Recent progress in the development of RNA interference for plant parasitic nematodes

Molecular Plant Pathology

Volumn 8, Issue 5, 2007, Pages 701-711

  Lilley, Catherine J ^a   Bakhetia, Manjula ^a   Charlton, Wayne L ^a   Urwin, Peter E ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 34548136140     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2007.00422.x     Document Type: Review

References (98)

1. de Almeida Engler, J.D., Van Poucke, K., Karimi, M., De Groodt, R., Gheysen, G. Engler, G. (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J. 38, 12 26.
2. Atkinson, H.J. (1995) Plant nematode interactions: molecular and genetic basis. In : Pathogenesis and Host Specificity in Plant Diseases, Vol. II: Eukaryotes (Kohmoto, K., Singh, U.S Singh, R.P., eds), pp. 355 370. Oxford : Pergamon Press.
3. Atkinson, H.J., Urwin, P.E. McPherson, M.J. (2003) Engineering plants for nematode resistance. Annu. Rev. Phytopathol. 41, 615 639.
4. Bakhetia, M., Charlton, W., Atkinson, H.J. McPherson, M.J. (2005) RNA interference of dual oxidase in the plant nematode Meloidogyne incognita. Mol. Plant-Microbe Interact. 18, 1099 1106.
5. Bakhetia, M., Urwin, P.E. Atkinson, H.J. (2007) qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Mol. Plant-Microbe Interact. 20, 306 312.
6. Birmingham, A., Andersen, E.M., Reynolds, A., Ilsley-Tyree, D., Leake, D., Fedorov, Y., Baskerville, S., Maksimova, E., Robinson, K., Karpilow, J., Marshall, W.S. Khvorova, A. (2006) 3′UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Meth. 3, 199 204.
7. Böckenhoff, A. Grundler, F.M.W. (1994) Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology, 109, 249 254.
8. Brodersen, P. Voinnet, O. (2006) The diversity of RNA silencing pathways in plants. Trends Genet. 22, 268 280.
9. Byzova, M., Verduyn, C., De Brouwer, D. De Block, M. (2004) Transforming petals into sepaloid organs in Arabidopsis and oilseed rape: implementation of the hairpin RNA-mediated gene silencing technology in an organ-specific manner. Planta, 218, 379 387.
10. Castagnone-Sereno, P. (2002) Genetic variability of nematodes: a threat to the durability of plant resistance genes? Euphytica, 124, 193 199.
11. Caudy, A.A., Ketting, R.F., Hammond, S.M., Denli, A.M., Bathoorn, A.M.P., Tops, B.B.J., Silva, J.M., Myers, M.M., Hannon, G.J. Plasterk, R.H.A. (2003) A micrococcal nuclease homologue in RNAi effector complexes. Nature, 425, 411 414.
12. Chen, Q., Rehman, S., Smant, G. Jones, J.T. (2005a) Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Mol. Plant-Microbe Interact. 18, 621 625.
13. Chen, C.C., Simard, M.J., Tabara, H., Brownell, D.R., McCollough, J.A. Mello, C.C. (2005b) A member of the polymerase beta nucleotidyltransferase superfamily is required for RNA interference in C. elegans. Curr. Biol. 15, 378 383.
14. Chitwood, D.J. (2003) Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Manage. Sci. 59, 748 753.
15. Cogoni, C. Macino, G. (2000) Post-transcriptional gene silencing across kingdoms. Curr. Opin. Genet. Dev. 10, 638 643.
16. Davis, E.L., Hussey, R.S., Baum, T.J., Bakker, J., Schots, A., Rosso, M.-N. Abad, P. (2000) Nematode parasitism genes. Annu. Rev. Phytopathol. 38, 365 396.
17. Davuluri, G.R., van Tuinen, A., Fraser, P.D., Manfredonia, A., Newman, R., Burgess, D., Brummell, D.A., King, S.R., Palys, J., Uhlig, J., Bramley, P.M., Pennings, H.M.J. Bowler, C. (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat. Biotechnol. 23, 890 895.
18. Denli, A.M. Hannon, G.J. (2003) RNAi: an ever-growing puzzle. Trends Biochem. Sci. 28, 196 201.
19. Dirks, R.P., Bouw, G.B., Huizen, R.R., Jansen, E.J. Martens, J.M. (2003) Functional genomics in Xenopus laevis: Towards transgene-driven RNA interference and cell-specific transgene expression. Curr. Genomics, 4, 699 711.
20. Du, T. Zamore, P.D. (2005) MicroPrimer: the biogenesis and function of microRNA. Development, 132, 4645 4652.
21. Escobar, M.A., Civerolo, E.L., Summerfelt, K.R. Dandekar, A.M. (2001) RNAi-mediated oncogene silencing confers resistance to crown gall tumorigenesis. Proc. Natl Acad. Sci. USA, 98, 13437 13442.
22. Fanelli, E., Di Vito, M., Jones, J.T. De Giorgi, C. (2005) Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene, 349, 87 95.
23. Feinberg, E.H. Hunter, C.P. (2003) Transport of dsRNA into cells by the transmembrane protein SID-1. Science, 301, 1545 1547.
24. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E. Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391, 806 811.
25. Forrest, E.C., Cogoni, C. Macino, G. (2004) The RNA-dependent RNA polymerase, QDE-1, is a rate-limiting factor in post-transcriptional gene silencing in Neurospora crassa. Nucleic Acids Res. 32, 2123 2128.
26. Gao, G., Raikar, S., Davenport, B., Mutapcic, L., Montgomery, R., Kuzmin, E. Bennett, K.L. (2006) Cross-species RNAi: selected Ascaris suum dsRNAs can sterilize Caenorhabditis elegans. Mol. Biochem. Parasitol. 146, 124 128.
27. Geldhof, P., Molloy, C. Knox, D.P. (2006) Combinatorial RNAi on intestinal cathepsin B-like proteinases in Caenorhabditis elegans questions the perception of their role in nematode biology. Mol. Biochem. Parasitol. 145, 128 132.
28. Gheysen, G. Fenoll, C. (2002) Gene expression in nematode feeding sites. Annu. Rev. Phytopathol. 40, 191 219.
29. Gheysen, G. Vanholme, B. (2007) RNAi from plants to nematodes. Trends Biotechnol. 25, 89 92.
30. Golinowski, W., Sobczak, M., Kurek, W. Grymaszewska, G. (1997) The structure of syncytia. In : Cellular and Molecular Aspects of Plant-Nematode Interactions (Fenoll, C., Grundler, F.M.W. Ohl, S.A., eds), pp. 80 97. Dordrecht, Netherlands : Kluwer Academic Publishers.
31. Goverse, A., Biesheuvel, J., Wijers, G.J., Gommers, F.J., Bakker, J., Schots, A. Helder, J. (1998) In planta monitoring of the activity of two constitutive promoters, CaMV 35S and TR2, in developing feeding cells induced by Globodera rostochiensis using green fluorescent protein in combination with confocal laser scanning microscopy. Physiol. Mol. Plant Pathol. 52, 275 284.
32. Grishok, A. (2005) RNAi mechanisms in Caenorhabditis elegans. FEBS Lett. 579, 5932 5939.
33. Grishok, A., Tabara, H. Mello, C.C. (2000) Genetic requirements for inheritance of RNAi in C. elegans. Science, 287, 2494 2497.
34. Hammond, S.M. (2005) Dicing and slicing - The core machinery of the RNA interference pathway. FEBS Lett. 579, 5822 5829.
35. Hannon, G.J. (2002) RNA interference. Nature, 418, 244 251.
36. Hedgecock, E.M., Culotti, J.G., Thomson, J.N. Perkins, L.A. (1985) Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111, 158 170.
37. Huang, G., Allen, R., Davis, E.L., Baum, T.J. Hussey, R.S. (2006a) 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, 103, 14302 14306.
38. Huang, G., Dong, R., Allen, R., Davis, E.L., Baum, T.J. Hussey, R.S. (2006b) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol. Plant-Microbe Interact. 19, 463 470.
39. Hussey, R.S. Mims, C.W. (1991) Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita. Protoplasma, 162, 99 107.
40. Jackson, A.L., Bartz, S.R., Schelter, J., Kobayashi, S.V., Burchard, J., Mao, M., Li, B., Cavet, G. Linsley, P.S. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635 637.
41. Jones, M.G.K. (1981a) The development and function of plant cells modified by endoparasitic nematodes. In : Plant Parasitic Nematodes. (Zuckerman, B.M., Mai, W.F. Rohde, R.A., eds), pp. 255 280. New York : Academic Press.
42. Jones, M.G.K. (1981b) Host cell responses to endoparasitic nematode attack: structure and function of giant cells and syncytia. Ann. Appl. Biol. 97, 353 372.
43. Jorgensen, R.A., Cluster, P.D., English, J., Que, Q. Napoli, C.A. (1996) Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single-copy vs. complex T-DNA sequences. Plant Mol. Biol. 31, 957 973.
44. Kaletta, T. Hengartner, M.O. (2006) Finding function in novel targets: C. elegans as a model organism. Nat. Rev. Drug Disc. 5, 387 398.
45. Kamath, R.S., Martinez-Campos, M., Zipperlen, P., Fraser, A.G. Ahringer, J. (2000) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2 (1 Research0002.
46. Kennerdell, J.R. Carthew, R.W. (2000) Heritable gene silencing in Drosophila using double stranded RNA. Nat. Biotechnol. 18, 896 898.
47. Kimber, M.J., Fleming, C.C., Prior, A., Jones, J.T., Halton, D.W. Maule, A.G. (2002) Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. Int. J. Parasitol. 32, 1095 1105.
48. Kimber, M.J., McKinney, S., McMaster, S., Day, T.A., Fleming, C.C. Maule, A.G. (2007) flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J. 21, 1233 1243.
49. Kumar, D., Gustafsson, C. Klessig, D.F. (2006) Validation of RNAi silencing specificity using synthetic genes: salicylic acid-binding protein 2 is required for innate immunity in plants. Plant J. 45, 863 868.
50. Kusaba, M. (2004) RNA interference in crop plants. Curr. Opin. Biotechnol. 15, 139 143.
51. Li, M. Rohrer, B. (2006) Gene silencing in Xenopus laevis by DNA-vector based RNA interference and transgenesis. Cell Res. 16, 99 105.
52. Lilley, C.J., Atkinson, H.J. Urwin, P.E. (2005a) Molecular aspects of cyst nematodes. Mol. Plant Pathol. 6, 577 588.
53. Lilley, C.J., Goodchild, S.A., Atkinson, H.J. Urwin, P.E. (2005b) Cloning and characterisation of a Heterodera glycines aminopeptidase cDNA. Int. J. Parasitol. 35, 1577 1585.
54. Mansoor, S., Amin, I., Hussain, M., Zafar, Y. Briddon, R.W. (2006) Engineering novel traits in plants through RNA interference. Trends Plant Sci. 11, 559 565.
55. Müller, J., Rehbock, K. Wyss, U. (1981) Growth of Heterodera schachtii with remarks on amounts of food consumed. Rev. Nématol. 4, 227 234.
56. Ogita, S., Uefuji, H., Morimoto, M. Sano, H. (2004) Application of RNAi to confirm theobromine as the major intermediate for caffeine biosynthesis in coffee plants with potential for construction of decaffeinated varieties. Plant Mol. Biol. 54, 931 941.
57. Pak, J. Fire, A. (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science, 315, 241 244.
58. Pooggin, M., Shivaprasad, P.V., Veluthambi, K. Mohn, T. (2003) RNAi targeting of DNA virus in plants. Nat. Biotechnol. 21, 131 132.
59. Qi, Y. Hannon, G.J. (2005) Uncovering RNAi mechanisms in plants: biochemistry enters the foray. FEBS Lett. 579, 5899 5903.
60. Roberts, P.A. (1992) Current status of the availability, development and use of host plant-resistance to nematodes. J. Nematol. 24, 213 227.
61. Rosso, M.N., Dubrana, M.P., Cimbolini, N., Jaubert, S. Abad, P. (2005) Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Mol. Plant-Microbe Interact. 18, 615 620.
62. Saleh, M.-C., van Rij, R.P., Hekele, A., Gillis, A., Foley, E., O'Farrell, P.H. Andino, R. (2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nature Cell Biol. 8, 793 802.
63. Sasser, J.N. Freckman, D.W. (1987) A world perspective on nematology: the role of the society. In : Vistas on Nematology (Veech, J.A. Dickerson, D.W., eds), pp. 7 14. Hyatsville, USA : Society of Nematologists.
64. Scacheri, P.C., Rozenblatt-Rosen, O., Caplen, N.J., Wolfsberg, T.G., Umayam, L., Lee, J.C., Hughes, C.M., Shanmugam, K.S., Battacharjee, A., Meyerson, M. Collins, F.S. (2004) Short interfering RNAs can induce unexpected and divergent changes in the levels of untargeted proteins in mammalian cells. Proc. Natl Acad. Sci. USA, 101, 1892 1897.
65. Schmid, A., Schindelholz, B. Zinn, K. (2002) Combinatorial RNAi: a method for evaluating the functions of gene families in Drosophila. Trends Neurosci. 25, 71 74.
66. Sen, G.L. Blau, H.M. (2006) A brief history of RNAi: the silence of the genes. FASEB J. 20, 1293 1299.
67. Shingles, J., Lilley, C.J., Atkinson, H.J. Urwin, P.E. (2007) Meloidogyne incognita: molecular and biochemical characterisation of a cathepsin L cysteine proteinase and the effect on parasitism following RNAi. Exp. Parasitol. 115, 114 120.
68. Sijen, T., Steiner, F.A., Thijssen, K.L. Plasterk, R.H.A. (2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science, 315, 244 247.
69. Sijmons, P.C., Grundler, F.M.W., Von Mende, N., Burrows, P.R. Wyss, U. (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J. 1, 245 254.
70. Silva, J., Chang, K., Hannon, G.J. Rivas, F.V. (2004) RNA-interference-based functional genomics in mammalian cells: reverse genetics coming of age. Oncogene, 23, 8401 8409.
71. Simmer, F., Moorman, C., van der Linden, A.M., Kuijk, E., van den Berghe, P.V.E., Kamath, R.S., Fraser, A.G., Ahringer, J. Plasterk, R.H.A. (2003) Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. Plos Biol. 1 (1 e12.
72. Simmer, F., Tijsterman, M., Parrish, S., Koushika, S.P., Nonet, M.L., Fire, A., Ahringer, J. Plasterk, R.H.A. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12, 1317 1319.
73. Smith, N.A., Singh, S.P., Wang, M.-B., Stoutjesdijk, P.A., Green, A.G. Waterhouse, P.M. (2000) Total silencing by intron-spliced hairpin RNAs. Nature, 407, 319 320.
74. Sobczak, M., Golinowski, W. Grundler, F.M.W. (1999) Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology, 1, 363 374.
75. Sontheimer, E.J. (2005) Assembly and function of RNA silencing complexes. Nat. Rev. Mol. Cell Biol. 6, 127 138.
76. Starr, J.L., Bridge, J. Cook, R. (2002) Resistance to plant-parasitic nematodes: History, current use and future potential. In : Plant Resistance to Parasitic Nematodes (Starr, J.L., Cook, R. Bridge, J., eds), pp. 1 22. Oxford : CAB International.
77. Steeves, R.M., Todd, T.C., Essig, J.S. Trick, H.N. (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Funct. Plant Biol. 33, 991 999.
78. Tabara, H., Grishok, A. Mello, C.C. (1998) RNAi in C. elegans: soaking in the genome sequence. Science, 282, 430 431.
79. Tabara, H., Yigit, Y., Siomi, H. Mello, C.C. (2002) The dsRNA binding protein RDE-4 interacts with RDE-1, DCR-1, and a DExH-box helicase to direct RNAi in C. elegans. Cell, 109, 861 871.
80. Tijsterman, M., May, R.C., Simmer, F., Okihara, K.L. Plasterk, R.H.A. (2004) Genes required for systemic RNA interference in Caenorhabditis elegans. Curr. Biol. 14, 111 116.
81. Timmons, L., Court, D.L. Fire, A. (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene, 263, 103 112.
82. Timmons, L. Fire, A. (1998) Specific interference by ingested dsRNA. Nature, 395, 854.
83. Tomari, Y. Zamore, P.D. (2005) Perspective: machines for RNAi. Genes Dev. 19, 517 529.
84. Urwin, P.E., Green, J. Atkinson, H.J. (2003) Expression of a plant cystatin confers partial resistance to Globodera, full resistance is achieved by pyramiding a cystatin with natural resistance. Mol. Breed, 12, 263 269.
85. Urwin, P.E., Lilley, C.J. Atkinson, H.J. (2002) Ingestion of double-stranded RNA by pre parasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant-Microbe Interact. 15, 747 752.
86. Urwin, P.E., McPherson, M.J. Atkinson, H.J. (1998) Enhanced transgenic plant resistance to nematodes by dual protease inhibitor constructs. Planta, 204, 472 479.
87. Urwin, P.E., Møller, S.G., Lilley, C.J., McPherson, M.J. Atkinson, H.J. (1997) Continual green-fluorescent protein monitoring of cauliflower mosaic virus 35S promoter activity in nematode-induced feeding cells in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 10, 394 400.
88. Vastenhouw, N.L., Brunschwig, K., Okihara, K.L., Müller, F., Tijsterman, M. Plasterk, R.H.A. (2006) Long-term gene silencing by RNAi. Nature, 442, 882.
89. Voinnet, O. (2001) RNA silencing as a plant immune system against viruses. Trends Genet. 17, 449 459.
90. Voinnet, O. (2002) RNA silencing: small RNAs as ubiquitous regulators of gene expression. Curr. Opin. Plant Biol. 5, 444 451.
91. Waterhouse, P.M., Graham, M.W. Wang, M.B. (1998) Virus resistance and gene silencing in plants can be induced by simultaneous expression of sense and antisense RNA. Proc. Natl Acad. Sci. USA, 95, 13959 13964.
92. Waterhouse, P.M., Wang, M.B. Lough, T. (2001) Gene silencing as an adaptive defence against viruses. Nature, 411, 834 842.
93. Wesley, S.V., Helliwell, C.A., Smith, N.A., Wang, M.-B., Rouse, D.T., Liu, Q., Gooding, P.S., Singh, S.P., Abbott, D., Stoutjesdijk, P.A., Robinson, S.P., Gleave, A.P., Green, A.G. Waterhouse, P.M. (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27, 581 590.
94. Winston, W.M., Molodowitch, C. Hunter, C.P. (2002) Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science, 295, 2456 2459.
95. Winter, M.D., McPherson, M.J. Atkinson, H.J. (2002) Neuronal uptake of pesticides disrupts chemosensory cells of nematodes. Parasitology, 125, 561 565.
96. Yadav, B.C., Veluthambi, K. Subramaniam, K. (2006) Host-generated double stranded RNA induces RNAi in plant-parasitic nematodes and protects the host from infection. Mol. Biochem. Parasitol. 148, 219 222.
97. Yigit, E., Batista, P.J., Bei, Y., Pang, K., Chen, C.G., Tolia, N.J., Joshua-Tor, L., Mitani, S., Simard, M.J. Mello, C.C. (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell, 127, 747 757.
98. Zamore, P.D., Tuschl, T., Sharp, P.A. Bartel, D.P. (2000) RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21-23 nucleotide intervals. Cell, 101, 25 33.