Exploring the transcriptome of the burrowing nematode Radopholus similis

Molecular Genetics and Genomics

Volumn 280, Issue 1, 2008, Pages 1-17

  Jacob, Joachim ^a   Mitreva, Makedonka ^b   Vanholme, Bartel ^a   Gheysen, Godelieve ^a  

^a GHENT UNIVERSITY   (Belgium)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endoparasitic migratory nematode; Expressed sequence tag analysis; G + C content; Parasitism; Trans spliced leader; Wolbachia

Indexed keywords

AMINO ACID; CYTOSINE; DNA; GUANINE; TRANSCRIPTOME;

ARTICLE; DNA SEQUENCE; EXPRESSED SEQUENCE TAG; GENBANK; GENE CLUSTER; GENETIC ANALYSIS; GENETIC CODE; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE CONTROL; PARASITEMIA; PREDICTION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN LOCALIZATION; RADOPHOLUS SIMILIS; REPRODUCTION; SEQUENCE HOMOLOGY; SURVIVAL TIME; TRANSCRIPTOMICS; UNINDEXED SEQUENCE;

ANIMALS; DATABASES, GENETIC; GENE EXPRESSION PROFILING; GENES, HELMINTH; HOST-PARASITE INTERACTIONS; NEMATODA; RNA, HELMINTH; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; WOLBACHIA;

NEMATODA; RADOPHOLUS SIMILIS; WOLBACHIA;

EID: 41449095270     PISSN: 16174615     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00438-008-0340-7     Document Type: Article

References (77)

1. Aaronson JS, Eckman B, Blevins RA, Borkowski JA, Myerson J, Imran S, Elliston KO (1996) Toward the development of a gene index to the human genome: an assessment of the nature of high-throughput EST sequence data. Genome Res 6:829-845
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
3. Atkinson H, Grimwood S, Johnston K, Green J (2004) Prototype demonstration of transgenic resistance to the nematode Radopholus similis conferred on banana by a cystatin. Transgenic Res 13:135-142
4. Bakhetia M, Charlton WL, Urwin PE, McPherson MJ, Atkinson HJ (2005) RNA interference and plant parasitic nematodes. Trends Plant Sci 10:362-367
5. Basak S, Ghosh TC (2005) On the origin of genomic adaptation at high temperature for prokaryotic organisms. Biochem Biophys Res Commun 330:629-632
6. Belle EM, Smith N, Eyre-Walker A (2002) Analysis of the phylogenetic distribution of isochores in vertebrates and a test of the thermal stability hypothesis. J Mol Evol 55:256-363
7. Bentwich I, Avniel A, Karov Y, Aharonov R, Gilad S, Barad O, Barzilai A, Einat P, Einav U, Meiri E, Sharon E, Spector Y, Bentwich Z (2005) Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 37:766-770
8. Berriman M, Aslett M, Hall N, Ivens A (2001) Parasites are GO. Trends Parasitol 17:463-464
9. Blumenthal T, Evans D, Link CD, Guffanti A, Lawson D, Thierry-Mieg J, Thierry-Mieg D, Chiu WL, Duke K, Kiraly M, Kim SK (2002) A global analysis of Caenorhabditis elegans operons. Nature 417:851-854
10. Boguski MS, Lowe TMJ, Tolstoshev CM (1993) dbEST - database for "expressed sequence tags". Nat Genet 4:332-333
11. Chen W-H, Wang X-X, Lin W, He X-W, Wu Z-Q, Lin Y, Hu S-N, Wang X-N (2006) Analysis of 10,000 ESTs from lymphocytes of the cynomolgus monkey to improve our understanding of its immune system. BMC Genomics 7:82. doi: 10.1186/1471-2164-7-82
12. 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 21:3674-3676
13. Cutter AD, Wasmuth JD, Blaxter ML (2006) The evolution of biased codon and amino acid usage in nematode genomes. Mol Biol Evol 23:2303-2315
14. Dubreuil G, Magliano M, Deleury E, Abad P, Rosso MN (2007) Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol 176:426-436
15. Elsen A, Jain SM, Swennen R, De Waele D (2004) Recent developments in early in vitro screening for resistance against migratory endoparasitic nematodes in Musa. Banana improvement: cellular, molecular biology, and induced mutations. Proceedings of a meeting held in Leuven, Belgium, 24-28 September 2001, Science publishers, Inc
16. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953-971
17. Foster J, Ganatra M, Kama I, Ware J, Makarova K, Ivanova N, Bhattacharyya A, Kapatral V, Kumar S, Posfai J, Vincze T, Ingram J, Moran L, Lapidus A, Omelchenko M, Kyrpides N, Ghedin E, Wang S, Goltsman E, Joukov V, Ostrovskaya O, Tsukerman K, Mazur M, Comb D, Koonin E, Slatko B (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLOS Biol 3:0599-0614
18. Garofalo A, Kennedy MW, Bradley JE (2003) The FAR proteins of parasitic nematodes: their possible involvement in the pathogenesis of infection and the use of Caenorhabditis elegans as a model system to evaluate their function. Med Microbiol Immunol 192:47-52
19. Gheysen G, Vanholme B (2007) RNAi from plants to nematodes. Trends Biotechnol 25:89-92
20. Gissi C, Pesole G (2003) Transcript mapping and genome annotation of Ascidian mtDNA using EST data. Genome Res 13:2203-2212
21. Guiliano DB, Blaxter ML (2006) Operon conservation and the evolution of trans-splicing in the phylum Nematoda. PLoS Genet 2:e198. doi: 10.1371/journal.pgen.0020198
22. Haegeman A, Jacob J, Vanholme B, Kyndt T, Gheysen G (2008) A family of GHF5 endo-1,4-beta-glucanases in the migratory plant-parasitic nematode Radopholus similis. Plant Pathol (in press). doi: 10.1111/j.1365-3059.2007. 01814.x
23. Hammond MP, Bianco AE (1992) Genes and genomes of parasitic nematodes. Parasitol Today 8:299-305
24. He Y, Jones J, Armstrong M, Lamberti F, Moens M (2005) The mitochondrial genome of Xiphinema americanum sensu stricto (Nematoda: Enoplea): considerable economization in the length and structural features of encoded genes. J Mol Evol 61:819-833
25. Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378-379
26. Hise AG, Gillette-Ferguson I, Pearlman E (2004) The role of endosymbiotic Wolbachia bacteria in filarial disease. Cell Microbiol 6:97-104
27. Hotopp JCD, Clark ME, Oliveira DCSG, Foster JM, Fischer P, Torres MCM, Giebel JD, Kumar N, Ishmael N, Wang S, Ingram J, Nene RV, Shepard J, Tomkins J, Richards S, Spiro DJ, Ghedin E, Slatko BE, Tettelin H, Werren JH (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753-1756
28. Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868-877
29. Iseli C, Jongeneel V, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 138-148
30. Jabbari K, Bernardi G (2004) Body temperature and evolutionary genomics of vertebrates: a lesson from the genomes of Takifugu rubripes and Tetraodon nigroviridis. Gene 333:179-181
31. Jacob J, Vanholme B, Haegeman A, Gheysen G (2007) Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 402:9-19
32. Jones JT, Reavy B, Smant G, Prior AE (2004) Glutathione peroxidases of the potato cyst nematode Globodera rostochiensis. Gene 324:47-54
33. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231-237
34. Kennedy MW, Allen JE, Wright AS, McCruden AB, Cooper A (1995) The gp15/400 polyprotein antigen of Brugia malayi binds fatty acids and retinoids. Mol Biochem Parasitol 71:41-50
35. 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 115:9-17
36. Kramer L, Passeri B, Corona S, Simoncini L, Casiraghi M (2003) Immunohistochemical/immunogold detection and distribution of the endosymbiont Wolbachia of Dirofilaria immitis and Brugia pahangi using a polyclonal antiserum raised against WSP (Wolbachia surface protein). Parasitol Res 89:381-386
37. Ledger TN, Jaubert S, Bosselut N, Abad P, Rosso M-N (2006) Characterization of a new beta-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 382:121-128
38. Leroy S, Bouamer S, Morand S, Fargette M (2007) Genome size of plant-parasitic nematodes. Nematology 9:449-450
39. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769-773
40. Liu D, Graber J (2006) Quantitative comparison of EST libraries requires compensation for systematic biases in cDNA generation. BMC Bioinformatics 7:77. doi: 10.1186/1471-2105-7-77
41. Liu F, Lu J, Hu W, Wang SY, Cui SJ, Chi M, Yan Q, Wang XR, Song HD, Xu XN, Wang JJ, Zhang XL, Zhang X, Wang ZQ, Xue CL, Brindley PJ, McManus DP, Yang PY, Feng Z, Chen Z, Han ZG (2006) New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PLoS Pathog 2:e29. doi: 10.1371/journal.ppat.0020029
42. Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787-3793
43. McCarter JP, Mitreva MD, Martin J, Dante M, Wylie T, Rao U, Pape D, Bowers Y, Theising B, Murphy CV, Kloek AP, Chiapelli BJ, Clifton SW, Bird DM, Waterston RH (2003) Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol 4:R26. doi: 10.1186/gb-2003-4-4- r26
44. Mitreva M, Elling AA, Dante M, Kloek AP, Kalyanaraman A, Aluru S, Clifton SW, Bird DM, Baum TJ, McCarter JP (2004) A survey of SL1-spliced transcipts from the root-lesion nematode Pratylenchus penetrans. Mol Genet Genomics 272:138-148
45. Mitreva M, Wendl MC, Martin J, Wylie T, Yin Y, Larson A, Parkinson J, Waterston RH, McCarter JP (2006) Codon usage patterns in Nematoda: analysis based on over 25 million codons in thirty-two species. Genome Biol 7:R75. doi: 10.1186/gb-2006-7-8-r75
46. Munoz E, Bogarad L, Deem M (2004) Microarray and EST database estimates of mRNA expression levels differ: the protein length versus expression curve for C. elegans. BMC Genomics 5:30-30
47. Nagaraj SH, Deshpande N, Gasser RB, Ranganathan S (2007a) ESTExplorer: an expressed sequence tag (EST) assembly and annotation platform. Nucleic Acids Res 35:W143-W147. doi: 10.1093/nar/gkm378
48. Nagaraj SH, Gasser RB, Ranganathan S (2007b) A hitchhiker's guide to expressed sequence tag (EST) analysis. Brief Bioinform 8:6-21
49. Nishikawa T, Nagai K (1996) EST error analysis in a large-scale GenBank search of ESTs using rapid-identity searching program for DNA sequences. In: Genome mapping and sequencing, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
50. Noel GR, Atibalentja N (2006) "Candidatus Paenicardinium endonii", an endosymbiont of the plant-parasitic nematode Heterodera glycines (Nemata: Tylenchida), affiliated to the phylum Bacteroidetes. Int J Syst Evol Microbiol 56:1697-1702
51. O'Bannon JH (1977) Worldwide dissemination of Radopholus similis and its importance in crop production. J Nematol 9:16-25
52. Opperman CH, Bird DM (1998) The soybean cyst nematode, Heterodera glycines: a genetic model system for the study of plant-parasitic nematodes. Current Opin Plant Biol 1:342-346
53. 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 19:651-652
54. Price NS (2006) The banana burrowing nematode, Radopholus similis (Cobb) Thorne, in the lake Victoria region of East Africa: its introduction, spread and impact. Nematology 8:801-817
55. 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 356:387-394
56. Ranganathan S, Nagaraj SH, Hu M, Strube C, Schnieder T, Gasser RB (2007) A transcriptomic analysis of the adult stage of the bovine lungworm, Dityocaulus viviparus. BMC Genomics 8:311. doi: 10.1186/1471-2164-8-311
57. Richly E, Leister D (2004) NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 21:1081-1084
58. Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E, Ariyanayagam MR, Ferguson MAJ, Fairlamb A, Jones JT (2000) Cloning, expression and functional characterisation of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Mol Biochem Parasitol 111:41-49
59. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127:1193-1207
60. Sarah JL, Pinochet J, Stanton J (1996) The burrowing nematode of bananas, Radopholus similis Cobb, 1913. International network for the improvement of banana and plantain, Montpellier, France
61. 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 31:3738-3741
62. Schwarz EM, Antoshechkin I, Bastiani C, Bieri T, Blasiar D, Canaran P, Chan J, Chen N, Chen WJ, Davis P, Fiedler TJ, Girard L, Harris TW, Kenny EE, Kishore R, Lawson D, Lee R, Muller HM, Nakamura C, Ozersky P, Petcherski A, Rogers A, Spooner W, Tuli MA, Van Auken K, Wang D, Durbin R, Spieth J, Stein LD, Sternberg PW (2006) WormBase: better software, richer content. Nucleic Acids Res 34:D475-D478
63. Smant G, Stokkermans JPWG, Yan YT, de Boer JM, Baum TJ, Wang XH, 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. PNAS 95:4906-4911
64. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D'Eustachio P, Fitch DHA, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, Stajich JE, Wei C, Willey D, Wilson RK, Durbin R, Waterston RH (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLOS Biol 1:e45-e45
65. Stoffelen R, Verlinden R, Pinochet J, Swennen RL, De Waele D (2000) Host plant response of Fusarium wilt resistant Musa genotypes to Radopholus similis and Pratylenchus coffeae. Int J Pest Manag 46:289-293
66. Taylor MJ, Bilo K, Cross HF, Archer JP, Underwood AP (1999) 16S rDNA phylogeny and ultrastructural characterization of Wolbachia intracellular bacteria of the filarial nematodes Brugia malayi, B. pahangi, and Wuchereria bancrofti. Exp Parasitol 91:356-361
67. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
68. Tytgat T, Vercauteren I, Vanholme B, De Meutter J, Vanhoutte I, Gheysen G, Borgonie G, Coomans A, Gheysen G (2005) An SXP/RAL-2 protein produced by the subventral pharyngeal glands in the plant parasitic root-knot nematode Meloidogyne incognita. Parasitol Res 95:50-54
69. United Nations Environment Programme (1995) Report of the methyl bromide technical options committee. Montreal protocol on substances that deplete the ozone layer
70. Vandekerckhove TTM, Coomans A, Cornelis K, Baert P, Gillis M (2002) Use of the Verrucomicrobia-specific probe EUB338-III and fluorescent in situ hybridization for detection of "Candidatus Xiphinematobacter" cells in nematode hosts. Appl Environ Microbiol 68:3121-3125
71. Wang J-PZ, Lindsay BG, Cui L, Wall PK, Marion J, Zhang J, dePamphilis CW (2006a) Gene capture prediction and overlap estimation in EST sequencing from one or multiple libraries. BMC Bioinformatics 6:300
72. Wang HC, Susko E, Roger AJ (2006b) On the correlation between genomic G + C content and optimal growth temperature in prokaryotes: data quality and confounding factors. Biochem Biophys Res Commun 342:681-684
73. Washietl S, Hofacker IL, Stadler PF (2005) Fast and reliable prediction of noncoding RNAs. PNAS 102:2454-2459
74. Wasmuth JD, Blaxter ML (2004) Prot4EST: translating expressed sequence tags from neglected genomes. BMC Bioinformatics 5:187
75. Wuyts N, Lognay G, Verscheure M, Marlier M, De Waele D, Swennen R (2007) Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). Plant Pathol 56:878-890
76. Wylie T, Martin JC, Dante M, Mitreva MD, Clifton SW, Chinwalla A, Waterston RH, Wilson RK, McCarter JP (2004) Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res 32:D423-D426
77. 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-W297