142. PubMed DOI

Xiong Y, Eickbush TH. Origin and evolution of retroelements based upon their reverse-transcriptase sequences. EMBO J. 1990;9:3353–3362. PubMed PMC

Richards EJ, Ausubel FM. Isolation of a higher eukaryotic telomere from Arabidopsis thaliana. Cell. 1988;53:127–136. doi: 10.1016/0092-8674(88)90494-1. PubMed DOI

Li RQ, Ye J, Li SG, Wang J, Han YJ, Ye C, Wang J, Yang HM, Yu J, Wong GKS, Wang J. ReAS: Recovery of ancestral sequences for transposable elements from the unassembled reads of a whole genome shotgun. PLoS Comput Biol. 2005;1:313–321. doi: 10.1371/journal.pcbi.0010043. PubMed DOI PMC

Elsik CG, Williams CG. Retroelements contribute to the excess low-copy-number DNA in pine. Mol Gen Genet. 2000;264:47–55. doi: 10.1007/s004380000279. PubMed DOI

Rabinowicz PD, Bennetzen JL. The maize genome as a model for efficient sequence analysis of large plant genomes. Curr Opin Plant Biol. 2006;9:149–156. doi: 10.1016/j.pbi.2006.01.015. PubMed DOI

Feschotte C, Jiang N, Wessler SR. Plant transposable elements: Where genetics meets genomics. Nat Rev Genet. 2002;3:329–341. doi: 10.1038/nrg793. PubMed DOI

Bennetzen JL, Ma JX, Devos K. Mechanisms of recent genome size variation in flowering plants. Ann Bot. 2005;95:127–132. doi: 10.1093/aob/mci008. PubMed DOI PMC

Gao LH, McCarthy EM, Ganko EW, McDonald JF. Evolutionary history of Oryza sativa LTR retrotransposons: a preliminary survey of the rice genome sequences. BMC Genomics. 2004;5 PubMed PMC

Hill P, Burford D, Martin DMA, Flavell AJ. Retrotransposon populations of Vicia species with varying genome size. Mol Genet Genomics. 2005;273:371–381. doi: 10.1007/s00438-005-1141-x. PubMed DOI

Flavell , Smith , Kumar Extreme heterogeneity of Ty1-copia group retrotransposons in plants. Mol Gen Genet. 1992;231:233–242. PubMed

Wicker T, Keller B. Genome-wide comparative analysis of copia retrotransposons 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

Macas J, Meszaros T, Nouzova M. PlantSat: a specialized database for plant satellite repeats. Bioinformatics. 2002;18:28–35. doi: 10.1093/bioinformatics/18.1.28. PubMed DOI

Navratilova A, Neumann P, Macas J. Long-range organization of plant satellite repeats investigated using strand-specific FISH. Cytogenet Genome Res. 2005;109:58–62. doi: 10.1159/000082382. PubMed DOI

Macas J, Navratilova A, Koblizkova A. Sequence homogenization and chromosomal localization of VicTR-B satellites differ between closely related Vicia species. Chromosoma. 2006;115:437–447. doi: 10.1007/s00412-006-0070-8. PubMed DOI

Kulikova O, Geurts R, Lamine M, Kim DJ, Cook DR, Leunissen J, de Jong H, Roe BA, Bisseling T. Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma. 2004;113:276–283. doi: 10.1007/s00412-004-0315-3. PubMed DOI

Jiang JM, Birchler JA, Parrott WA, Dawe RK. A molecular view of plant centromeres. Trends Plant Sci. 2003;8:570–575. doi: 10.1016/j.tplants.2003.10.011. PubMed DOI

Fajkus J, Sykorova E, Leitch AR. Telomeres in evolution and evolution of telomeres. Chromosome Res. 2005;13:469–479. doi: 10.1007/s10577-005-0997-2. PubMed DOI

Vershinin AV, Heslop-Harrison JS. Comparative analysis of the nucleosomal structure of rye, wheat and their relatives. Plant Mol Biol. 1998;36:149–161. doi: 10.1023/A:1005912822671. PubMed DOI

The NCBI Trace Archive

Altschul SF, Madden TL, Schaffer AA, Zhang JH, 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 SQ, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu CL, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang YL, 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

Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110:462–467. doi: 10.1159/000084979. PubMed DOI

Jurka J. Repbase Update – a database and an electronic journal of repetitive elements. Trends Genet. 2000;16:418–420. doi: 10.1016/S0168-9525(00)02093-X. PubMed DOI

Zmasek CM, Eddy SR. ATV: display and manipulation of annotated phylogenetic trees. Bioinformatics. 2001;17:383–384. doi: 10.1093/bioinformatics/17.4.383. PubMed DOI

Rambaut A, Charleston M. TreeEdit – Phylogeny Editor and Manipulator

Clamp M, Cuff J, Searle SM, Barton GJ. The Jalview Java alignment editor. Bioinformatics. 2004;20:426–427. doi: 10.1093/bioinformatics/btg430. PubMed DOI

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

Leitch A, Schwarzacher T, Jackson D, Leitch I. In Situ Hybridization: a practical guide. Oxford: BIOS Scientific Publishers Ltd; 1994.

Neumann P, Pozarkova D, Vrana J, Dolezel J, Macas J. Chromosome sorting and PCR-based physical mapping in pea (Pisum sativum L.) Chromosome Res. 2002;10:63–71. doi: 10.1023/A:1014274328269. PubMed DOI

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