Transcriptomes of Plant-Parasitic Nematodes

  • Joachim Jacob
  • Makedonka Mitreva


Undoubtedly, transcriptomic analysis has contributed significantly to the understanding of the molecular basis of parasitism by plant-parasitic nematodes. In this chapter we will review the contributions by this approach. We will discuss the generation of EST sequences and their characteristics. We provide a summary of generally applied bioinformatics processing step to reach the goal of increasing the understanding of the parasitism process at the molecular level and host-parasite interactions. Herewith, useful tools and software are being referenced to. The selection of tools described in this chapter is not all inclusive, but rather reflects those used by the authors at the time of writing. We discuss the results obtained from a pan-phylum comparison of EST data, before ending with thoughts about future developments in the field of transcriptomics.


Parasitic Nematode Nematode Species Plant Parasitic Nematode Parasitism Gene Pharyngeal Gland 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud M-C, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Segurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso M-N, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotech 26:909–915CrossRefGoogle Scholar
  2. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995PubMedGoogle Scholar
  3. Bellafiore S, Shen Z, Rosso M-N, Abad P, Shih P, Briggs SP (2008) Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathog 4:e1000192PubMedCrossRefGoogle Scholar
  4. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795PubMedCrossRefGoogle Scholar
  5. Bird DM, Opperman CH (2009) The secret(ion) life of worms. Genome Biol 10:205PubMedCrossRefGoogle Scholar
  6. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676PubMedCrossRefGoogle Scholar
  7. Curtis RH (2007) Plant parasitic nematode proteins and the host parasite interaction. Brief funct Genomic Proteomic 6:50–58PubMedCrossRefGoogle Scholar
  8. Dautova M, Rosso MN, Abad P, Gommers FJ, Bakker J, Smant G (2001) Single pass cDNA sequencing—a powerful tool to analyse gene expression in preparasitic juveniles of the southern root-knot nematode Meloidogyne incognita. Nematology 3:129–139CrossRefGoogle Scholar
  9. Davis EL, Hussey RS, Baum TJ (2004) Getting to the roots of parasitism by nematodes. Trends Parasitol 20:134–141PubMedCrossRefGoogle Scholar
  10. De Boer JM, Overmars H, Pomp HR, Davis EL, Zilverentant JF, Goverse A, Smant G, Stokkermans J, Hussey RS, Gommers FJ, Bakker J, Schots A (1996a) Production an characterisation of monoclonal antibodies to antigens from second stage juveniles of the potato cyst nematode Globodera rostochiensis. Fund App Nematol 19:545–554Google Scholar
  11. De Boer JM, Smant G, Goverse A, Davis EL, Overmars HA, Pomp H, van Gent-Pelzer M, Zilverentant JF, Stokkermans JP, Hussey RS, Gommers FJ, Bakker J, Schots A (1996b) Secretory granule proteins from the subventral esophageal glands of the potato cyst nematode identified by monoclonal antibodies to a protein fraction from second-stage juveniles. Mol Plant Microbe Interact 9:39–46CrossRefGoogle Scholar
  12. De Boer JM, McDermott JP, Davis EL, Hussey RS, Smant G, Baum TJ (2002) Cloning of a putative pectate lyase gene expressed in the subventral esophageal glands of Heterodera glycines. J Nematol 33:9–11Google Scholar
  13. Ding X, Shields J, Allen R, Hussey RS (2000) Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol 30:77–81PubMedCrossRefGoogle Scholar
  14. Doyle EA, Lambert KN (2002) Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Mol Plant Microbe Interact 15:549–556PubMedCrossRefGoogle Scholar
  15. Droege M, Hill B (2008) The genome sequencer FLX(TM) system–longer reads, more applications, straight forward bioinformatics and more complete data sets. J Biotechnol 136:3–10PubMedCrossRefGoogle Scholar
  16. Elling AA, Davis EL, Hussey RS, Baum TJ (2007a) Active uptake of cyst nematode parasitism proteins into the plant cell nucleus. Int J Parasitol 37:1269–1279CrossRefGoogle Scholar
  17. Elling A, Mitreva M, Recknor J, Gai X, Martin J, Maier T, McDermott J, Hewezi T, McK Bird D, Davis E, Hussey R, Nettleton D, McCarter J, Baum T (2007b) Divergent evolution of arrested development in the dauer stage of Caenorhabditis elegans and the infective stage of Heterodera glycines. Genome Biol 8:R211CrossRefGoogle Scholar
  18. Elling AA, Mitreva M, Gai X, Martin J, Recknor J, Davis EL, Hussey RS, Nettleton D, McCarter JP, Baum TJ (2009) Sequence mining and transcript profiling to explore cyst nematode parasitism. BMC Genomics 10:58PubMedCrossRefGoogle Scholar
  19. Fioretti L, Warry A, Porter A, Haydock P, Curtis R (2001) Isolation and localisation of an annexin gene (gp-nex) from the potato cyst nematode, Globodera pallida. Nematology 3:45–54CrossRefGoogle Scholar
  20. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001) Molecular characterisation and expression of two venom allergen-like protein genes in Heterodera glycines. Int J Parasitol 31:1617–1625PubMedCrossRefGoogle Scholar
  21. Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant Microbe Interact 16:720–726PubMedCrossRefGoogle Scholar
  22. Giebel J (1973) Biochemical mechanisms of plant resistance to nematodes: A review. J Nematol 6:175–184Google Scholar
  23. Givnish TJ, Evans TM, Zjhra ML, Patterson TB, Berry PE, Sytsma KJ (2000) Molecular evolution, adaptive radiation, and geographic diversification in theamphiatlantic family Rapateaceae: evidence from ndhF sequences and morphology. Int J Org Evol 54:1915–1937Google Scholar
  24. Goellner M, Smant G, de Boer JM, Baum TJ, Davis EL (2000) Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. J Nematol 32:154–165PubMedGoogle Scholar
  25. Haegeman A, Vanholme B, Jacob J, Vandekerckhove TTM, Claeys M, Borgonie G, Gheysen G (2009) An endosymbiotic bacterium in a plant-parasitic nematode: Member of a new Wolbachia supergroup. Int J Parasitol 39:1045–1054PubMedCrossRefGoogle Scholar
  26. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, De La Cruz N, Davis P, Duesbury M, Fang R, Fernandes J, Han M, Kishore R, Lee R, Muller H-M, Nakamura C, Ozersky P, Petcherski A, Rangarajan A, Rogers A, Schindelman G, Schwarz EM, Tuli MA, Van Auken K, Wang D, Wang X, Williams G, Yook K, Durbin R, Stein LD, Spieth J, Sternberg PW (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 38:D463–D467PubMedCrossRefGoogle Scholar
  27. Huang GZ, Gao BL, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 16:376–381PubMedCrossRefGoogle Scholar
  28. Huang GZ, Dong RH, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2004) Use of solid-phase subtractive hybridization for the identification of parasitism gene candidates from the root-knot nematode Meloidogyne incognita. Mol Plant Pathol 5:217–222PubMedCrossRefGoogle Scholar
  29. Jacob J (2009) Plant-parasitic nematodes: from genomics to functional analysis of parasitism genes. PhD Thesis, Ghent University, Faculty of Bioscience Engineering, Ghent, BelgiumGoogle Scholar
  30. Jacob J, Mitreva M, Vanholme B, Gheysen G (2008) Exploring the transcriptome of the burrowing nematode Radopholus similis. Mol Genet Genomics 280:1–17, PMID: 18386064PubMedCrossRefGoogle Scholar
  31. Jacob J, Vanholme B, Van Leeuwen T, Gheysen G (2009) A unique genetic code change in the mitochondrial genome of the parasitic nematode Radopholus similis. BMC Res Notes 2:192PubMedCrossRefGoogle Scholar
  32. Jang CS, Jung JH, Yim WC, Lee BM, Seo YW, Kim W (2007) Divergence of genes encoding non-specific lipid transfer proteins in the poaceae family. Mol Cells 24:215–223PubMedGoogle Scholar
  33. Jones JT, Furlanetto C, Kikuchi T (2003) Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes. Nematology 7:641–646CrossRefGoogle Scholar
  34. Jones JT, Reavy B, Smant G, Prior AE (2004) Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47–54PubMedCrossRefGoogle Scholar
  35. Karim N, Jones J, Okada H, Kikuchi T (2009) Analysis of expressed sequence tags and identification of genes encoding cell-wall-degrading enzymes from the fungivorous nematode Aphelenchus avenae. BMC Genomics 10:525PubMedCrossRefGoogle Scholar
  36. Kikuchi T, Shibuya H, Jones JT (2005) Molecular and biochemical characterization of an endo-beta-1,3-glucanase from the pinewood nematode Bursaphelenchus xylophilus acquired by horizontal gene transfer from bacteria. Biochem J 389:117–125PubMedCrossRefGoogle Scholar
  37. Kikuchi T, Aikawa T, Kosaka H, Pritchard L, Ogura N, Jones JT (2007) Expressed sequence tag (EST) analysis of the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus. Mol Biochem Parasitol 155:9–17PubMedCrossRefGoogle Scholar
  38. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–298PubMedCrossRefGoogle Scholar
  39. Lambert KN, Allen KD, Sussex IM (1999) Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant Microbe Interact 12:328–336PubMedCrossRefGoogle Scholar
  40. Lilley CJ, Urwin PE, Atkinson HJ (1999) Characterization of plant nematode genes: identifying targets for a transgenic defence. Parasitology 118:S63–S72PubMedCrossRefGoogle Scholar
  41. Liu D, Graber J (2006) Quantitative comparison of EST libraries requires compensation for systematic biases in cDNA generation. BMC Bioinformatics 7:77PubMedCrossRefGoogle Scholar
  42. Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141PubMedCrossRefGoogle Scholar
  43. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen Y-J, Chen Z, 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 J-B, 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 P, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  44. Martin J, Abubucker S, Wylie T, Yin Y, Wang Z, Mitreva M (2009) update 2008: improvements enabling more efficient data mining and comparative nematode genomics. Nucleic Acids Res 37:D571–D578PubMedCrossRefGoogle Scholar
  45. Mitreva M, Mardis ER (2009) Large-scale sequencing and analytical processing of ESTs. Methods Mol Biol 533:153–187PubMedCrossRefGoogle Scholar
  46. Mitreva M, McCarter JP, Martin J, Dante M, Wylie T, Chiapelli B, Pape D, Clifton SW, Nutman TB, Waterston RH (2004a) Comparative genomics of gene expression in the parasitic and free-living nematodes Strongyloides stercoralis and Caenorhabditis elegans. Genome Res 14:209–220CrossRefGoogle Scholar
  47. Mitreva M, Elling AA, Dante M, Kloek AP, Kalyanaraman A, Aluru S, Clifton SW, Bird DM, Baum TJ, McCarter JP (2004b) A survey of SL1-spliced transcripts from the root-lesion nematode Pratylenchus penetrans. Mol Genet Genomics 272:138–148CrossRefGoogle Scholar
  48. Mitreva M, McCarter JP, Arasu P, Hawdon J, Martin J, Dante M, Wylie T, Xu J, Stajich JE, Kapulkin W, Clifton SW, Waterston RH, Wilson RK (2005) Investigating hookworm genomes by comparative analysis of two Ancylostoma species. BMC Genomics 6:58PubMedCrossRefGoogle Scholar
  49. Mitreva M, Wendl M, Martin J, Wylie T, Yin Y, Larson A, Parkinson J, Waterston R, McCarter J (2006) Codon usage patterns in Nematoda: analysis based on over 25 million codons in thirty-two species. Genome Biol 7:R75CrossRefGoogle Scholar
  50. Mitreva-Dautova M, Roze E, Overmars H, de Graaff L, Schots A, Helder J, Goverse A, Bakker J, Smant G (2006) A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita. Mol Plant Microbe Interact 19:521–529PubMedCrossRefGoogle Scholar
  51. Munoz ET, Bogarad LD, Deem MW (2004) Microarray and EST database estimates of mRNA expression levels differ: the protein length versus expression curve for C. elegans. BMC Genomics 5:30PubMedCrossRefGoogle Scholar
  52. Nagaraj SH, Deshpande N, Gasser RB, Ranganathan S (2007) ESTExplorer: an expressed sequence tag (EST) assembly and annotation platform. Nucleic Acids Res W143–W147Google Scholar
  53. Nagaraj SH, Gasser RB, Ranganathan S (2008) Needles in the EST Haystack: Large-scale identification and analysis of Excretory-Secretory (ES) proteins in parasitic nematodes using Expressed Sequence Tags (ESTs). PLoS Negl Trop Dis 2:e301PubMedCrossRefGoogle Scholar
  54. Olsen A, Skriver K (2003) Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends Plant Sci 8:55–57PubMedCrossRefGoogle Scholar
  55. Opperman CH, Bird DM (1998) The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes. Curr Opin Plant Biol 1:342–346PubMedCrossRefGoogle Scholar
  56. Opperman CH, Bird DM, Williamson VM, Rokhsar DS, Burke M, Cohn J, Cromer J, Diener S, Gajan J, Graham S, Houfek TD, Liu Q, Mitros T, Schaff J, Schaffer R, Scholl E, Sosinski BR, Thomas VP, Windham E (2008) Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proc Natl Acad Sci USA 105:14802–14807PubMedCrossRefGoogle Scholar
  57. Panhuis TM, Clark NL, Swanson WJ (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc B: Biol Sci 361:261–268CrossRefGoogle Scholar
  58. Parkinson J, Blaxter ML (2003) SimiTri–visualizing similarity relationships for groups of sequences. Bioinformatics 19:390–395PubMedCrossRefGoogle Scholar
  59. Parkinson J, Anthony A, Wasmuth J, Schmid R, Hedley A, Blaxter M (2004a) PartiGene—constructing partial genomes. Bioinformatics 20:1398–1404CrossRefGoogle Scholar
  60. Parkinson J, Mitreva M, Whitton C, Thomson M, Daub J, Martin J, Hall N, Barrell B, Waterston RH, McCarter JP, Blaxter M (2004b) A transcriptomic analysis of the phylum Nematoda. Nat Genet 36:1259–1267CrossRefGoogle Scholar
  61. Parkinson J, Whitton C, Schmid R, Thomson M, Blaxter M (2004c) NEMBASE: a resource for parasitic nematode ESTs. Nucleic Acids Res 32:D427–D430CrossRefGoogle Scholar
  62. Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067PubMedCrossRefGoogle Scholar
  63. Peng J, Huang CH (2006) Rh proteins vs Amt proteins: an organismal and phylogenetic perspective on CO2 and NH3 gas channels. Transfus Clin Biol 13:85–94PubMedCrossRefGoogle Scholar
  64. Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652PubMedCrossRefGoogle Scholar
  65. Popeijus H, Blok VC, Cardle L, Bakker E, Phillips MS, Helder J, Smant G, Jones JT (2000) Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and G. pallida using the expressed sequence tag approach. Nematology 2:567–574CrossRefGoogle Scholar
  66. Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L, Cooper A, Kennedy MW (2001) A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochem J 356:387–394PubMedCrossRefGoogle Scholar
  67. Qin L, Overmars H, Helder J, Popeijus H, van der Voort JR, Groenink W, van Koert P, Schots A, Bakker J, Smant G (2000) An efficient cDNA-AFLP-based strategy for the identification of putative pathogenicity factors from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact 13:830–836PubMedCrossRefGoogle Scholar
  68. Robinson MW, Connolly B (2005) Proteomic analysis of the excretory-secretory proteins of the Trichinella spiralis L1 larva, a nematode parasite of skeletal muscle. Proteomics 5:4525–4532PubMedCrossRefGoogle Scholar
  69. Rosso MN, Favery B, Piotte C, Arthaud L, De Boer JM, Hussey RS, Bakker J, Baum TJ, Abad P (1999) Isolation of a cDNA encoding a beta-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol Plant Microbe Interact 12:585–591PubMedCrossRefGoogle Scholar
  70. Roze E, Hanse B, Mitreva M, Vanholme B, Bakker J, Smant G (2008) Mining the secretome of the root-knot nematode Meloidogyne chitwoodi for candidate parasitism genes. Mol Plant Pathol 9:1–10PubMedGoogle Scholar
  71. Schiex T, Gouzy J, Moisan A, de Oliveira Y (2003) FrameD: a flexible program for quality check and gene prediction in prokaryotic genomes and noisy matured eukaryotic sequences. Nucleic Acids Res 31:3738–3741PubMedCrossRefGoogle Scholar
  72. Simon SA, Zhai J, Nandety RS, McCormick KP, Zeng J, Mejia D, Meyers BC (2009) Short-Read sequencing technologies for transcriptional analyses. Ann Rev Plant Biol 60:305–333CrossRefGoogle Scholar
  73. Smant G, Stokkermans JP, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci U S A 95:4906–4911PubMedCrossRefGoogle Scholar
  74. Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6:175–182PubMedGoogle Scholar
  75. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A et al. (2003) The genome sequence of Caenorhabditis briggsae: A platform for comparative genomics. PLoS Biol 1:E45PubMedCrossRefGoogle Scholar
  76. The Gene Ontology C (2008) The gene ontology project in 2008. Nucleic Acids Res 36:D440–D444CrossRefGoogle Scholar
  77. Tucker ML, Xue P, Raina A, Ehrenfried ML, Asif M, Thai VK (2005) Characterization of several Heterodera glycines mRNAs that encode small proteins with putative signal peptides. J Nematol 37:422–428PubMedGoogle Scholar
  78. Uehara T, Kushida A, Momota Y (2001) PCR-based cloning of two beta-1,4-endoglucanases from the root-lesion nematode Pratylenchus penetrans. Nematology 3:335–41CrossRefGoogle Scholar
  79. Vanholme B, De Meutter J, Tytgat T, Van Montagu M, Coomans A, Gheysen G (2004) Secretions of plant-parasitic nematodes: a molecular update. Gene 332:13–27PubMedCrossRefGoogle Scholar
  80. Vanholme B, Mitreva M, Van Criekinge W, Logghe M, Bird D, McCarter J, Gheysen G (2006) Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii. Parasitol Res 98:414–424PubMedCrossRefGoogle Scholar
  81. Wang J-P, Lindsay B, Cui L, Wall PK, Marion J, Zhang J, dePamphilis C (2005) Gene capture prediction and overlap estimation in EST sequencing from one or multiple libraries. BMC Bioinformatics 6:300PubMedCrossRefGoogle Scholar
  82. Wang X, Allen R, Ding X, Goellner M, Maier T, de Boer JM, Baum TJ, Hussey RS, Davis EL (2001) Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 14:536–544PubMedCrossRefGoogle Scholar
  83. Wang Z, Martin J, Abubucker S, Yin Y, Gasser R, Mitreva M (2009) Systematic analysis of insertions and deletions specific to nematode proteins and their proposed functional and evolutionary relevance. BMC Evol Biol 9:23PubMedCrossRefGoogle Scholar
  84. Wang Z, Abubucker S, Martin J, Wilson RK, Hawdon J, Mitreva M (2010) Characterizing Ancylostoma caninum transcriptome and exploring nematode parasitic adaptation. BMC Genomics 11:307PubMedCrossRefGoogle Scholar
  85. Wasmuth JD, Blaxter ML (2004) prot4EST: translating expressed sequence tags from neglected genomes. BMC Bioinformatics 5:187PubMedCrossRefGoogle Scholar
  86. Wasmuth J, Schmid R, Hedley A, Blaxter M (2008) On the extent and origins of genic novelty in the phylum Nematoda. PloS Negl Trop Dis 2:e258PubMedCrossRefGoogle Scholar
  87. Wylie T, Martin J, Dante M, Mitreva M, Clifton SW, Chinwalla A, Waterston RH, Wilson RK, McCarter JP (2004) a tool for Navigating Sequences from Parasitic and Free-Living Nematodes. Nucleic Acids Res 32:D423–D426PubMedCrossRefGoogle Scholar
  88. Wylie T, Martin J, Abubucker S, Yin Y, Messina D, Wang Z, McCarter J, Mitreva M (2008) NemaPath: online exploration of KEGG-based metabolic pathways for nematodes. BMC Genomics 9:525PubMedCrossRefGoogle Scholar
  89. Yan J, Marr TG (2005) Computational analysis of 3′-ends of ESTs shows four classes of alternative polyadenylation in human, mouse, and rat. Genome Res 15:369–375PubMedCrossRefGoogle Scholar
  90. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–297PubMedCrossRefGoogle Scholar
  91. Yin Y, Martin J, Abubucker S, Wang Z, Wyrwicz L, Rychlewski L, McCarter J, Wilson R, Mitreva M (2009) Molecular determinants archetypical to the phylum Nematoda. BMC Genomics 10:114PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Bioinformatics Training and Service facility, VIBGentBelgium
  2. 2.Department of GeneticsWashington University School of MedicineSt. Louis, MO.USA

Personalised recommendations