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Host-delivered RNAi-mediated silencing using fusion cassettes of different functional groups of genes precludes Meloidogyne incognita multiplication in Nicotiana tabacum

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Abstract

Key message

This study demonstrates multi-gene silencing approach for simultaneous silencing of several functional genes through a fusion gene strategy for protecting plants against root-knot nematode, Meloidogyne incognita.

The ability of root-knot nematode (RKN), Meloidogyne incognita, to cause extensive yield decline in a wide range of cultivated crops is well-documented. Due to the inadequacies of current management approaches, the alternatively employed contemporary RNA interference (RNAi)-based host-delivered gene silencing (HD-RNAi) strategy targeting different functional effectors/genes has shown substantial potential to combat RKNs. In this direction, we have explored the possibility of simultaneous silencing of four esophageal gland genes, six plant cell-wall modifying enzymes (PCWMEs) and a serine protease gene of M. incognita using the fusion approach. In vitro RNAi showed that combinatorial gene silencing is the most effective in affecting nematode behavior in terms of reduced attraction, penetration, development, and reproduction in tomato and adzuki beans. In addition, qRT-PCR analysis of M. incognita J2s soaked in fusion-dsRNA showed perturbed expression of all the genes comprising the fusion construct confirming successful dsRNA processing which is also supported by increased mRNA abundance of five key-RNAi pathway genes. In addition, hairpin RNA expressing constructs of multi-gene fusion cassettes were developed and used for generation of Nicotiana tabacum transgenic plants. The integration of gene constructs and expression of siRNAs in transgenic events were confirmed by Southern and Northern blot analyses. Besides, bio-efficacy analyses of transgenic events, conferred up to 87% reduction in M. incognita multiplication. Correspondingly, reduced transcript accumulation of the target genes in the M. incognita females extracted from transgenic events confirmed successful gene silencing.

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Data availability

The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abad P, Williamson VM (2010) Plant nematode interaction: a sophisticated dialogue. Adv Bot Res 53:147–192

    Article  CAS  Google Scholar 

  • Adam MAM, Phillips MS, Jones JT, Block VC (2008) Characterization of the cellulose-binding proteins Mj-cbp-1 of the root knot nematode, Meloidogyne javanica. Physiol Mol Plant Pathol 72:21–28

    Article  CAS  Google Scholar 

  • Banakar P, Sharma A, Lilley CJ, Gantasala NP, Kumar M, Rao U (2015) Combinatorial in vitro RNAi of two neuropeptide genes and a pharyngeal gland gene on Meloidogyne incognita. Nematology 17(2):155–167

    Article  Google Scholar 

  • Banakar P, Hada A, Papolu PK, Rao U (2020) Simultaneous RNAi knockdown of three FMRFamide-Like Peptide Genes, Mi-flp1, Mi-flp12, and Mi-flp18 provides resistance to root-knot nematode, Meloidogyne incognita. Front Microbiol 11:2690

    Article  Google Scholar 

  • Berg RH, Fester T, Taylor CG (2009) Development of the root-knot nematode feeding cell. In: Berg RH, Taylor CG (eds) Cell biology of plant nematode parasitism. Springer, Berlin, pp 115–152

    Chapter  Google Scholar 

  • Blok VC, Jones JT, Phillips MS, Trudgill DL (2008) Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. BioEssays 30(3):249–259

    Article  CAS  Google Scholar 

  • Carreón-Anguiano KG, Islas-Flores I, Vega-Arreguín J, Sáenz-Carbonell L, Canto-Canché B (2020) Effhunter: a tool for prediction of effector protein candidates in fungal proteomic databases. Biomol Ther 10:712

    Google Scholar 

  • Chaudhary S, Dutta TK, Shivakumara TN, Rao U (2019a) RNAi of esophageal gland-specific gene Mi-msp-1 alters early stage infection behaviour of root-knot nematode, Meloidogyne incognita. J Gen Plant Pathol 85(3):232–242

    Article  CAS  Google Scholar 

  • Chaudhary S, Dutta TK, Tyagi N, Shivakumara TN, Papolu PK, Chobhe KA, Rao U (2019b) Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant. Transgenic Res 28(3):327–340

    Article  CAS  Google Scholar 

  • Dalzell JJ, McMaster S, Fleming CC, Maule AG (2010) Short interfering RNA-mediated gene silencing in Globodera pallida and Meloidogyne incognita infective stage juveniles. Int J Parasitol 40(1):91–100

    Article  CAS  Google Scholar 

  • 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 (2013) Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLoS Pathog 9(10):e1003745

    Article  Google Scholar 

  • de Souza Júnior JD, Coelho RR, Lourenço IT, da Rocha FR, Viana AA, de Macedo LL, da Silva MC, Carneiro RM, Engler G, de Almeida-Engler J, Grossi-de-Sa MF (2013) Knocking-down Meloidogyne incognita proteases by plant-delivered dsRNA has negative pleiotropic effect on nematode vigor. PLoS One 8(12):e85364

    Article  Google Scholar 

  • Ding X, Shields J, Allen R, Hussey RS (2000) Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. Int J Parasitol 30:77–81

    Article  CAS  Google Scholar 

  • Dinh PTY, Zhang L, Brown CR, Elling AA (2014) Plantmediated 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

    Article  CAS  Google Scholar 

  • Duarte A, Maleita C, Egas C, Abrantes I, Curtis R (2017) Significant effects of RNAi silencing of the venom allergen-like protein (Mhi-vap-1) of the root-knot nematode Meloidogyne hispanica in the early events of infection. Plant Pathol 66(8):1329–1337

    Article  CAS  Google Scholar 

  • Dutta TK, Khan MR, Phani V (2019) Plant-parasitic nematode management via biofumigation using brassica and non-brassica plants: current status and future prospects. Curr Plant Biol 17:17–32

    Article  Google Scholar 

  • Elling AA (2013) Major emerging problems with minor Meloidogyne species. Phytopathology 103(11):1092–1102

    Article  Google Scholar 

  • Favery B, Dubreuil GAR, Chen MS, Giron D, Abad P (2020) Gall-inducing parasites: convergent and conserved strategies of plant manipulation by insects and nematodes. Annu Rev Phytopathol 58:1–22

    Article  CAS  Google Scholar 

  • Forghani F, Hajihassani A (2020) Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Front Plant Sci 11:1125

    Article  Google Scholar 

  • Gantasala NP, Papolu PK, Thakur PK, Kamaraju D, Sreevathsa R, Rao U (2013) Selection and validation of reference genes for quantitative gene expression studies by real-time PCR in eggplant (Solanum melongena L). BMC Res Notes 6(1):1–11

    Article  Google Scholar 

  • Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:1–7

    Article  Google Scholar 

  • Gowda M, Rai A, Singh B (2017) Root knot nematode a threat to vegetable production and its management. IIVR Technology, New York. https://iivr.icar.gov.in/sites/default/files/Technical%20Bulletins/Final%20Bulletin_76.pdf

  • Hada A, Kumari C, Phani V, Singh D, Chinnusamy V, Rao U (2020a) Host-induced silencing of FMRFamide-like peptide genes, flp-1 and flp-12, in rice impairs reproductive fitness of the root-knot nematode Meloidogyne graminicola. Front Plant Sci 11:894

    Article  Google Scholar 

  • Hada A, Dutta TK, Singh N, Singh B, Rai V, Singh NK, Rao U (2020b) A genome-wide association study in Indian wild rice accessions for resistance to the root-knot nematode Meloidogyne graminicola. PLoS One 15(9):e0239085

    Article  CAS  Google Scholar 

  • Hada A, Patil BL, Bajpai A, Kesiraju K, Dinesh-Kumar S, Paraselli B, Sreevathsa R, Rao U (2021a) Micro RNA-induced gene silencing strategy for the delivery of siRNAs targeting Meloidogyne incognita in a model plant Nicotiana benthamiana. Pest Manag Sci 77(7):3396–3405

    Article  CAS  Google Scholar 

  • Hada A, Singh D, Papolu PK, Banakar P, Raj A, Rao U (2021b) Host-mediated RNAi for simultaneous silencing of different functional groups of genes in Meloidogyne incognita using fusion cassettes in Nicotiana tabacum. Plant Cell Rep 40(12):2287–2302

    Article  CAS  Google Scholar 

  • Hada A, Singh D, Satyanarayana KKVV, Chatterjee M, Phani V, Rao U (2021c) Effect of fluensulfone on different functional genes of root-knot nematode. J Nematol 53:e2021–e2073

    Article  CAS  Google Scholar 

  • Haegeman A, Mantelin S, Jones JT, Gheysen G (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492:19–31

    Article  CAS  Google Scholar 

  • Hamamouch N, Li C, Hewezi T, Baum TJ, Mitchum MG, Hussey RS, Vodkin LO, Davis EL (2012) The interaction of the novel 30C02 cyst nematode effector protein with a plant beta-1,3 endoglucanase may suppress host defence to promote parasitism. J Exp Bot 63:3683–3695

    Article  CAS  Google Scholar 

  • Hassan S, Behm CA, Mathesius U (2010) Effectors of plant parasitic nematodes that re-program root cell development. Funct Plant Biol 37:933–942

    Article  CAS  Google Scholar 

  • Hewezi T, Baum TJ (2013) Manipulation of plant cells by cyst and rootknot nematode effectors. Mol Plant Microbe Interact 26:9–16

    Article  CAS  Google Scholar 

  • Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093

    Article  CAS  Google Scholar 

  • Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984

    Article  CAS  Google Scholar 

  • Hu L, Cui R, Sun L, Lin B, Zhuo K, Liao J (2013) Molecular and biochemical characterization of the β-1,4-endoglucanase gene Mj-eng-3 in the root-knot nematode Meloidogyne javanica. Exp Parasitol 135:15–23

    Article  CAS  Google Scholar 

  • Huang G, Gao B, Maier T, Allen R, Davis EL, Baum TJ et al (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 16:376–381

    Article  CAS  Google Scholar 

  • Huang G, Dong R, Maier T, Allen R, Davis EL, Baum TJ et al (2004) Use of solid-phase subtractive hybridization for the identification of parasitism gene candidates from the root-knot nematode Meloidogyne incognita. Mol Plant Pathol 5:217–222

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hussey RS, Davis EL, Baum TJ (2002) Secrets in secretions: genes that control nematode parasitism of plants. Braz J Plant Physiol 14(3):183–194

    Article  CAS  Google Scholar 

  • Iberkleid I, Vieira P, de Almeida EJ, Firester K, Spiegel Y, Horowitz SB (2013) Fatty acid and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS One 8:e64586

    Article  CAS  Google Scholar 

  • Ibrahim HM, Alkharouf NW, Meyer SL, Aly MA, Gamal EAK (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol 127:90–99

    Article  CAS  Google Scholar 

  • Jagdale S, Rao U, Giri AP (2021) Effectors of root-knot nematodes: an arsenal for successful parasitism. Front Plant Sci 12:800030

    Article  Google Scholar 

  • Jaouannet M, Perfus-Barbeoch L, Deleury E, Magliano M, Engler G, Vieira P, Danchin EGJ, Da Rocha M, Coquillard P, Abad P et al (2012) A root knot nematode secreted protein is injected into giant cells and targeted to the nuclei. New Phytol 194:924–931

    Article  CAS  Google Scholar 

  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WM, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961

    Article  Google Scholar 

  • Kassam R, Yadav J, Chawla G, Kundu A, Hada A, Jaiswal N, Rao U et al (2021a) Identification, characterization, and evaluation of nematophagous fungal species of Arthrobotrys and Tolypocladium for the management of Meloidogyne incognita. Front Microbiol 12:790223

    Article  Google Scholar 

  • Kassam R, Yadav J, Jaiswal N, Chatterjee M, Hada A, Chawla G, Kamil D, Rao U (2021b) Identification and potential utility of Metarhizium anisopliae (ITCC9014) for the management of root‑knot nematode, Meloidogyne incognita. Ind Phytopathol. https://doi.org/10.1007/s42360-022-00498-5

  • Kassam R, Jaiswal N, Hada A, Phani V, Yadav J, Budhwar R, Godwin J, Rao U et al (2022) Evaluation of Paecilomyces tenuis producing Huperzine A for the management of root-knot nematode Meloidogyne incognita (Nematoda: Meloidogynidae). J Pest Sci. https://doi.org/10.1007/s10340-022-01521-4

    Article  Google Scholar 

  • Kim KH, Kabir E, Jahan SA (2017) Exposure to pesticides and the associated human health effects. Sci Total Environ 575:525–535

    Article  CAS  Google Scholar 

  • Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey RS, Bennett M, Mitchum MG (2011) The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–880

    Article  CAS  Google Scholar 

  • Leitão L, Prista C, Moura TF, Loureiro-Dias MC, Soveral G (2012) Grapevine aquaporins: gating of a tonoplast intrinsic protein (TIP2;1) by cytosolic pH. PLoS One 7:e33219

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    Article  CAS  Google Scholar 

  • Mantelin S, Bellafiore S, Kyndt T (2017) Meloidogyne graminicola: a major threat to rice agriculture. Mol Plant Pathol 18(1):3–15

    Article  Google Scholar 

  • Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis EL (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol 199(4):879–894

    Article  Google Scholar 

  • Mitreva-Dautova M, Roze E, Overmars H, De Graaff L, Schots A, Helder J et al (2006) A symbiont-independent endo-1,4-β-xylanase from the plant-parasitic nematode Meloidogyne incognita. Mol Plant-Microbe Interact 19:521–529

    Article  CAS  Google Scholar 

  • 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(1):1–3

    CAS  Google Scholar 

  • Oka Y (2014) Nematicidal activity of fluensulfone against some migratory nematodes. Pest Manag Sci 70:1850–1858

    Article  CAS  Google Scholar 

  • 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(11):e80603

    Article  CAS  Google Scholar 

  • Papolu PK, Dutta TK, Tyagi N, Urwin PE, Lilley CJ, Rao U (2016) Expression of a cystatin transgene in eggplant provides resistance to root-knot nematode, Meloidogyne incognita. Front Plant Sci 7:1122

    Article  Google Scholar 

  • Papolu PK, Dutta TK, Hada A, Singh D, Rao U (2020) The production of a synthetic chemodisruptive peptide in planta precludes Meloidogyne incognita multiplication in Solanum melongena. Physiol Mol Plant Physiol 112:101542

    Article  CAS  Google Scholar 

  • Roderick H, Urwin PE, Atkinson HJ (2018) Rational design of biosafe crop resistance to a range of nematodes using RNA interference. Plant Biotechnol J 16(2):520–529

    Article  CAS  Google Scholar 

  • Rosso MN, Favery B, Piotte C, Arthaud L, De Boer JM, Hussey RS et al (1999) Isolation of a cDNA encoding a β-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Mol Plant-Microbe Interact 12:585–591

    Article  CAS  Google Scholar 

  • Rosso MN, Dubrana MP, 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(7):615–620

    Article  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Shivakumara TN, Papolu PK, Dutta TK, Kamaraju D, Chaudhary S, Rao U (2016) RNAi-induced silencing of an effector confers transcriptional oscillation in another group of effectors in the root-knot nematode, Meloidogyne incognita. Nematology 18(7):857–870

    Article  CAS  Google Scholar 

  • Shivakumara TN, Chaudhary S, Kamaraju D, Dutta TK, Papolu PK, Banakar P, Sreevathsa R, Singh B, Manjaiah KM, Rao U (2017) Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant. Front Plant Sci 8:473

    Article  Google Scholar 

  • Shivakumara TN, Somvanshi VS, Phani V, Chaudhary S, Hada A, Budhwar R, Shukla RN, Rao U (2019) Meloidogyne incognita (Nematoda: Meloidogynidae) sterol-binding protein Mi-SBP-1 as a target for its management. Int J Parasitol 49(13–14):1061–1073

    Article  CAS  Google Scholar 

  • Taylor CM, Wang Q, Rosa BA, Huang SCC, Powell K, Schedl T, Pearce EJ, Abubucker S, Mitreva M (2013) Discovery of anthelmintic drug targets and drugs using chokepoints in nematode metabolic pathways. PLoS Pathog 9:e1003505

    Article  CAS  Google Scholar 

  • Urwin PE, McPherson MJ, Atkinson HJ (1998) Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta 204(4):472–479

    Article  CAS  Google Scholar 

  • Vieira P, Gleason C (2019) Plant-parasitic nematode effectors—insights into their diversity and new tools for their identification. Curr Opin Plant Biol 50:37–43

    Article  CAS  Google Scholar 

  • Walawage SL, Britton MT, Leslie CA, Uratsu SL, Li Y, Dandekar AM (2013) Stacking resistance to crown gall and nematodes in walnut rootstocks. BMC Genom 14:668

    Article  CAS  Google Scholar 

  • Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38

    Article  Google Scholar 

  • Xue B, Hamamouch N, Li C, Huang G, Hussey RS, Baum TJ et al (2013) The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103:175–181

    Article  CAS  Google Scholar 

  • Yang Y, Jittayasothorn Y, Chronis D, Wang X, Cousins P, Zhong GY (2013) Molecular characteristics and efficacy of 16D10 siRNAs in inhibiting root-knot nematode infection in transgenic grape hairy roots. PLoS One 8:e69463

    Article  CAS  Google Scholar 

  • Zhang L, Davies LJ, Elling AA (2015) A Meloidogyne incognita effector is imported into the nucleus and exhibits transcriptional activation activity in planta. Mol Plant Pathol 16:48–60

    Article  Google Scholar 

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Acknowledgements

We thank the Director and the Joint Director (Research), ICAR-Indian Agricultural Research Institute, New Delhi, India for extending support and facilities to complete the study.

Funding

This work was supported by ICAR-Indian Agricultural Research Institute, New Delhi-110012 from the Institutional research and development fund.

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Authors and Affiliations

  1. Division of Nematology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Alkesh Hada, Divya Singh, Prakash Banakar, Pradeep K. Papolu, Rami Kassam, Madhurima Chatterjee, Jyoti Yadav & Uma Rao

  2. Department of Nematology and Centre for Bio-Nanotechnology, Chaudhary Charan Singh Haryana Agricultural University, Hisar, 125004, India

    Prakash Banakar

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  1. Alkesh Hada
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Contributions

UR: conceptualization, supervision and fund acquisition. AH and PB: design the gene constructs. AH performed all the experiments. PKP: help in molecular characterization of the transgenics. DS, RK, MC and JY: assisted with in vitro studies and plant transformation. AH: nematode bioassays, data analysis and wrote the original draft of the manuscript. AH and UR: finalized the final draft of the manuscript. All authors read and approved the manuscript.

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Hada, A., Singh, D., Banakar, P. et al. Host-delivered RNAi-mediated silencing using fusion cassettes of different functional groups of genes precludes Meloidogyne incognita multiplication in Nicotiana tabacum. Plant Cell Rep 42, 29–43 (2023). https://doi.org/10.1007/s00299-022-02934-2

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