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RNA interference in plant parasitic nematodes: a summary of the current status

Published online by Cambridge University Press:  05 January 2012

C. J. LILLEY ,
L. J. DAVIES  and
P. E. URWIN
C. J. LILLEY
Affiliation:
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
L. J. DAVIES
Affiliation:
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
P. E. URWIN*
Affiliation:
Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK
*
*Corresponding Author: Tel: +44 (113) 3432909. E-mail: [email protected]
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Summary

RNA interference (RNAi) has emerged as an invaluable gene-silencing tool for functional analysis in a wide variety of organisms, particularly the free-living model nematode Caenorhabditis elegans. An increasing number of studies have now described its application to plant parasitic nematodes. Genes expressed in a range of cell types are silenced when nematodes take up double stranded RNA (dsRNA) or short interfering RNAs (siRNAs) that elicit a systemic RNAi response. Despite many successful reports, there is still poor understanding of the range of factors that influence optimal gene silencing. Recent in vitro studies have highlighted significant variations in the RNAi phenotype that can occur with different dsRNA concentrations, construct size and duration of soaking. Discrepancies in methodology thwart efforts to reliably compare the efficacy of RNAi between different nematodes or target tissues. Nevertheless, RNAi has become an established experimental tool for plant parasitic nematodes and also offers the prospect of being developed into a novel control strategy when delivered from transgenic plants.

Keywords

RNA interferenceRNAinematodeplant parasiticgene silencingefficacyresistance
Type
Research Article
Information
Parasitology , Volume 139 , Special Issue 5: Genetic manipulation of parasitic helminths to define gene function , April 2012 , pp. 630 - 640
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V. C., Caillaud, M. C., Coutinho, P. M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J. V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T. R., Markov, G. V., 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, T. J., Blaxter, M., Bleve-Zacheo, T., Davis, E. L., Ewbank, J. J., Favery, B., Grenier, E., Henrissat, B., Jones, J. T., Laudet, V., Maule, A. G., Quesneville, H., Rosso, M. N., Schiex, T., Smant, G., Weissenbach, J. and Wincker, P. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909–915.CrossRefGoogle ScholarPubMed
Adam, M. A. M., Phillips, M. S., Jones, J. T. and Blok, V. C. (2008). Characterisation of the cellulose-binding protein Mj-cbp-1 of the root knot nematode, Meloidogyne javanica. Physiological and Molecular Plant Pathology 72, 21–28.CrossRefGoogle Scholar
Alkharouf, N. W., Klink, V. P. and Matthews, B. F. (2007). Identification of Heterodera glycines (soybean cyst nematode SCN) cDNA sequences with high identity to those of Caenorhabditis elegans having lethal mutant or RNAi phenotypes. Experimental Parasitology 115, 247–258.CrossRefGoogle ScholarPubMed
Aoki, K., Moriguchi, H., Yoshioka, T., Okawa, K. and Tabara, H. (2007). In vitro analyses of the production and activity of secondary small interfering RNAs in C. elegans. EMBO Journal 26, 5007–5019.Google Scholar
Bakhetia, M., Charlton, W., Atkinson, H. J. and McPherson, M. J. (2005 a). RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 18, 1099–1106.CrossRefGoogle ScholarPubMed
Bakhetia, M., Charlton, W. L., Urwin, P. E., McPherson, M. J. and Atkinson, H. J. (2005 b). RNA interference and plant parasitic nematodes. Trends in Plant Science 10, 362–367.CrossRefGoogle ScholarPubMed
Bakhetia, M., Urwin, P. E. and Atkinson, H. J. (2007). qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular Plant-Microbe Interactions 20, 306–312.Google Scholar
Bakhetia, M., Urwin, P. E. and Atkinson, H. J. (2008). Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi. International Journal for Parasitology 38, 1589–1597.CrossRefGoogle ScholarPubMed
Berg, R. H., Fester, T. and Taylor, C. G. (2009). Development of the root-knot nematode feeding cell. In Cell Biology of Plant Nematode Parasitism (eds. Berg, R. H. and Taylor, C. G.), Plant Cell Monographs 15, pp. 115–152. Springer, Berlin.CrossRefGoogle Scholar
Brodersen, P. and Voinnet, O. (2006). The diversity of RNA silencing pathways in plants. Trends in Genetics 22, 268–280.CrossRefGoogle ScholarPubMed
Charlton, W. C., Harel, H. Y. M., Bakhetia, M., Hibbard, J. K., Atkinson, H. J. and McPherson, M. J. (2010). Additive effects of plant expressed double-stranded RNAs on root-knot nematode development. International Journal for Parasitology 40, 855–864.Google Scholar
Chen, Q., Rehman, S., Smant, G. and Jones, J. T. (2005). Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Molecular Plant-Microbe Interactions 18, 621–625.Google Scholar
Cheng, X. Y., Dai, S. M., Xiao, L. and Xie, B. Y. (2010). Influence of cellulase gene knockdown by dsRNA interference on the development and reproduction of the pine wood nematode, Bursaphelenchus xylophilus. Nematology 12, 225–233.CrossRefGoogle Scholar
Dalzell, J. J., McMaster, S., Fleming, C. C. and Maule, A. G. (2010 a). Short interfering RNA-mediated gene silencing in Globodera pallida and Meloidogyne incognita infective stage juveniles. International Journal for Parasitology 40, 91–100.CrossRefGoogle ScholarPubMed
Dalzell, J. J., McMaster, S., Johnstone, M. J., Kerr, R., Fleming, C. C. and Maule, A. G. (2009). Non-nematode-derived double-stranded RNAs induce profound phenotypic changes in Meloidogyne incognita and Globodera pallida infective juveniles. International Journal for Parasitology 39, 1503–1516.CrossRefGoogle ScholarPubMed
Dalzell, J. J., McVeigh, P., Warnock, N. D., Mitreva, M., Bird, D. McK., Abad, P., Fleming, C. C., Day, T. A., Mousley, A., Marks, N. J. and Maule, A. G. (2011). RNAi effector diversity in nematodes. PLoS Neglected Tropical Diseases 5 (6), e1176.CrossRefGoogle ScholarPubMed
Dalzell, J. J., Warnock, N. D., Stevenson, M. A., Mousley, A., Fleming, C. C. and Maule, A. G. (2010 b). Short interfering RNA-mediated knockdown of drosha and pasha in undifferentiated Meloidogyne incognita eggs leads to irregular growth and embryonic lethality. International Journal for Parasitology 40, 1303–1310.CrossRefGoogle ScholarPubMed
Davis, E. L., Hussey, R. S. and Baum, T. J. (2004). Getting to the roots of parasitism by nematodes. Trends in Parasitology 20, 134–141.Google Scholar
Dubreuil, G., Magliano, M., Deleury, E., Abad, P. and Rosso, M. N. (2007). Transcriptome analysis of root-knot nematode functions induced in the early stages of parasitism. New Phytologist 176, 426–436.Google Scholar
Fairbairn, D. J., Cavallaro, A. S., Bernard, M., Mahalinga-Iyer, J., Graham, M. W. and Botella, J. R. (2007). Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226, 1525–1533.CrossRefGoogle ScholarPubMed
Fanelli, E., Di Vito, M., Jones, J. T. and De Giorgi, C. (2005). Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene 349, 87–95.CrossRefGoogle Scholar
Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.Google Scholar
Geldhof, P., Visser, A., Clark, D., Saunders, G., Britton, C., Gilleard, J., Berriman, M. and Knox, D. (2007). RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134, 609–619.CrossRefGoogle ScholarPubMed
Gheysen, G. and Fenoll, C. (2002). Gene expression in nematode feeding sites. Annual Review of Phytopathology 40, 191–219.CrossRefGoogle ScholarPubMed
Gheysen, G. and Mitchum, M. G. (2009). Molecular insights in the susceptible plant response to nematode infection. In Cell Biology of Plant Nematode Parasitism (ed. Berg, R. H. and Taylor, C. G.), Plant Cell Monographs 15, pp. 45–81. Springer, Berlin.CrossRefGoogle Scholar
Gheysen, G. and Vanholme, B. (2007). RNAi from plants to nematodes. Trends in Biotechnology 25, 89–92.Google Scholar
Gleason, C. A., Liu, Q. L. and Williamson, V. M. (2008). Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Molecular Plant-Microbe Interactions 21, 576–585.CrossRefGoogle Scholar
Grishok, A. (2005). RNAi mechanisms in Caenorhabditis elegans. FEBS Letters 579, 5932–5939.Google Scholar
Grishok, A., Tabara, H. and Mello, C. C. (2000). Genetic requirements for inheritance of RNAi in C. elegans. Science 287, 2494–2497.Google ScholarPubMed
Haegeman, A., Vanholme, B. and Gheysen, G. (2009). Characterization of a putative endoxylanase in the migratory plant-parasitic nematode Radopholus similis. Molecular Plant Pathology 10, 389–401.CrossRefGoogle ScholarPubMed
Hedgecock, E. M., Culotti, J. G., Thomson, J. N. and Perkins, L. A. (1985). Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Developmental Biology 111, 158–170.CrossRefGoogle ScholarPubMed
Huang, G. Z., Allen, R., Davis, E. L., Baum, T. J. and Hussey, R. S. (2006). Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proceedings of the National Academy of Sciences, USA 103, 14302–14306.CrossRefGoogle ScholarPubMed
Ibrahim, H. M. M., Alkharouf, N. W., Meyer, S. L. F., Aly, M. A. M., Gamal El-Din, A. Y., Hussein, E. H. A. and Matthews, B. F. (2011). Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Experimental Parasitology 127, 90–99.CrossRefGoogle ScholarPubMed
Jones, P. W., Tylka, G. L. and Perry, R. N. (1998). Hatching. In The Physiology and biochemistry of free-living and plant-parasitic nematodes (ed. Perry, R. N. and Wright, D. J.), pp. 181–212. CAB International, Oxford.Google Scholar
Kamath, R. S. and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313–321.Google Scholar
Kang, J. S., Lee, D. W., Koh, Y. H. and Lee, S. H. (2011). A soluble acetylcholinesterase provides chemical defense against xenobiotics in the pinewood nematode. PLoS ONE 6, e19063.Google Scholar
Kimber, M. J. and Fleming, C. C. (2005). Neuromuscular function in plant parasitic nematodes: a target for novel control strategies? Parasitology 131, S129–S142.CrossRefGoogle ScholarPubMed
Kimber, M. J., McKinney, S., McMaster, S., Day, T. A., Fleming, C. C. and Maule, A. G. (2007). flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB Journal 21, 1233–1243.CrossRefGoogle Scholar
Klink, V. P., Kim, K.-H., Martins, V., MacDonald, M. H., Beard, H. S., Alkharouf, N. W., Lee, S.-K., Park, S.-C. and Matthews, B. F. (2009). A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta 250, 53–71.CrossRefGoogle Scholar
Li, J., Todd, T. C., Oakley, T. R., Lee, J. and Trick, H. N. (2010 b). Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232, 775–785.CrossRefGoogle ScholarPubMed
Li, J., Todd, T. C. and Trick, H. N. (2010 a). Rapid in planta evaluation of root expressed transgenes in chimeric soybean plants. Plant Cell Reports 29, 113–123.Google Scholar
Li, X., Zhuo, K., Luo, M., Sun, L. and Liao, J. (2011). Molecular cloning and characterization of a calreticulin cDNA from the pinewood nematode Bursaphelenchus xylophilus. Experimental Parasitology 128, 121–126.Google Scholar
Lilley, C. J., Atkinson, H. J. and Urwin, P. E. (2005 a). Molecular aspects of cyst nematodes. Molecular Plant Pathology 6, 577–588.CrossRefGoogle ScholarPubMed
Lilley, C. J., Bakhetia, M., Charlton, W. L. and Urwin, P. E. (2007). Recent progress in the development of RNA interference for plant parasitic nematodes. Molecular Plant Pathology 8, 701–711.CrossRefGoogle ScholarPubMed
Lilley, C. J., Goodchild, S. A., Atkinson, H. J. and Urwin, P. E. (2005 b). Cloning and characterisation of a Heterodera glycines aminopeptidase cDNA. International Journal for Parasitology 35, 1577–1585.CrossRefGoogle ScholarPubMed
Lilley, C. J., Kyndt, T. and Gheysen, G. (2011). Nematode resistant GM crops in industrialised and developing countries. In Exploiting Genomics and Molecular Biology to Understand Plant-Nematode Interactions (ed. Jones, J. T., Gheysen, G. and Fenoll, C.), pp. 515–539. Springer, Dordrecht.Google Scholar
Maeda, I., Kohara, Y., Yamamoto, M. and Sugimoto, A. (2001). Large scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Current Biology 11, 171–176.CrossRefGoogle ScholarPubMed
Michaeli, S., Kenigsbuch, D., Livneh, O., Levy, D. and Khayat, E. (2005). Bar Ilan University, Hazera Genetics, Rahan Meristem. Plants resistant to cytoplasm-feeding parasites, WO/2005/019408.Google Scholar
Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J., Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. (2008). Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences, USA 105, 14802–14807.Google Scholar
Pak, J. and Fire, A. (2007). Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315, 241–244.Google ScholarPubMed
Park, J. E., Lee, K. Y., Lee, S. J., Oh, W. S., Jeong, P. Y., Woo, T., Kim, C. B., Paik, Y. K. and Koo, H. S. (2008). The efficiency of RNA interference in Bursaphelenchus xylophilus. Molecules and Cells 26, 81–86.CrossRefGoogle ScholarPubMed
Patel, N., Hamamouch, N., Li, C. Y., Hewezi, T., Hussey, R. S., Baum, T., Mitchum, M. and Davis, E. L. (2010). A nematode effector protein similar to annexins in host plants. Journal of Experimental Botany 61, 235–248.CrossRefGoogle ScholarPubMed
Patel, N., Hamamouch, N., Li, C. Y., Hussey, R. S., Mitchum, M., Baum, T., Wang, X. and Davis, E. L. (2008). Similarity and functional analyses of expressed parasitism genes in Heterodera schachtii and Heterodera glycines. Journal of Nematology 40, 299–310.Google Scholar
Perrimon, N., Ni, J. Q. and Perkins, L. (2010). In vivo RNAi: Today and tomorrow. Cold Spring Harbor Perspectives in Biology 2, a003640.Google Scholar
Rosso, M. N., Dubrana, M. P., Cimbolini, N., Jaubert, S. and Abad, P. (2005). Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Molecular Plant-Microbe Interactions 18, 615–620.Google Scholar
Rosso, M. N. and Grenier, E. (2011). Other nematode effectors and evolutionary constraints. In Genomics and Molecular Genetics of Plant-Nematode Interactions (ed. Jones, J., Gheysen, G. and Fenoll, C.), pp. 287–307. Springer, Netherlands.Google Scholar
Shingles, J., Lilley, C. J., Atkinson, H. J. and Urwin, P. E. (2007). Meloidogyne incognita: Molecular and biochemical characterisation of a cathepsin L cysteine proteinase and the effect on parasitism following RNAi. Experimental Parasitology 115, 114–120.Google Scholar
Sijen, T., Steiner, F. A., Thijssen, K. L. and Plasterk, R. H. A. (2007). Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315, 244–247.Google Scholar
Silva, J., Chang, K., Hannon, G. J. and Rivas, F. V. (2004). RNA-interference-based functional genomics in mammalian cells: reverse genetics coming of age. Oncogene 23, 8401–8409.Google Scholar
Sindhu, A. S., Maier, T. R., Mitchum, M. G., Hussey, R. S., Davis, E. L. and Baum, T. J. (2009). Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. Journal of Experimental Botany 60, 315–324.CrossRefGoogle ScholarPubMed
Sobczak, M. and Golinowski, W. (2009). Structure of cyst nematode feeding sites. In Cell Biology of Plant Nematode Parasitism (ed. Berg, R. H. and Taylor, C. G.), Plant Cell Monographs 15, pp. 153–157. Springer, Berlin.Google Scholar
Sontheimer, E. J. (2005). Assembly and function of RNA silencing complexes. Nature Reviews Molecular and Cellular Biology 6, 127–138.CrossRefGoogle ScholarPubMed
Srinivasan, J., Durak, O. and Sternberg, P. W. (2008). Evolution of a polymodal sensory response network. BMC Biology 6, 52.CrossRefGoogle ScholarPubMed
Steeves, R. M., Todd, T. C., Essig, J. S. and Trick, H. N. (2006). Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Functional Plant Biology 33, 991–999.Google Scholar
Sukno, S. A., McCuiston, J., Wong, M. Y., Wang, X., Thon, M. R., Hussey, R., Baum, T. and Davis, E. (2007). Quantitative detection of double-stranded RNA-mediated gene silencing of parasitism genes in Heterodera glycines. Journal of Nematology 39, 145–152.Google ScholarPubMed
Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J., Barthel, A., Bebas, P., Bitram, K., Bravo, A., Chevalier, F., Collinge, D. P., Crava, C. M., de Maagd, R. A., Duvic, B., Erlandson, M., Faye, I., Felfoldi, G., Fujiwara, H., Futahashi, R., Gandhe, A. S., Gatehouse, H. S., Gatehouse, L. N., Giebultowicz, J. M., Gomez, I., Grimmelikhuijzen, C. J. P., Groot, A. T., Hauser, F., Heckel, D. G., Hegedus, D. D., Hrycaj, S., Huang, L., Hull, J. J., Iatrou, K., Iga, M., Kanost, M. R., Kotwica, J., Li, C., Li, J., Liu, J., Lundmark, M., Matsumoto, S., Meyering-Vos, M., Millichap, P. J., Monteiro, A., Mrinal, N., Niimi, T., Nowara, D., Ohnishi, A., Oostra, V., Ozaki, K., Papakonstantinou, M., Popadic, A., Rajam, M. V., Saenko, S., Simpson, R. M., Soberon, M., Strand, M. R., Tomita, S., Toprak, U., Wang, P., Wei Wee, C., Whyard, S., Zhang, W., Nagaraju, J., ffrench-Constant, R. H., Herrero, S., Gordon, K., Swevers, L. and Smagghe, G. (2011). RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology 57, 231–245.CrossRefGoogle ScholarPubMed
Urwin, P. E., Lilley, C. J. and Atkinson, H. J. (2002). Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions 15, 747–752.CrossRefGoogle ScholarPubMed
Vanholme, B., Van Thuyne, W., Vanhouteghem, K., De Meutter, J., Cannoot, B. and Gheysen, G. (2007). Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Molecular Plant Pathology 8, 267–278.Google Scholar
Vastenhouw, N. L., Brunschwig, K., Okihara, K. L., Müller, F., Tijsterman, M. and Plasterk, R. H. A. (2006). Long-term gene silencing by RNAi. Nature 442, 882.Google Scholar
Viney, M. E. and Thompson, F. J. (2008). Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. International Journal for Parasitology 38, 43–47.Google Scholar
Wang, D., Jones, L. M., Urwin, P. E. and Atkinson, H. J. (2011). A synthetic peptide shows retro- and anterograde neuronal transport before disrupting the chemosensation of plant-pathogenic nematodes. PLoS ONE 6 (3), e17475.Google Scholar
Yadav, B. C., Veluthambi, K. and Subramaniam, K. (2006). Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Molecular and Biochemical Parasitology 148, 219–222.Google Scholar