Gene silencing in root lesion nematodes (Pratylenchus spp.) significantly reduces reproduction in a plant host

Experimental Parasitology

Volumn 133, Issue 2, 2013, Pages 166-178

  Tan, Jo Anne C H ^a   Jones, Michael G K ^a   Fosu Nyarko, John ^a  

^a MURDOCH UNIVERSITY   (Australia)

Author keywords

Calponin; Carrot mini disc culture; Double stranded RNA (dsRNA); Pratylenchus spp.; RNA interference (RNAi); Troponin C

Indexed keywords

CALPONIN; DOUBLE STRANDED RNA; FLUORESCEIN ISOTHIOCYANATE; TROPONIN C;

ARTICLE; CALPONIN GENE; CONTROLLED STUDY; GENE; GENE IDENTIFICATION; GENE SILENCING; GENE TARGETING; GROWTH INHIBITION; HOST RESISTANCE; MOLECULAR DYNAMICS; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PAT 10 GENE; PLANT PATHOGEN INTERACTION; PRATYLENCHUS THORNEI; PRATYLENCHUS ZEAE; PRIORITY JOURNAL; RNA INTERFERENCE; RNA SEQUENCE; SEQUENCE ANALYSIS; TROPONIN C GENE; UNC 87 GENE;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; CALCIUM-BINDING PROTEINS; CROPS, AGRICULTURAL; DAUCUS CAROTA; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GENE SILENCING; MICROFILAMENT PROTEINS; OCTOPAMINE; PLANT DISEASES; REPRODUCTION; RESORCINOLS; RNA, DOUBLE-STRANDED; SACCHARUM; SORGHUM; SPERMIDINE; TRITICUM; TROPONIN C; TYLENCHOIDEA; WESTERN AUSTRALIA;

DAUCUS CAROTA; NEMATODA; PRATYLENCHUS; PRATYLENCHUS THORNEI; PRATYLENCHUS ZEAE; TRITICUM AESTIVUM;

EID: 84871454821     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2012.11.011     Document Type: Article

References (50)

1. Abramoff M.D., Magalhaes P.J., Ram S.J. Image processing with Imge. J. Biophotonics Int. 2004, 11:36-42.
2. Adam M.A.M., Phillips M.S., Jones J.T., Blok V.C. Characterisation of the cellulose-binding protein Mj-cbp-1 of the root knot nematode, Meloidogyne javanica. Physiol. Mol. Plant Pathol. 2008, 72:21-28.
3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
4. Bakhetia M., Charlton W., Atkinson H.J., McPherson M.J. RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol. Plant Microbe Interact. 2005, 18:1099-1106.
5. Bucher G., Scholten J., Klingler M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 2002, 12:R85-R86.
6. Castillo P., Vovlas N. Biology and ecology of Pratylenchus. Pratylenchus (Nematoda: Pratylenchidae): Diagnosis, Biology, Pathogenicity and Management 2008, vol. 6:305-310. Brill, Leiden.
7. Cheng X.-Y., Dai S.-M., Xiao L., Xie B.-Y. Influence of cellulase gene knockdown by dsRNA interference on the development and reproduction of the pine wood nematode, Bursaphelenchus xylophilus. Nematology 2010, 12:225-233.
8. Dalzell J.J., McVeigh P., Warnock N.D., Mitreva M., Bird D.M., Abad P., Fleming C.C., Day T.A., Mousley A., Marks N.J., Maule A.G. RNAi effector diversity in nematodes. PLoS Negl. Trop. Dis. 2011, 5:e1176.
9. Descotte V., Montgomery M.K. Differing susceptibilities to RNAi within the Caenorhabditis clade. Dev. Biol. 2003, 259:466.
10. Dubreuil G., Magliano M., Deleury E., Abad P., Rosso M.N. Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytol. 2007, 176:426-436.
11. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.
12. Fairbairn D., Cavallaro A., Bernard M., Mahalinga-Iyer J., Graham M., Botella J. Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 2007, 226:1525-1533.
13. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
14. Fire A. RNA-triggered gene silencing. Trends Genet. 1999, 15:358-363.
15. Fraser A.G., Kamath R.S., Zipperlen P., Martinez-Campos M., Sohrmann M., Ahringer J. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 2000, 408:325-330.
16. Goetinck S., Waterston R.H. The Caenorhabditis elegans UNC-87 Protein is essential for maintenance, but not assembly, of bodywall muscle. J. Cell Biol. 1994, 127:71-78.
17. Goto D.B., Fosu-Nyarko J., Sakuma F., Sadler J., Flottman-Reid M., Uehara T., Kondo N., Yamaguchi J., Jones M.G.K. In planta observation of live fluorescent plant endoparasitic nematodes during early stages of infection. Nematological Res. 2010, 40:15-19.
18. Haegeman A., Vanholme B., Gheysen G. Characterization of a putative endoxylanase in the migratory plant-parasitic nematode Radopholus similis. Mol. Plant Pathol. 2009, 10:389-401.
19. Haegeman A., Joseph S., Gheysen G. Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Mol. Biochem. Parasitol. 2011, 178:7-14.
20. Huang G., Allen R., Davis E.L., Baum T.J., Hussey R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. USA 2006, 103:14302-14306.
21. Kaplan D.T., Davis E.L. Improved nematode extraction from carrot disk culture. J. Nematol. 1990, 22:399-406.
22. Kennerdell J.R., Carthew R.W. Use of dsRNA-mediated genetic interference to demonstrate that frizzled and frizzled 2 act in the wingless pathway. Cell 1998, 95:1017-1026.
23. Kimber M.J., McKinney S., McMaster S., Day T.A., Fleming C.C., Maule A.G. Flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J. 2007, 21:1233-1243.
24. Krusberg L.R. Studies on the culturing and parasitism of plant-parasitic nematodes, in particular Ditylenchus dipsaci and Aphelenchoides ritzeiwabosi on alfalfa tissues. Nematologica 1961, 6:181-200.
25. Lownsbery B.F., Huang C.S., Johnson R.N. Tissue culture and maintenance of the root-lesion nematode, Pratylenchus vulnus. Nematologica 1967, 13:390-394.
26. Lück, S., Douchkov, D., 2009. si-Fi. In: Free Software Foundation, Boston, USA.
27. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 2001, 11:171-176.
28. Matthews B.F., Pilitt K.L., Klink V. Molecular characterisation of a soybean cyst nematode (Heterodera glycines) homolog of unc-87. J. Nematol. 2004, 36:457-465.
29. Mello C.C., Fire A. DNA transformation. Caenorhabditis elegans: Modern Biological Analysis of an Organism 1995, 451-482. Academic Press, San Diego. H.F. Epstein, D.C. Shakes (Eds.).
30. Ngô H., Tschudi C., Gull K., Ullu E. Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. Proc. Natl. Acad. Sci. USA 1998, 95:14687-14692.
31. Nicol P., Gill R., Fosu-Nyarko J., Jones M.G.K. De novo analysis and functional classification of the transcriptome of the root lesion nematode, Pratylenchus thornei, after 454 GS FLX sequencing. Int. J. Parasitol. 2012, 42:225-237.
32. Nuez I., Felix M.A. Evolution of susceptibility to ingested double-stranded RNAs in Caenorhabditis nematodes. PLoS One 2012, 7.
33. Oliviera C.M.G., Inomoto M.M., Viera A.M.C., Monteiro A.R. Effect of initial population densities of Pratylenchus brachyurus on the growth of Coffea arabica cv. Mundo Novo and C. canephora cv. Apota. Nematropica 1999, 29:215-221.
34. Ono K., Ono S. Tropomyosin and troponin are required for ovarian contraction in the Caenorhabditis elegans reproductive system. Mol. Biol. Cell 2004, 15:2782-2793.
35. Orii H., Mochii M., Watanabe K. A simple 'soaking method' for RNA interference in the planarian Dugesia japonica. Dev. Genes. Evol. 2003, 213:138-141.
36. Park J.E., Lee K.Y., Lee S.J., Oh W.S., Jeong P.Y., Woo T., Kim C.B., Paik Y.K., Koo H.S. The efficiency of RNA interference in Bursaphelenchus xylophilus. Mol. Cells 2008, 26:81-86.
37. Reise R.W., Huettel R.N., Sayre R.M. Carrot callus tissue for culture of endoparasitic nematodes. J. Nematol. 1987, 19:387-389.
38. Romano N., Macino G. Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol. Microbiol. 1992, 6:3343-3353.
39. Rosso M.N., Dubrana M.P., Cimbolini N., Jaubert S., Abad P. Application of RNA interference to root-knot nematode genes encoding oesophageal gland proteins. Mol. Plant Microbe Interact. 2005, 18:615-620.
40. Rosso M.N., Jones J.T., Abad P. RNAi and functional genomics in plant parasitic nematodes. Annu. Rev. Phytopathol. 2009, 47:207-232.
41. Schroeder N.E., MacGuidwin A.E. Incorporation of a fluorescent compound by live Heterodera glycines. J. Nematol. 2007, 39:43-49.
42. Seinhorst J.W. The common relation between population density and plant weight in pot and microplot experiments with various nematode plant combinations. Fundam. Appl. Nematol. 1998, 21:459-468.
43. Sindhu A.S., Maier T.R., Mitchum M.G., Hussey R.S., Davis E.L., Baum T.J. Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J. Exp. Bot. 2009, 60:315-324.
44. Smiley R.W., Whittaker R.G., Gourlie J.A., Easley S.A. Pratylenchus thornei associated with reduced wheat yield in Oregon. J. Nematol. 2005, 37:45-54.
45. Sukno S.A., McCuiston J., Wong X., Thon M.R., Hussey R.S., Baum T.J., Davis E.L. Quantitative detection of double-stranded RNA-mediated gene silencing of parasitism genes in Heterodera glycines. J. Nematol. 2007, 39:145-152.
46. Tabara H., Grishok A., Mello C.C. RNAi in C. elegans: soaking in the genome sequence. Science 1998, 282:430-431.
47. Terami H., Williams B.D., Kitamura S.-I., Sakube Y., Matsumoto S., Doi S., Obinata T., Kagawa H. Genomic organization, expression, and analysis of the troponin C gene pat-10 of Caenorhabditis elegans. J. Cell Biol. 1999, 146:193-202.
48. Timmons L., Fire A. Specific interference by ingested dsRNA. Nature 1998, 395:854.
49. Urwin P.E., Lilley C.J., Atkinson H.J. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant Microbe Interact. 2002, 15:747-752.
50. Yadav B.C., Veluthambi K., Subramaniam K. Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol. Biochem. Parasitol. 2006, 148:219-222.