Fast evolving 18S rRNA sequences from Solenogastres (Mollusca) resist standard PCR amplification and give new insights into mollusk substitution rate heterogeneity

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Meyer, Achim ^a   Todt, Christiane ^b   Mikkelsen, Nina T ^b   Lieb, Bernhard ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EVOLUTIONARY BIOLOGY; GENETIC MARKER; HETEROGENEITY; MOLECULAR ANALYSIS; MOLLUSC; PHYLOGENETICS; POLYMERASE CHAIN REACTION; RNA;

ANIMALIA; APLACOPHORA; CEPHALOPODA; DOCOGLOSSA; MOLLUSCA; PATELLIDAE;

RNA 18S;

ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; CONFORMATION; DNA BASE COMPOSITION; GENETICS; MOLLUSC; PHYLOGENY; POLYMERASE CHAIN REACTION;

ANIMALS; BASE COMPOSITION; MOLLUSCA; NUCLEIC ACID CONFORMATION; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 18S;

EID: 77949714108     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-70     Document Type: Article

References (69)

1. Choosing the right molecular genetic markers for studying biodiversity: from molecular evolution to practical aspects. A Chenuil, Genetica 2006 127 1 101 120 10.1007/s10709-005-2485-1 16850217
2. Ribosomal DNA: molecular evolution and phylogenetic inference. DM Hillis MT Dixon, The Quarterly Review of Biology 1991 66 4 411 453 10.1086/417338 1784710
3. The involvement of RNA in ribosome function. PB Moore TA Steitz, Nature 2002 418 6894 229 235 10.1038/418229a 12110899
4. Molecular phylogeny of the animal kingdom. KG Field GJ Olsen DJ Lane SJ Giovannoni MT Ghiselin EC Raff NR Pace RA Raff, Science 1988 239 4841 748 753 10.1126/science.3277277 3277277
5. Evidence for a clade of nematodes, arthropods and other moulting animals. AMA Aguinaldo JM Turbeville LS Linford MC Rivera JR Garey RA Raff JA Lake, Nature 1997 387 6632 489 493 10.1038/387489a0 9168109
6. The new view of animal phylogeny. KM Halanych, Annual Review of Ecology Evolution and Systematics 2004 35 229 256 10.1146/annurev.ecolsys.35.112202. 130124 (Pubitemid 40059720)
7. Consideration of RNA secondary structure significantly improves likelihood-based estimates of phylogeny: Examples from the Bilateria. M Telford M Wise V Gowri-Shankar, Molecular Biology and Evolution 2005 22 4 1129 1136 10.1093/molbev/msi099 15689526
8. Can comprehensive background knowledge be incorporated into substitution models to improve phylogenetic analyses? A case study on major arthropod relationships. B von Reumont K Meusemann N Szucsich E Dell'Ampio V Gowri-Shankar D Bartel S Simon H Letsch R Stocsits Y-x Luan, et al. BMC Evolutionary Biology 2009 9 1 119 10.1186/1471-2148-9-119 19473484
9. An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. G Tsagkogeorga X Turon RR Hopcroft MK Tilak T Feldstein N Shenkar Y Loya D Huchon EJ Douzery F Delsuc, BMC Evolutionary Biology 2009 9 187 10.1186/1471-2148-9-187 19656395
10. Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. H Jow C Hudelot M Rattray P Higgs, Molecular Biology and Evolution 2002 19 9 1591 1601 12200486
11. Phylogeny and Evolution of Glass Sponges (Porifera, Hexactinellida). M Dohrmann D Janussen J Reitner AG Collins G Worheide, Systematic Biology 2008 57 3 388 405 10.1080/10635150802161088 18570034
12. Nearly complete rRNA genes assembled from across the metazoan animals: Effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction. J Mallatt CW Craig MJ Yoder, Molecular Phylogenetics and Evolution 2009 19786108
13. Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons. G Giribet A Okusu AR Lindgren SW Huff M Schroedl MK Nishiguchi, Proceedings of the National Academy of Sciences 2006 103 20 7723 7728 10.1073/pnas.0602578103 (Pubitemid 43752848)
14. New 18S rRNA sequences from neomenioid aplacophorans and the possible origin of persistent exogenous contamination. A Okusu G Giribet, Journal of Molluscan Studies 2003 69 4 385 387 10.1093/mollus/69.4.385
15. Limitations of Metazoan 18S rRNA Sequence Data: Implications for Reconstructing a Phylogeny of the Animal Kingdom and Inferring the Reality of the Cambrian Explosion. E Abouheif R Zardoya A Meyer, Journal of Molecular Evolution 1998 47 4 394 405 10.1007/PL00006397 9767685
16. The new animal phylogeny: Reliability and implications. A Adoutte G Balavoine N Lartillot O Lespinet B Prud'homme R de Rosa, Proceedings of the National Academy of Sciences of the United States of America 2000 97 9 4453 4456 10.1073/pnas.97.9.4453 10781043
17. Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. KJ Peterson DJ Eernisse, Evolution & Development 2001 3 3 170 205 10.1046/j.1525-142x.2001.003003170.x 11440251
18. Lophotrochozoan phylogeny assessed with LSU and SSU data: Evidence of lophophorate polyphyly. Y Passamaneck KM Halanych, Molecular Phylogenetics and Evolution 2006 40 1 20 28 10.1016/j.ympev.2006.02.001 16556507
19. Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences. YJ Passamaneck C Schander KM Halanych, Molecular Phylogenetics and Evolution 2004 32 1 25 38 10.1016/j.ympev.2003.12. 016 15186794
20. Relationships of higher molluscan taxa. G Haszprunar C Schander KM Halanych, Berkley, Los Angeles, London: University of California Press 2008 18431810
21. Phylogeny and Evolution of the Mollusca. C Todt A Okusu C Schander E Schwabe, Berkley, Los Angeles, London: University of California Press 2008
22. Investigation of molluscan phylogeny on the basis of 18S rRNA sequences. B Winnepenninckx T Backeljau R De Wachter, Molecular Biology and Evolution 1996 13 10 1306 1317 8952075
23. A combined approach to the phylogeny of Cephalopoda (Mollusca). AR Lindgren G Giribet MK Nishiguchi, Cladistics 2004 20 5 454 486 10.1111/j.1096-0031.2004.00032.x (Pubitemid 40047707)
24. Broad phylogenomic sampling improves resolution of the animal tree of life. C Dunn A Hejnol D Matus K Pang W Browne S Smith E Seaver G Rouse M Obst G Edgecombe, Nature 2008 452 7188 745 749 10.1038/nature06614 18322464
25. Phylogenetic support values are not necessarily informative: the case of the Serialia hypothesis (a mollusk phylogeny). JW Wägele H Letsch A Klussmann-Kolb C Mayer B Misof H Wägele, Frontiers in Zoology 2009 6 1 12 10.1186/1742-9994-6-12 19555513
26. Assessing the molluscan hypothesis Serialia (Monoplacophora + Polyplacophora) using novel molecular data. NG Wilson GW Rouse G Giribet, Molecular Phylogenetics and Evolution 2009 54 1 187 193 10.1016/j.ympev.2009.07. 028 19647088
27. A stitch in time: Efficient computation of genomic DNA melting bubbles. E Tostesen, Algorithms for Molecular Biology 2008 3 10 18637171
28. Disparity Index: A Simple Statistic to Measure and Test the Homogeneity of Substitution Patterns Between Molecular Sequences. S Kumar SR Gadagkar, Genetics 2001 158 3 1321 1327 11454778
29. MEGA 4: Molecular evolutionary genetics analysis (MEGA) software version 4. K Tamura J Dudley M Nei S Kumar, Molecular Biology and Evolution 2007 24 8 1596 1599 10.1093/molbev/msm092 17488738
30. A reversible jump method for bayesian phylogenetic inference with a nonhomogeneous substitution model. V Gowri-Shankar M Rattray, Molecular Biology and Evolution 2007 24 6 1286 1299 10.1093/molbev/msm046 17347157
31. Comparison of weighted labelled trees. D Robinson L Foulds, Combinatorial Mathematics VI 1979 119 126
32. Model Selection and Model Averaging in Phylogenetics: Advantages of Akaike Information Criterion and Bayesian Approaches Over Likelihood Ratio Tests. D Posada TR Buckley, Systematic Biology 2004 53 5 793 808 10.1080/10635150490522304 15545256
33. Frequency of formation of chimeric molecules as a consequence of PCR coamplification of 16S rRNA genes from mixed bacterial genomes. G Wang Y Wang, Applied and Environmental Microbiology 1997 63 12 4645 4650 9406382
34. DNA recombination during PCR. A Meyerhans J-P Vartanian S Wain-Hobson, Nucleic Acids Research 1990 18 7 1687 1691 10.1093/nar/18.7.1687 2186361
35. Betaine, Dimethyl Sulfoxide, and 7-Deaza-dGTP, a Powerful Mixture for Amplification of GC-Rich DNA Sequences. M Musso R Bocciardi S Parodi R Ravazzolo I Ceccherini, Journal of Molecular Diagnostics 2006 8 5 544 550 10.2353/jmoldx.2006.060058 17065422
36. Improved PCR method for amplification of GC-Rich DNA sequences. F Hube P Reverdiau S Iochmann Y Gruel, Molecular Biotechnology 2005 31 1 81 84 10.1385/MB:31:1:081 16118416
37. PCR-amplification of GC-rich regions: 'slowdown PCR'. UH Frey HS Bachmann J Peters W Siffert, Nature Protocols 2008 3 8 1312 1317 10.1038/nprot.2008.112 18714299
38. The digestive tract of Helicoradomenia (Solenogastres, Mollusca), aplacophoran molluscs from the hydrothermal vents of the East Pacific Rise. C Todt L von Salvini-Plawen, Invertebrate Biology 2005 124 3 230 253 10.1111/j.1744-7410.2005.00023.x (Pubitemid 41500885)
39. Ultrastructure of the midgut epithelium of Wirenia argentea (Mollusca: Solenogastres). C Todt L von Salvini-Plawen, Journal of Molluscan Studies 2004 70 3 213 224 10.1093/mollus/70.3.213
40. Cases in which parsimony or compatibility methods will be positively misleading. J Felsenstein, Systematic Zoology 1978 27 401 410 10.2307/2412923
41. What can 18S rDNA do for bivalve phylogeny? G Steiner M Müller, Journal of Molecular Evolution 1978 43 1 58 70 10.1007/BF02352300
42. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. C Gissi F Iannelli G Pesole, Heredity 2008 101 4 301 320 10.1038/hdy.2008.62 18612321
43. Molluscan Phylogeny: The Paleontological Viewpoint. B Runnegar J Pojeta Jr, Science 1974 186 4161 311 317 10.1126/science.186.4161.311 17839855
44. A modern approach to rotiferan phylogeny: combining morphological and molecular data. MV Sørensen G Giribet, Molecular Phylogenetics and Evolution 2006 40 2 585 608 10.1016/j.ympev.2006.04.001 16690327
45. Triploblastic Relationships with Emphasis on the Acoelomates and the Position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: A Combined Approach of 18S rDNA Sequences and Morphology. G Giribet DL Distel M Polz W Sterrer WC Wheeler, Systematic Biology 2000 49 3 539 562 10.1080/10635159950127385 12116426
46. Back in time: a new systematic proposal for the Bilateria. J Baguñà P Martinez J Paps M Riutort, Philosophical Transactions of the Royal Society B : Biological Sciences 2008 363 1496 1481 1491 10.1098/rstb.2007.2238
47. Lophotrochozoa internal phylogeny: new insights from an up-to-date analysis of nuclear ribosomal genes. J Paps J Baguñà M Riutort, Proceedings of the Royal Society B : Biological Sciences 2009 276 1660 1245 1254
48. Genomic clocks and evolutionary timescales. BS Hedges S Kumar, Trends in Genetics 2003 19 4 200 206 10.1016/S0168-9525(03)00053-2 12683973
49. Molecular dating when rates vary. JJ Welch L Bromham, Trends in Ecology & Evolution 2005 20 6 320 327 10.1016/j.tree.2005.02.007 (Pubitemid 40772079)
50. Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. WF Ponder DR Lindberg, Zoological Journal of the Linnean Society 1997 119 2 83 265 10.1111/j.1096-3642.1997.tb00137.x
51. A molecular phylogeny of the Patellogastropoda (Mollusca : Gastropoda). MG Harasewych AG McArthur, Marine Biology 2000 137 2 183 194 10.1007/s002270000332
52. There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. JA Thomas JJ Welch M Woolfit L Bromham, Proceedings of the National Academy of Sciences of the United States of America 2006 103 19 7366 7371 10.1073/pnas.0510251103 16651532
53. Rates of Molecular Evolution Are Linked to Life History in Flowering Plants. SA Smith MJ Donoghue, Science 2008 322 5898 86 89 10.1126/science. 1163197 18832643
54. Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. Fv Wintzingerode UB Goebel E Stackebrandt, FEMS Microbiology Reviews 1997 21 3 213 229 10.1111/j.1574-6976.1997.tb00351.x 9451814
55. Broad phylogenomic sampling improves resolution of the animal tree of life. CW Dunn A Hejnol DQ Matus K Pang WE Browne SA Smith E Seaver GW Rouse M Obst GD Edgecombe, et al. Nature 2008 452 7188 745 749 10.1038/nature06614 18322464
56. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. H Elwood G Olsen M Sogin, Molecular Biology and Evolution 1985 2 5 399 410 3939705
57. Deuterostome phylogeny and the sister group of the chordates: evidence from molecules and morphology. J Turbeville J Schulz R Raff, Molecular Biology and Evolution 1994 11 4 648 655 8078403
58. Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. C Bleidorn, Zoological Journal of the Linnean Society 2005 144 1 59 73 10.1111/j.1096-3642.2005.00160.x (Pubitemid 40670066)
59. Reparametrizing the loop entropy weights: effect on DNA melting curves. R Blossey E Carlon, Physical review E, Statistical, nonlinear, and soft matter physics 2003 68 0619111 0619118
60. Turner Algorithms and Thermodynamics for RNA Secondary Structure Prediction: A Practical Guide in RNA Biochemistry and Biotechnology. M Zuker DH Mathews DH Turner (eds), Kluwer Academic Publishers 1999
61. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. K Katoh K Misawa K-i Kuma T Miyata, Nucleic Acids Research 2002 30 14 3059 3066 10.1093/nar/gkf436 12136088
62. Recent developments in the MAFFT multiple sequence alignment program. K Katoh H Toh, Briefings in Bioinformatics 2008 9 4 286 298 10.1093/bib/bbn013 18372315
63. Accurate and efficient reconstruction of deep phylogenies from structured RNAs. RR Stocsits H Letsch J Hertel B Misof PF Stadler, Nucleic Acids Research 2009 37 18 6184 6193 10.1093/nar/gkp600 19723687
64. Phylogenetic utility of indels within ribosomal DNA and [beta]-tubulin sequences from fungi in the Rhizoctonia solani species complex. D González MA Cubeta R Vilgalys, Molecular Phylogenetics and Evolution 2006 40 2 459 470 10.1016/j.ympev.2006.03.022 16647865
65. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. A Stamatakis, Bioinformatics 2006 22 21 2688 2690 10.1093/bioinformatics/btl446 16928733
66. A Monte Carlo Approach Successfully Identifies Randomness in Multiple Sequence Alignments : A More Objective Means of Data Exclusion. B Misof K Misof, Systematic Biology 2009 58 1 21 34 10.1093/sysbio/syp006
67. Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. A Loytynoja N Goldman, Science 2008 320 5883 1632 1635 10.1126/science.1158395 18566285
68. How Many Bootstrap Replicates are Necessary? ND Pattengale M Alipour ORP Bininda-Emonds BME Moret A Stamatakis, Proceedings of RECOMB 2009
69. BEAST: Bayesian evolutionary analysis by sampling trees. A Drummond A Rambaut, BMC Evolutionary Biology 2007 7 1 214 10.1186/1471-2148-7-214 17996036