The Use of RNA Interference in Enhancing Plant Resistance against Nematodes
Source: By:Author(s)
DOI: https://doi.org/10.30564/jrb.v2i1.1759
Abstract:Plant-parasitic nematodes caused severe yield loss in major crops all over the world. The most wild-used strategies to combat the nematodes is the chamical nematicides, but the overuse of synthetic nematicides threaten sustainable agriculture development. Other strategies, like resistance cultivars and crop rotation, have limited efficiency. Thus, the utilization of molecular biotechnology like RNA interference (RNAi) would be one of the alternative ways to enhance plant resistance against nematodes. RNAi has already used as a tool for gene functional analysis in a wide range of species, especially in the non-parasitic nematode, Caenorhabtidis elegans. In plant-parasitic nematodes, RNAi is induced by soaking nematodes with double-strand RNA(dsRNA) solution mixed with neurostimulants, which is called in vitro RNAi delivery method. In another way around, in planta RNAi method, which is Host-mediated RNAi approach also showed a great success in conferring the resistance against root-knock nematodes. Two main advantages of RNAi-based transgenics are RNAi technology do not produce any functional foreign proteins and it target organisms in a sequence-specific way. Even though the development of RNAi-based transgenics against plant-parasitic nematodes is still in the initial phase, it offers the prospect into a novel nematode control strategy in the future.
References:[1] Abd-Elgawad, M. M., & Askary, T. H.. 1 Impact of Phytonematodes on Agriculture Economy. In Biocontrol Agents of Phytonematodes, CABI Wallingford, UK, 2015: 3-49. [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. Physiological and Molecular Plant Pathology, 2008, 72(1-3): 21-28. DOI: https://doi.org/10.1016/j.pmpp.2008.05.002 [3] Antonino, Coelho, R. R., Lourenço, I. T., da Rocha Fragoso, R., Viana, A. A. B., de Macedo, L. L. P., de Almeida-Engler, J.. Knocking-down Meloidogyne incognita proteases by plant-delivered dsRNA has negative pleiotropic effect on nematode vigor. PLoS One, 2013, 8(12): e85364. [4] Bakhetia, Urwin, & Atkinson. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular Plant-Microbe Interactions, 2007, 20(3): 306-312. [5] Bakhetia, M., Urwin, P., & Atkinson, H. J.. qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular Plant-Microbe Interactions, 2007, 20(3): 306-312. [6] Bakhetia, M., Urwin, P. E., & Atkinson, H. J.. Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi. Int J Parasitol, 2008, 38(13): 1589-1597. DOI: https://doi.org/10.1016/j.ijpara.2008.05.003 [7] Banerjee, S., Gill, S. S., Jain, P. K., & Sirohi, A.. Isolation, cloning, and characterization of a cuticle collagen gene, Mi-col-5, in Meloidogyne incognita. 3 Biotech, 2017, 7(1): 64. DOI: https://doi.org/10.1007/s13205-017-0665-1 [8] Charlton, W. L., Harel, H. Y., Bakhetia, M., Hibbard, J. K., Atkinson, H. J., & McPherson, M. J.. Additive effects of plant expressed double-stranded RNAs on root-knot nematode development. Int J Parasitol, 2010, 40(7): 855-864. DOI: https://doi.org/10.1016/j.ijpara.2010.01.003 [9] Cheng, X.-Y., Dai, S.-M., Xie, B.-Y., & Xiao, L.. Influence of cellulase gene knockdown by dsRNA interference on the development and reproduction of the pine wood nematode, Bursaphelenchus xylophilus. Nematology, 2010, 12(2): 225-233. DOI: https://doi.org/10.1163/138855409x12469541205044 [10] Dalzell, J. J., McVeigh, P., Warnock, N. D., Mitreva, M., Bird, D. M., Abad, P., . . . Maule, A. G.. RNAi effector diversity in nematodes. PLoS Negl Trop Dis, 2011, 5(6): e1176. DOI: https://doi.org/10.1371/journal.pntd.0001176 [11] Dinh, P. T., Brown, C. R., & Elling, A. A.. RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in Arabidopsis and potato. Phytopathology, 2014, 104(10): 1098- 1106. [12] Dutta, T. K., Papolu, P. K., Banakar, P., Choudhary, D., Sirohi, A., & Rao, U.. Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Front Microbiol, 2015, 6(260). DOI: https://doi.org/10.3389/fmicb.2015.00260 [13] Dutta, T. K., Papolu, P. K., Banakar, P., Choudhary, D., Sirohi, A., & Rao, U.. Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Frontiers in Microbiology, 2015, 6(260). DOI: https://doi.org/10.3389/fmicb.2015.00260 [14] Elling, A. A.. Major emerging problems with minor Meloidogyne species. Phytopathology, 2013, 103(11): 1092-1102. [15] Fairbairn, D. J., Cavallaro, A. S., Bernard, M., Mahalinga-Iyer, J., Graham, M. W., & Botella, J. R.. Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta, 2007, 226(6): 1525-1533. [16] Fanelli, E., Di Vito, M., Jones, J. T., & De Giorgi, C.. Analysis of chitin synthase function in a plant parasitic nematode, Meloidogyne artiellia, using RNAi. Gene, 2005, 349: 87-95. DOI: https://doi.org/10.1016/j.gene.2004.11.045 [17] Ferguson, C. M., Barratt, B. I., Bell, N., Goldson, S. L., Hardwick, S., Jackson, M., Rennie, G.. Quantifying the economic cost of invertebrate pests to New Zealand’s pastoral industry. New Zealand Journal of Agricultural Research, 2018: 1-61. [18] 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(6669): 806. [19] Gleason, C. A., Liu, Q. L., & Williamson, V. M.. Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Molecular Plant-Microbe Interactions, 2008, 21(5): 576-585. [20] Gu, S., Jin, L., Zhang, F., Sarnow, P., & Kay, M. A.. Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nature structural & molecular biology, 2009, 16(2), 144. [21] Haegeman, A., Vanholme, B., & Gheysen, G.. Characterization of a putative endoxylanase in the migratory plant-parasitic nematode Radopholus similis. Mol Plant Pathol, 2009, 10(3): 389-401. DOI: https://doi.org/10.1111/j.1364-3703.2009.00539.x [22] Ibrahim, H. M., Alkharouf, N. W., Meyer, S. L., Aly, M. A., Gamal El-Din Ael, K., Hussein, E. H., & Matthews, B. F.. Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol, 2011, 127(1): 90-99. DOI: https://doi.org/10.1016/j.exppara.2010.06.037 [23] Jones, Tylka, G., Perry, R., & Wright, D.. The Physiology and biochemistry of free-living and plant-parasitic nematodes. In: CABI Publishing London,1998. [24] Jones, J. T., Haegeman, A., Danchin, E. G., Gaur, H. S., Helder, J., Jones, M. G., Wesemael, W. M.. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 2013, 14(9): 946-961. [25] Jones, L. M., Giorgi, C. D., & Urwin, P. E.. C.elegans as a Resource for Studies on Plant Parasitic Nematodes. In J. Jones, G. Gheysen, & C. Fenoll (Eds.), Genomics and Molecular Genetics of Plant-Nematode Interactions. Dordrecht: Springer Netherlands, 2011: 175-220. [26] Klink, V. P., Kim, K. H., Martins, V., Macdonald, M. H., Beard, H. S., Alkharouf, N. W., Matthews, B. F.. 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, 2009, 230(1): 53-71. DOI: https://doi.org/10.1007/s00425-009-0926-2 [27] Kumar, A., Kakrana, A., Sirohi, A., Subramaniam, K., Srinivasan, R., Abdin, M. Z., & Jain, P. K.. Host-delivered RNAi-mediated root-knot nematode resistance in Arabidopsis by targeting splicing factor and integrase genes. Journal of General Plant Pathology, 2017, 83(2): 91-97. DOI: https://doi.org/10.1007/s10327-017-0701-3 [28] Li, J., Todd, T. C., Lee, J., & Trick, H. N.. Biotechnological application of functional genomics towards plant-parasitic nematode control. Plant biotechnology journal, 2011, 9(9): 936-944. [29] Li, J., Todd, T. C., Oakley, T. R., Lee, J., & Trick, H. N.. Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta, 2010, 232(3): 775- 785. DOI: https://doi.org/10.1007/s00425-010-1209-7 [30] Li, J., Todd, T. C., & Trick, H. N.. Rapid in planta evaluation of root expressed transgenes in chimeric soybean plants. Plant Cell Rep, 2010, 29(2): 113- 123. DOI: https://doi.org/10.1007/s00299-009-0803-2 [31] Lilley, C. J., Bakhetia, M., Charlton, W. L., & Urwin, P. E.. Recent progress in the development of RNA interference for plant parasitic nematodes. Mol Plant Pathol, 2007, 8(5): 701-711. DOI: https://doi.org/10.1111/j.1364-3703.2007.00422.x [32] Meister, G., & Tuschl, T.. Mechanisms of gene silencing by double-stranded RNA. nature, 2004, 431(7006): 343. [33] Mello, C. C., & Conte Jr, D.. Revealing the world of RNA interference. nature, 2004, 431(7006): 338. [34] Niu, J., Liu, P., Liu, Q., Chen, C., Guo, Q., Yin, J., Jian, H.. Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Sci Rep, 2016, 6: 19443. DOI: https://doi.org/10.1038/srep19443 [35] Papolu, P. K., Gantasala, N. P., Kamaraju, D., Banakar, P., Sreevathsa, R., & Rao, U.. Utility of host delivered RNAi of two FMRF amide like peptides, flp-14 and flp-18, for the management of root knot nematode, Meloidogyne incognita. PLoS One, 2013, 8(11): e80603. [36] Park, J.-E., Lee, K. Y., Lee, S.-J., Oh, W.-S., Jeong, P.-Y., Woo, T., . . . Koo, H.-S.. The efficiency of RNA interference in Bursaphelenchus xylophilus. Molecules & Cells (Springer Science & Business Media BV), 2008, 26(1). [37] Patel, N., Hamamouch, N., Li, C., Hewezi, T., Hussey, R. S., Baum, T. J., . . . Davis, E. L.. A nematode effector protein similar to annexins in host plants. J Exp Bot, 2010, 61(1): 235-248. DOI: https://doi.org/10.1093/jxb/erp293 [38] Ramon, M., Devos, Y., Lanzoni, A., Liu, Y., Gomes, A., Gennaro, A., & Waigmann, E.. RNAi-based GM plants: food for thought for risk assessors. Plant biotechnology journal, 2014, 12(9): 1271-1273. [39] Reboul, J., Vaglio, P., Tzellas, N., Thierry-Mieg, N., Moore, T., Jackson, C., Thierry-Mieg, J.. Openreading-frame sequence tags (OSTs) support the existence of at least 17,300 genes in C. elegans. Nature genetics, 2001, 27(3): 332. [40] Rosso, Dubrana, & Cimbolini.. Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Molecular Plant-Microbe Interactions, 2005, 18(7): 615-620. [41] Rosso, M. N., Jones, J. T., & Abad, P.. RNAi and functional genomics in plant parasitic nematodes. Annu Rev Phytopathol, 2009, 47: 207-232. DOI: https://doi.org/10.1146/annurev.phyto.112408.132605 [42] Rual, Ceron, J., Koreth, J., Hao, T., Nicot, A.-S., Hirozane-Kishikawa, T., . . . van den Heuvel, S.. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome research, 2004, 14(10b): 2162-2168. [43] Rual, J. F., Klitgord, N., & Achaz, G.. Novel insights into RNAi off-target effects using C. elegans paralogs. BMC Genomics, 2007, 8(106). DOI: https://doi.org/10.1186/1471-2164-8-106 [44] Siddique, S., Wieczorek, K., Szakasits, D., Kreil, D. P., & Bohlmann, H.. The promoter of a plant defensin gene directs specific expression in nematode-induced syncytia in Arabidopsis roots. Plant Physiology and Biochemistry, 2011, 49(10): 1100-1107. [45] 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(1): 315-324. DOI: https://doi.org/10.1093/jxb/ern289 [46] Singer, G. A., Lloyd, A. T., Huminiecki, L. B., & Wolfe, K. H.. Clusters of co-expressed genes in mammalian genomes are conserved by natural selection. Molecular biology and evolution, 2004, 22(3): 767-775. [47] Sontheimer, E. J.. Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol, 2005, 6(2): 127-138. DOI: https://doi.org/10.1038/nrm1568 [48] Steeves, R. M., Todd, T. C., Essig, J. S., & Trick, H. N.. Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Functional Plant Biology, 2006, 33(11). DOI: https://doi.org/10.1071/fp06130 [49] Stram, Y., & Kuzntzova, L.. Inhibition of viruses by RNA interference. Virus Genes, 2006, 32(3): 299- 306. DOI: https://doi.org/10.1007/s11262-005-6914-0 [50] Tabara, H., Grishok, A., & Mello, C. C.. RNAi in C. elegans: soaking in the genome sequence. Science, 1998, 282(5388): 430-431. [51] Thorat, Y. E.. Develop Root-Knot Nematode, Meloidogyne incognita Specific Gene Expression System in Tomato, Solanum lycopersicum L. Division of Nematology Icar-Indian Agricultural Research Institute New Delhi, 2017. [52] Timmons, L., Court, D. L., & Fire, A.. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene, 2001, 263(1-2): 103-112. [53] Vanholme, B., W, V. A. N. T., Vanhouteghem, K., J, D. E. M., Cannoot, B., & Gheysen, G.. Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Mol Plant Pathol, 2007, 8(3): 267-278. DOI: https://doi.org/10.1111/j.1364-3703.2007.00392.x [54] Wani, S. H., Sanghera, G. S., & Singh, N. B.. Biotechnology and plant disease control-role of RNA interference. American Journal of Plant Sciences, 2010, 1(02): 55. [55] 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(2): 219-222. DOI: https://doi.org/10.1016/j.molbiopara.2006.03.013 [56] Zhuo, K., Chen, J., Lin, B., Wang, J., Sun, F., Hu, L., & Liao, J.. A novel Meloidogyne enterolobii effector MeTCTP promotes parasitism by suppressing programmed cell death in host plants. Mol Plant Pathol, 2017, 18(1): 45-54. DOI: https://doi.org/10.1111/mpp.12374