Deep sequencing of mixed total DNA without barcodes allows efficient assembly of highly plastic Ascidian mitochondrial genomes

Genome Biology and Evolution

Volumn 5, Issue 6, 2013, Pages 1185-1199

  Rubinstein, Nimrod D ^a,e   Feldstein, Tamar ^a   Shenkar, Noa ^a   Botero Castro, Fidel ^b   Griggio, Francesca ^c   Mastrototaro, Francesco ^d   Delsuc, Frédéric ^b   Douzery, Emmanuel J P ^b   Gissi, Carmela ^c   Huchon, Dorothée ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF BARI   (Italy)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Ascidians; Gene order; Genome assembly; Illumina; Mitochondrial genome; Mitogenomics; Mixture models; Next generation sequencing; Phylogeny; Rearrangements; Tunicates

Indexed keywords

ANIMAL; ARTICLE; ASCIDIACEA; GENE ORDER; GENE REARRANGEMENT; GENETICS; GENOME ASSEMBLY; HIGH THROUGHPUT SEQUENCING; ILLUMINA; METHODOLOGY; MITOCHONDRIAL GENOME; MITOGENOMICS; MIXTURE MODELS; MOLECULAR GENETICS; NEXT-GENERATION SEQUENCING; NUCLEOTIDE SEQUENCE; PHYLOGENY; REARRANGEMENTS; UROCHORDATA; PROCEDURES;

ASCIDIANS; GENE ORDER; GENOME ASSEMBLY; ILLUMINA; MITOCHONDRIAL GENOME; MITOGENOMICS; MIXTURE MODELS; NEXT-GENERATION SEQUENCING; PHYLOGENY; REARRANGEMENTS; TUNICATES;

ANIMALS; BASE SEQUENCE; GENE ORDER; GENE REARRANGEMENT; GENOME, MITOCHONDRIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MOLECULAR SEQUENCE DATA; PHYLOGENY; UROCHORDATA;

EID: 84885390910     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evt081     Document Type: Article

References (62)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
2. Belinky F, Rot C, Ilan M, Huchon D. 2008. The complete mitochondrial genome of the demosponge Negombata magnifica (Poecilosclerida). Mol Phylogenet Evol. 47:1238-1243.
3. Bernt M, et al. 2007. CREx: inferring genomic rearrangements based on common intervals. Bioinformatics 23:2957-2958.
4. Betley JN, Frith MC, Graber JH, Choo S, Deshler JO. 2002. A ubiquitous and conserved signal for RNA localization in chordates. Curr Biol. 12:1756-1761.
5. Binladen J, et al. 2007. The use of coded PCR primers enables highthroughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2:e197.
6. Blanchette M, Bourque G, Sankoff D. 1997. Breakpoint phylogenies. Genome Inform Ser Workshop Genome Inform. 8:25-34.
7. Capella-Gutierrez S, Silla-Mart́inez JM, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972-1973.
8. Dahlberg C, et al. 2009. Refining the Ciona intestinalis model of central nervous system regeneration. PLoS One 4:e4458.
9. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicatesand not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968.
10. Denoeud F, et al. 2010. Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330:1381-1385.
11. Dettai A, et al. 2012. Conveniently pre-tagged and pre-packaged: extended molecular identification and metagenomics using complete metazoan mitochondrial genomes. PLoS One 7:e51263.
12. D'Onorio de Meo P, et al. 2012. MitoZoa 2.0:a database resource and search tools for comparative and evolutionary analyses of mitochondrial genomes in Metazoa. Nucleic Acids Res. 40:D1168-D1172.
13. Durrheim GA, Corfield VA, Harley EH, Ricketts MH. 1993. Nucleotide sequence of cytochrome oxidase (subunit III) from the mitochondrion of the tunicate Pyura stolonifera: evidence that AGR encodes glycine. Nucleic Acids Res. 21 3587-3588.
14. Fulton TM, Chunwongse J, Tanksley SD. 1995. Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep. 13:207-209.
15. Geller JB, Darling JA, Carlton JT. 2010. Genetic perspectives on marine biological invasions. Annu Rev Mar. Sci. 2:367-393.
16. Gissi C, et al. 2010. Hypervariability of ascidian mitochondrial gene order: exposing the myth of deuterostome organelle genome stability. Mol Biol Evol. 27:211-215.
17. Gissi C, Iannelli F, Pesole G. 2004. Complete mtDNA of Ciona intestinalis reveals extensive gene rearrangement and the presence of an atp8 and an extra trnM gene in ascidians. J Mol Evol. 58:376-389.
18. Gissi C, Pesole G. 2003. Transcript mapping and genome annotation of ascidian mtDNA using EST data. Genome Res. 13:2203-2212.
19. Govindarajan AF, Bucklin A, Madin LP. 2011. A molecular phylogeny of the Thaliacea. J Plankton Res. 33:843-853.
20. Groenenberg D J S, Pirovano W, Gittenberger E, Schilthuizen M. 2012. The complete mitogenome of Cylindrus obtusus (Helicidae, Ariantinae) using Illumina next generation sequencing. BMC Genomics 13:114.
21. Hazkani-Covo E, Zeller RM, Martin W. 2010. Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet. 6:e1000834.
22. Henson J, Tischler G, Ning Z. 2012. Next-generation sequencing and large genome assemblies. Pharmacogenomics 13:901-915.
23. Iannelli F, Griggio F, Pesole G, Gissi C. 2007. The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level. BMC Evol Biol. 7:155.
24. Iannelli F, Pesole G, Sordino P, Gissi C. 2007. Mitogenomics reveals two cryptic species in Ciona intestinalis. Trends Genet. 23:417-422.
25. Lambert G. 2001. A global overview of ascidian introductions and their possible impact on endemic fauna. In: Sawada H, Yokosawa H, Lambert CC, editors. The biology of ascidians. Tokyo (Japan): Springer-Verlag. p. 267-269.
26. Lambert G. 2009. Adventures of a sea squirt sleuth: unraveling the identity of Didemnum vexillum, a global ascidian invader. Aquat Invasions. 4:5-28.
27. Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3:a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286-2288.
28. Lartillot N, Philippe H. 2004. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol. 21:1095-1109.
29. Laslett D, Canback B. 2008. ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24:172-175.
30. Lavrov DV, Lang BF. 2005. Transfer RNA gene recruitment in mitochondrial DNA. Trends Genet. 21:129-133.
31. Li R, et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20:265-272.
32. Lin Y, et al. 2011. Comparative studies of de novo assembly tools for nextgeneration sequencing technologies. Bioinformatics 27:2031-2037.
33. 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.
34. Maricic T, Whitten M, Paabo S. 2010. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One 5:e14004.
35. Mastrototaro F, Dappiano M. 2008. New record of the non-indigenous species Microcosmus squamiger (Ascidiacea: Stolidobranchia) in the harbour of Salerno (Tyrrhenian Sea, Italy). Mar. Biodiv Rec. 1:2008e12.
36. McComish BJ, Hills S F K, Biggs PJ, Penny D. 2010. Index-free de novo assembly and deconvolution of mixed mitochondrial genomes. Genome Biol Evol. 2:410-424.
37. Miller JR, Koren S, Sutton G. 2010. Assembly algorithms for next-generation sequencing data. Genomics 95:315-327.
38. Monniot C, Monniot F, Laboute P. 1991. Coral reef ascidians of New Caledonia. Paris (France): ORSTOM editions.
39. Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470-474.
40. Pavesi G, Mauri G, Iannelli F, Gissi C, Pesole G. 2004. GeneSyn: a tool for detecting conserved gene order across genomes. Bioinformatics 20:1472-1474.
41. Pérez-Portela R, Bishop J D D, Davis AR, Turon X. 2009. Phylogeny of the families Pyuridae and Styelidae (Stolidobranchiata, Ascidiacea) inferred from mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol. 50:560-570.
42. Pesole G, Liuni S, D'Souza M. 2000. PatSearch: a pattern matcher software that finds functional elements in nucleotide and protein sequences and assesses their statistical significance. Bioinformatics 16:439-450.
43. Pollock DD, Eisen JA, Doggett NA, Cummings MP. 2000. A case for evolutionary genomics and the comprehensive examination of sequence biodiversity. Mol Biol Evol. 17:1776-1788.
44. Ranwez V, Harispe S, Delsuc F, Douzery E J P. 2011. MACSE: Multiple Alignment of Coding SEquences accounting for frameshifts and stop codons. PLoS One 6:e22594.
45. Robertson G, et al. 2010. De novo assembly and analysis of RNA-seq data. Nat Methods. 7:909-912.
46. Shenkar N, et al. World Ascidiacea Database [Internet] 2012. [cited 2013 Jun. 14]. Available from: http://www.marinespecies.org/ascidiacea.
47. Shenkar N, Loya Y. 2008. The solitary ascidian Herdmania momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biol Invasions. 10:1431-1439.
48. Shenkar N, Swalla BJ. 2011. Global diversity of Ascidiacea. PLoS One 6:e20657.
49. Simpson JT, et al. 2009. ABySS: a parallel assembler for short read sequence data. Genome Res. 19:1117-1123.
50. Singh TR, et al. 2009. Tunicate mitogenomics and phylogenetics: peculiarities of the Herdmania momus mitochondrial genome and support for the new chordate phylogeny. BMC Genomics 10:534.
51. Stach T, Braband A, Podsiadlowski L. 2010. Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. Mol Phylogenet Evol. 55:860-870.
52. Swalla BJ, Cameron CB, Corley LS, Garey JR. 2000. Urochordates are monophyletic within the deuterostomes. Syst Biol. 49:52-64.
53. Swofford DL. 2000. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4b10. Sunderland (MA): Sinauer Associates.
54. Timmermans M J T N, et al. 2010. Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Res. 38:1-4.
55. Tsagkogeorga G, et al. 2009. An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evol Biol. 9:187.
56. Tsagkogeorga G, Turon X, Galtier N, Douzery E J P, Delsuc F. 2010. Accelerated evolutionary rate of housekeeping genes in tunicates. J Mol Evol. 71:153-167.
57. Wolstenholme DR. 1992. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 141:173-216.
58. Yokobori S, Oshima T, Wada H. 2005. Complete nucleotide sequence of the mitochondrial genome of Doliolum nationalis with implications for evolution of urochordates. Mol Phylogenet Evol. 34:273-283.
59. Yokobori S, et al. 1999. Complete DNA sequence of the mitochondrial genome of the ascidian Halocynthia roretzi (Chordata, Urochordata). Genetics 153:1851-1862.
60. Zeng L, Swalla BJ. 2005. Molecular phylogeny of protochordates: chordate evolution. Can J Zool. 83:24-33.
61. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821.
62. Zerbino DR, McEwen GK, Margulies EH, Birney E. 2009. Pebble and rock band: heuristic resolution of repeats and scaffolding in the velvet shortread de novo assembler. PLoS One 4:e8407.