Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes

详细信息    查看全文

• 作者：Tahera Sultana (1)
  Jiyeon Kim (2)
  Sang-Hwa Lee (2)
  Hyerim Han (3)
  Sanghee Kim (4)
  Gi-Sik Min (1)
  Steven A Nadler (5)
  Joogn-Ki Park (2) (6)
  
• 关键词：Plant parasitism ; Tylenchomorpha ; Chromadorea ; Nematoda ; Mitochondrial genome ; Molecular phylogeny
• 刊名：BMC Evolutionary Biology
• 出版年：2013
• 出版时间：December 2013
• 年：2013
• 卷：13
• 期：1
• 全文大小：402KB
• 参考文献：1. Golden AM: Classification of the genera and higher categories of the order Tylenchida (Nematoda). In / Plant parasitic nematdoes. Volume 1. Edited by: Zuckerman BM, Mai WF, Rohde RA. New York/London: Academic Press; 1971:191鈥?32.
  2. Poinar GO Jr: Nematoda and Nematomorpha. In / Ecology and Classification of North American Freshwater Invertebrat. Edited by: New York: Thorp JH, Covich AP. Academic Press; 1991:249鈥?83.
  3. Baldwin JG, Nadler SA, Adams BJ: Evolution of plant parasitism among nematodes. / Annu Rev Phytopathol 2004, 42:83鈥?05. CrossRef
  4. Malakhov VV: / Nematodes: Structure, Development, Classification, and Phylogeny. Edited by: Hope WD. Washington/London: Smithsonian Institution Press; 1994.
  5. Bridge J, Starr JL: / Plant Nematodes of Agricultural Importance: A Color Handbook. London: Academic Press; 2007.
  6. Mai WF: Introduction. In / Plant Parasitic Nematodes. Volume 1. Edited by: Zuckerman BM, Mai WF, Rohde RA. New York/London: Academic Press; 1971:1鈥?.
  7. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK: A molecular evolutionary framework for the phylum Nematoda. / Nature 1998, 392:71鈥?5. CrossRef
  8. Dorris M, De Lay P, Blaxter ML: Molecular analysis of nematode diversity and the evolution of parasitism. / Parasitol Today 1999, 15:188鈥?93. CrossRef
  9. Holterman M, van der Wurff A, van den Elsen S, van Megen H, Bongers T, Holovachov O, Bakker J, Helder J: Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. / Mol Biol Evol 2006, 23:1792鈥?800. CrossRef
  10. Smythe A, Sanderson MJ, Nadler SA: Nematode small subunit phylogeny correlates with alignment parameters. / Syst Biol 2006, 55:972鈥?92. CrossRef
  11. Bert W, Leliaert F, Vierstraete AR, Vanfleteren JR, Borgonie G: Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda: Rhabditida). / Mol Phylogenet Evol 2008, 48:728鈥?44. CrossRef
  12. De Ley P, Blaxter ML: Systematic position and phylogeny. In / The Biology of Nematodes. Edited by: Lee BL. New York: Taylor; 2002:1鈥?0.
  13. De Ley P, Blaxter ML: A new system for Nematoda: combining morphological characters with molecular trees, and translating clades into ranks and taxa. / Nematology Monographs and Perspectives 2004, 2:633鈥?53.
  14. Siddiqi MR: The origin and phylogeny of the nematode orders Tylenchida Thorne, 1949 and Aphelenchida n. ord. / Helminth Abstr Ser B 1980, 49:143鈥?70.
  15. Lorenzen S: Entwurf eines phylogenetischen systems der freilebenden nematoden. / Ver枚ff Inst Meeresforsch Bremerh 1981, 7:1鈥?72.
  16. Geraert E: The use of the female reproductive systems in nematode systematics. In / Concepts in Nematode Systematics. Edited by: Stone AR, Platt HM, Khalil LF. London: Academic Press; 1983:73鈥?4.
  17. Siddiqi MR: / Tylenchida: Parasites of Plants and Insects. 2nd edition. Wallingford: CABI; 2000. CrossRef
  18. Maggenti AR: Nemata. In / Synopsis and Classification of Living Organisms. Edited by: Parker SP. New York: McGraw-Hill; 1982:879鈥?29.
  19. Siddiqi MR: Evolution of plant parasitism in nematodes. In / Concepts in Nematode Systematics. Edited by: Stone AR, Platt HM, Khalil LF. London: Academic Press; 1983:113鈥?29.
  20. Ragsdale E, Ngo PT, Crum J, Ellisman MH, Baldwin JG: Reconstruction of the pharyngeal corpus of Aphelenchus avenae (Nematoda: Tylenchomorpha), with implications for phylogenetic congruence. / Zool J Linn Soc 2011, 161:1鈥?0. CrossRef
  21. Hu M, Gasser RB: Mitochondrial genomes of parasitic nematodes-progress and perspectives. / Trends Parasitol 2006, 22:78鈥?4. CrossRef
  22. Kim KH, Eom KS, Park JK: The complete mitochondrial genome of Anisakis simplex (Ascaridida. Nematoda) and phylogenetic implications. / Int J Parasitol 2006, 36:319鈥?28. CrossRef
  23. Kang S, Sultana T, Eom KS, Park YC, Soonthornpong N, Nadler SA, Park JK: The mitochondrial genome sequence of Enterobius vermicularis (Nematoda. Oxyurida)-an idiosyncratic gene order and phylogenetic information for chromadorean nematodes. / Gene 2009, 429:87鈥?7. CrossRef
  24. Park JK, Sultana T, Lee SH, Kang S, Kim HL, Min GS, Eom KS, Nadler SA: Monophyly of clade III nematodes is not supported by phylogenetic analysis of complete mitochondrial genome sequences. / BMC Genomics 2011, 12:392. CrossRef
  25. Jacob JEM, Vanholme B, Van Leeuwen T, Gheysen G: A unique genetic code change in the mitochondrial genome of the parasitic nematode Radopholus similis. / BMC Research Notes 2009, 2:192. CrossRef
  26. Gibson T, Farrugia D, Barrett J, Chitwood DJ, Rowe J, Subbotin S, Dowton M: The mitochondrial genome of the soybean cyst nematodes, Heterodera glycines. / Genome 2011, 54:565鈥?74. CrossRef
  27. Okimoto R, Chamberlin HM, Macfarlane JL, Wolstenholme DR: Repeated sequence sets in mitochondrial DNA molecules of root knot nematodes (Meloidogyne): nucleotide sequences, genome location and potential for host-race identification. / Nucleic Acids Res 1991, 19:1619鈥?626. CrossRef
  28. Hyman BC, Lewis SC, Tang S, Wu Z: Rampant gene rearrangement and haplotype hypervariation among nematode mitochondrial genomes. / Genetica 2011, 139:611鈥?15. CrossRef
  29. Lavrov DV, Brown WM: Trichinella spiralis mtDNA: a nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAs and has a gene arrangement relatable to those of coelomate metazoans. / Genetics 2001, 157:621鈥?37.
  30. Wolstenholme DR: Animal mitochondrial DNA: structure and evolution. / Int Rev Cytol 1992, 141:173鈥?16. CrossRef
  31. Ojala D, Montoya J, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. / Nature 1981, 290:470鈥?74. CrossRef
  32. Okimoto R, Macfarlane JL, Clary DO, Wolstenholme DR: The mitochondrial genomes of two Nematodes, Caenorhabditis elegans and Ascaris suum. / Genetics 1992, 130:471鈥?98.
  33. Keddie EM, Higazi T, Unnasch TR: The mitochondrial genome of Onchocerca volvulus: sequence, structure and phylogenetic analysis. / Mol Biochem Parasitol 1998, 95:111鈥?27. CrossRef
  34. Hu M, Chilton NB, Gasser RB: The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda. Secernentea). / Int J Parasitol 2002, 32:145鈥?58. CrossRef
  35. Hu M, Chilton NB, Gasser RB: The mitochondrial genome of Strongyloides stercoralis (Nematoda)-idiosyncratic gene order and evolutionary implications. / Int J Parasitol 2003, 33:1393鈥?408. CrossRef
  36. Bentzen P, Leggett WC, Brown GG: Length and restriction site heteroplasmy in the mitochondrial DNA of American shad (Alosa sapidissima). / Genetics 1988, 118:509鈥?18.
  37. Boyce TM, Zwick ME, Aquadro CF: Mitochondrial DNA in the bark weevils: size, structure and heteroplasmy. / Genetics 1989, 123:825鈥?36.
  38. Gjetvaj B, Cook DI, Zouros E: Repeated sequences and large-scale variation of mitochondrial DNA: a common feature among scallops (Bivalvia. Pectinidae). / Mol Biol Evol 1992, 9:106鈥?24.
  39. Tang S, Hyman BC: Mitochondrial genome haplotype hypervariation within the isopod parasitic nematode Thaumamermis cosgrovei. / Genetics 2007, 176:1139鈥?150. CrossRef
  40. Lunt DH, Whipple LE, Hyman BC: Mitochondrial DNA variable number tandem repeats (VNTRs): utility and problems in molecular ecology. / Mol Ecol 1998, 7:1441鈥?455. CrossRef
  41. Boore JL, Brown WM: Big trees from little genomes: mitochondrial gene order as a phylogenetic tool. / Curr Opin Genetics Deve 1998, 8:668鈥?74. CrossRef
  42. Boore JL: Animal mitochondrial genomes. / Nucleic Acids Res 1999, 27:1767鈥?780. CrossRef
  43. Lavrov DV, Lang BF: Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. / Syst Biol 2005, 54:651鈥?59. CrossRef
  44. Boore JL, Medina M, Rosenberg LA: Complete sequences of the highly rearranged molluscan mitochondrial genomes of the scaphopod Graptacme eborea and the bivalve Mytilus edulis. / Mol Biol Evol 2004, 21:1492鈥?503. CrossRef
  45. Valles Y, Boore JL: Lophotrochozoan mitochondrial genomes. / Integr Comp Biol 2006, 46:544鈥?57. CrossRef
  46. Stach T, Braband A, Podsiadlowski L: Erosion of phylogenetic signal in tunicate mitochondrial genomes on different levels of analysis. / Mol Phylogenet Evol 2010, 55:860鈥?70. CrossRef
  47. Kilpert F, Podsiadlowski L: The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features. / BMC Genomics 2006, 7:241. CrossRef
  48. Thorne G: On the classification of the Tylenchida, new order (Nematoda. Phasmidia). / Proc Helminth Soc Wash 1949, 16:37鈥?3.
  49. Paramonov AA: / Plant-Parasitic Nematodes: Systematics of Nematodes Superfamily Tylenchoidea. Volume 3. Edited by: Skrjabin K. Washington DC: The U.S. Department of Agriculture and the National Science Foundation; 1972.
  50. Maggenti AR: Nematode higher classification as influenced by species and family concepts. In / Concepts in Nematode Systematics. Edited by: Stone AR, Platt HM, Khalil LF. London: Academic Press; 1983:25鈥?0.
  51. Paramonov AA: A critical review of the suborder Tylenchida (Filipjev, 1934) (Nematoda. Secernentea). / Akad Nauk SSSR Trudy Gel鈥檓int Lab 1967, 18:78鈥?01.
  52. Maggenti AR: Nemic relationships and the origins of plant parasitic nematodes. In / Plant Parasitic Nematodes. Volume 1. Edited by: Zuckerman BM, Mai WF, Rohde RA. New York/London: Academic Press; 1971:65鈥?1.
  53. Andr谩ssy I: / Evolution as a Basis for the Systematization of Nematodes. London: Pitman Publishing; 1976.
  54. Poinar GO Jr: / The Natural History of Nematodes. Englewood Cliffs, NJ: Prentice Hall; 1983.
  55. Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genome sequences. / Nucleic Acids Res 1997, 25:955鈥?64.
  56. 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鈥?882. CrossRef
  57. Wernersson R, Pedersen AG: RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. / Nucleic Acids Res 2003, 31:3537鈥?539. CrossRef
  58. Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. / Bioinformatics 2006, 22:2688鈥?690. CrossRef
  59. Miller MA, Pfeiffer W, Schwartz T: Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In / Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans; 2010:1鈥?.
  60. Shimodaira H, Hasagawa M: Multiple comparisons of log-likelihoods with applications to phylogenetic inference. / Mol Biol Evol 1999, 16:1114鈥?116. CrossRef
  61. Nylander JAA: / MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. 2004. Available from http://www.abc.se/~nylander/
  62. Abascal F, Zardoya R, Posada D: ProtTest: Selection of best-fit models of protein evolution. / Bioinformatics 2007, 24:1104鈥?105.
  
• 作者单位：Tahera Sultana (1)
  Jiyeon Kim (2)
  Sang-Hwa Lee (2)
  Hyerim Han (3)
  Sanghee Kim (4)
  Gi-Sik Min (1)
  Steven A Nadler (5)
  Joogn-Ki Park (2) (6)
  
  1. Department of Biological Sciences, Inha University, Incheon, 402-751, Republic of Korea
  2. Graduate Program in Cell Biology and Genetics, College of Medicine, Chungbuk National University, Cheongju, 361-763, Republic of Korea
  3. Division of Forest Insect Pests and Diseases, Korea Forest Research Institute, Seoul, 130-012, Republic of Korea
  4. Korea Polar Research Institute, Songdo Techno Park, Yeonsu-gu, Incheon, 406-840, Republic of Korea
  5. Department of Entomology and Nematology, University of California, Davis, CA, 95616, USA
  6. Graduate Program in Cell Biology and Genetics and Department of Parasitology, College of Medicine, Chungbuk National University, Cheongju, 361-763, Republic of Korea
  

文摘

Background The nematode infraorder Tylenchomorpha (Class Chromadorea) includes plant parasites that are of agricultural and economic importance, as well as insect-associates and fungal feeding species. Among tylenchomorph plant parasites, members of the superfamily Tylenchoidea, such as root-knot nematodes, have great impact on agriculture. Of the five superfamilies within Tylenchomorpha, one (Aphelenchoidea) includes mainly fungal-feeding species, but also some damaging plant pathogens, including certain Bursaphelenchus spp. The evolutionary relationships of tylenchoid and aphelenchoid nematodes have been disputed based on classical morphological features and molecular data. For example, similarities in the structure of the stomatostylet suggested a common evolutionary origin. In contrast, phylogenetic hypotheses based on nuclear SSU ribosomal DNA sequences have revealed paraphyly of Aphelenchoidea, with, for example, fungal-feeding Aphelenchus spp. within Tylenchomorpha, but Bursaphelenchus and Aphelenchoides spp. more closely related to infraorder Panagrolaimomorpha. We investigated phylogenetic relationships of plant-parasitic tylenchoid and aphelenchoid species in the context of other chromadorean nematodes based on comparative analysis of complete mitochondrial genome data, including two newly sequenced genomes from Bursaphelenchus xylophilus (Aphelenchoidea) and Pratylenchus vulnus (Tylenchoidea). Results The complete mitochondrial genomes of B. xylophilus and P. vulnus are 14,778 bp and 21,656 bp, respectively, and identical to all other chromadorean nematode mtDNAs in that they contain 36 genes (lacking atp8) encoded in the same direction. Their mitochondrial protein-coding genes are biased toward use of amino acids encoded by T-rich codons, resulting in high A+T richness. Phylogenetic analyses of both nucleotide and amino acid sequence datasets using maximum likelihood and Bayesian methods did not support B. xylophilus as most closely related to Tylenchomorpha (Tylenchoidea). Instead, B. xylophilus, was nested within a strongly supported clade consisting of species from infraorders Rhabditomorpha, Panagrolaimomorpha, Diplogasteromorpha, and Ascaridomorpha. The clade containing sampled Tylenchoidea (P. vulnus, H. glycines, and R. similis) was sister to all analyzed chromadoreans. Comparison of gene arrangement data was also consistent with the phylogenetic relationships as inferred from sequence data. Alternative tree topologies depicting a monophyletic grouping of B. xylophilus (Aphelenchoidea) plus Tylenchoidea, Tylenchoidea plus Diplogasteromorpha (Pristionchus pacificus), or B. xylophilus plus Diplogasteromorpha were significantly worse interpretations of the mtDNA data. Conclusions Phylogenetic trees inferred from nucleotide and amino acid sequences of mtDNA coding genes are in agreement that B. xylophilus (the single representative of Aphelenchoidea) is not closely related to Tylenchoidea, indicating that these two groups of plant parasites do not share an exclusive most recent common ancestor, and that certain morphological similarities between these stylet-bearing nematodes must result from convergent evolution. In addition, the exceptionally large mtDNA genome size of P. vulnus, which is the largest among chromadorean nematode mtDNAs sequenced to date, results from lengthy repeated segments in non-coding regions.