Host-delivered RNAi-mediated root-knot nematode resistance in Arabidopsis by targeting splicing factor and integrase genes

Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Ségurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915 Atamian HS, Roberts PA, Kaloshian I (2012) High and low throughput screens with root-knot nematodes Meloidogyne spp. J Vis Exp 61:e39 Bakhetia M, Urwin PE, Atkinson HJ (2008) 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 38:1589–1597 Carvalho LM, Benda ND, Vaughan MM, Cabrera AR, Hung K, Cox T, Abdo Z, Allen LH, Teal PE (2015) Mi-1-mediated nematode resistance in tomatoes is broken by short-term heat stress but recovers over time. J Nematol 47:133–140 Chitwood DJ (2003) Research on plant-parasitic nematode biology conducted by the United States Department of Agriculture-Agricultural Research Service. Pest Manag Sci 59:748–753 Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743 Danchin EG, Arguel MJ, Campan-Fournier A, Perfus-Barbeoch L, Magliano M, Rosso MN, Da Rocha M, Da Silva C, Nottet N, Labadie K, Guy J, Artiguenave F, Abad P (2013) Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLoS Pathog 9:e1003745 Dinh PTY, Brown CR, Elling AA (2014a) RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in Arabidopsis and potato. Phytopathology 104:1098–1106 Dinh PTY, Zhang L, Brown CR, Elling AA (2014b) Plant-mediated RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in diverse genetic backgrounds of potato and reduces pathogenicity of nematode offspring. Nematology 16:669–682 Dong L, Xu J, Chen S, Li X, Zuo Y (2016) Mi-flp-18 and Mi-mpk-1 genes are potential targets for Meloidogyne incognita control. J Parasitol 102:208–213 Dutta TK, Papolu PK, Banakar P, Chaudhary D, Sirohi A, Rao U (2015) Tomato transgenic plants expressing hairpin construct of a nematode protease gene conferred enhanced resistance to root-knot nematodes. Front Microbiol 6:260 Eisenback JD, Sasser JN, and CC (1985) Diagnostic characters useful in the identification of the four most common species of root-knot nematodes (Meloidogyne spp.) In: Sasser JN, Carter CC (eds.) An advanced treatise on Meloidogyne 1: Biology and control, North Carolina State University Graphics, Raleigh, pp 95–112 Elling AA (2013) Major emerging problems with minor Meloidogyne species. Phytopathology 103:1092–1102 Fairbairn DJ, Cavallaro AS, Bernard M, Mahalinga-Iyer J, Graham MW, Botella JR (2007) Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226:1525–1533 Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811 Huang G, Allen R, Davis EL, Baum TJ, Hussey RS (2006) 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 Ibrahim HMM, Alkharouf NW, Meyer SLF, Aly MA, Gamal El-Din Ael K, Hussein EH, Matthews BF (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol 127:90–99 Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, Abad P, Rosso MN (2013) The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Mol Plant Microbe Interact 26:97–105 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 Klink VP, Kim KH, Martins V, Macdonald MH, Beard HS, Alkharouf NW, Lee SK, Park SC, Matthews BF (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 230:53–71 Li J, Todd TC, Oakley TR, Lee J, Trick HN (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232:775–785 Lourenço-Tessutti IT, Souza Junior JDA, Martins-de-Sa D, Viana AA, Carneiro RM, Togawa RC, de Almeida-Engler J, Batista JA, Silva MC, Fragoso RR, Grossi-de-Sa MF (2015) Knock-down of heat-shock protein 90 and isocitrate lyase gene expression reduced root-knot nematode reproduction. Phytopathology 105:628–637 Niu J, Jian H, Xu J, Chen C, Guo Q, Liu Q, Guo Y (2012) RNAi silencing of the Meloidogyne incognita Rpn7 gene reduces nematode parasitic success. Eur J Plant Pathol 134:131–144 Niu J, Liu P, Liu Q, Chen C, Guo Q, Yin J, Yang G, Jian H (2016) Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Sci Rep 6:19443 Papolu PK, Gantasala NP, Kamaraju D, Banakar P, Sreevathsa R, Rao U (2013) 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 8:e80603 Rosso MN, Jones JT, Abad P (2009) RNAi and functional genomics in plant parasitic nematodes. Annu Rev Phytopathol 47:207–232 Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386 Sindhu AS, Maier TR, Mitchum MG, Hussey RS, Davis EL, Baum TJ (2009) Effective and specific in planta RNAi in cyst nematodes: expression interference of four parasitism genes reduces parasitic success. J Exp Bot 60:315–324 Steeves RM, Todd TC, Essig JS, Trick HN (2006) Transgenic soybeans expressing siRNAs specific to a major sperm protein gene suppress Heterodera glycines reproduction. Funct Plant Biol 33:991–999 Tamilarasan S, Rajam MV (2013) Engineering crop plants for nematode resistance through host-herived RNA interference. Cell Dev Biol 2:114 Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369 Williamson VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36:277–293 Xue B, Hamamouch N, Li C, Huang G, Hussey RS, Baum TJ, Davis EL (2013) The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103:175–181 Yadav BC, 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 Zijlstra C, Donkers-Venne DTHM, Fargette M (2000) Identification of Meloidogyne incognita, M. javanica and M. arenaria using sequence characterised amplified region (SCAR) based PCR assays. Nematology 2:847–853