Host-induced RNA interference targeting the neuromotor gene FMRFamide-like peptide-14 (Mi-flp14) perturbs Meloidogyne incognita parasitic success in eggplant.


Journal

Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970

Informations de publication

Date de publication:
22 Jun 2024
Historique:
received: 02 04 2024
accepted: 04 06 2024
medline: 22 6 2024
pubmed: 22 6 2024
entrez: 22 6 2024
Statut: epublish

Résumé

The study demonstrates the successful management of Meloidogyne incognita in eggplant using Mi-flp14 RNA interference, showing reduced nematode penetration and reproduction without off-target effects across multiple generations. Root-knot nematode, Meloidogyne incognita, causes huge yield losses worldwide. Neuromotor function in M. incognita governed by 19 neuropeptides is vital for parasitism and parasite biology. The present study establishes the utility of Mi-flp14 for managing M. incognita in eggplant in continuation of our earlier proof of concept in tobacco (US patent US2015/0361445A1). Mi-flp14 hairpin RNA construct was used for generating 19 independent transgenic eggplant events. PCR and Southern hybridization analysis confirmed transgene integration and its orientation, while RT-qPCR and Northern hybridization established the generation of dsRNA and siRNA of Mi-flp14. In vitro and in vivo bio-efficacy analysis of single-copy events against M. incognita showed reduced nematode penetration and development at various intervals that negatively impacted reproduction. Interestingly, M. incognita preferred wild-type plants over the transgenics even when unbiased equal opportunity was provided for the infection. A significant reduction in disease parameters was observed in transgenic plants viz., galls (40-48%), females (40-50%), egg masses (35-40%), eggs/egg mass (50-55%), and derived multiplication factor (60-65%) compared to wild type. A unique demonstration of perturbed expression of Mi-flp14 in partially penetrated juveniles and female nematodes established successful host-mediated RNAi both at the time of penetration even before the nematodes started withdrawing plant nutrients and later stage, respectively. The absence of off-target effects in transgenic plants was supported by the normal growth phenotype of the plants and T-DNA integration loci. Stability in the bio-efficacy against M. incognita across T

Identifiants

pubmed: 38907748
doi: 10.1007/s00299-024-03259-y
pii: 10.1007/s00299-024-03259-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

178

Subventions

Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR5908/AGR/36/727/2012

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG (2008) Genome sequence of the metazoan plant parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:909–915. https://doi.org/10.1038/nbt.1482
doi: 10.1038/nbt.1482 pubmed: 18660804
Abd-Elgawad MMM, Askary TH (2015) Impact of phytonematodes on agriculture economy. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CABI, UK, pp 3–49
doi: 10.1079/9781780643755.0003
Atkinson HJ, Isaac RE, Harris PD, Sharpe CM (1988) FMRFamide like immunoreactivity within the nervous system of the nematodes Panagrellus redivius, Caenorhabditis elegans and Heterodera glycines. J Zool 216:663–671. https://doi.org/10.1111/j.1469-7998.1988.tb02464.x
doi: 10.1111/j.1469-7998.1988.tb02464.x
Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162:2028–2041. https://doi.org/10.1104/pp.113.222372
doi: 10.1104/pp.113.222372 pubmed: 23800991 pmcid: 3729780
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. https://doi.org/10.1163/15685411-00002859
doi: 10.1163/15685411-00002859
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 11:573916. https://doi.org/10.3389/fmicb.2020.573916
doi: 10.3389/fmicb.2020.573916 pubmed: 33193182
Banerjee S, Gill SS, Jain PK, Sirohi A (2017) Isolation, cloning, and characterization of a cuticle collagen gene, Mi-col-5 in Meloidogyne incognita. 3 Biotech 7(1):64. https://doi.org/10.1007/s13205-017-0665-1
doi: 10.1007/s13205-017-0665-1 pubmed: 28452012 pmcid: 5428120
Bhardwaj A, Thapliyal S, Dahiya Y, Babu K (2018) FLP-18 functions through the G-protein-coupled receptors NPR-1 and NPR-4 to modulate reversal length in Caenorhabditis elegans. J Neurosci 38(20):4641–4654. https://doi.org/10.1523/JNEUROSCI.1955-17.2018
doi: 10.1523/JNEUROSCI.1955-17.2018 pubmed: 29712787 pmcid: 5965667
Blok VC, Jones JT, Phillips MS, Trudgill DL (2008) Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialization. BioEssays 30(3):249–259. https://doi.org/10.1002/bies.20717
doi: 10.1002/bies.20717 pubmed: 18293363
Chaudhary S, Dutta TK, Tyagi N, Shivakumara TN, Papolu PK, Chobhe KA, Rao U (2019) Host-induced silencing of Mi-msp-1 confers resistance to root-knot nematode Meloidogyne incognita in eggplant. Transgenic Res 28(3):327–340. https://doi.org/10.1007/s11248-019-00126-5
doi: 10.1007/s11248-019-00126-5 pubmed: 30955133
Cruz-Martinez H, Ruiz-Vega J, Matadamas-Ortiz PT, Cortes-Martinez CI, Rosas-Diaz J (2017) Formulation of entomopathogenic nematodes for crop pest control—a review. Plant Prot Sci 53:15–24. https://doi.org/10.17221/35/2016-pps
doi: 10.17221/35/2016-pps
Dalzell JJ, McMaster S, Johnston MJ, Kerr R, Fleming CC, Maule AG (2009) Non-nematode-derived double-stranded RNAs induce profound phenotypic changes in Meloidogyne incognita and Globodera pallida infective juveniles. Int J Parasitol 39:1503–1516. https://doi.org/10.1016/j.ijpara.2009.05.006
doi: 10.1016/j.ijpara.2009.05.006 pubmed: 19482028
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 40:91–100. https://doi.org/10.1016/j.ijpara.2009.07.003
doi: 10.1016/j.ijpara.2009.07.003 pubmed: 19651131
Danchin EGJ, Arguel MJ, Campan-Fournier A, Perfus-Barbeoch L, Magliano M, Rosso M-N et al (2013) Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PloS Pathogen 9:e1003745. https://doi.org/10.1371/journal.ppat.1003745
doi: 10.1371/journal.ppat.1003745
Dlamini BE, Addison P, Malan AP (2019) A review of the biology and control of Phlyctinus callosus (Schonherr) (Coleoptera: Curculionidae), with special reference to biological control using entomopathogenic nematodes and fungi. Afr Entomol 27:279–288. https://doi.org/10.4001/003.027.0279
doi: 10.4001/003.027.0279
Dong L, Li X, Huang L, Gao Y, Zhong L, Zheng Y et al (2014) Lauric acid in crown daisy root exudate potently regulates root-knot nematode chemotaxis and disrupts Mi-flp-18 expression to block infection. J Exp Bot 65:131–141. https://doi.org/10.1093/jxb/ert356
doi: 10.1093/jxb/ert356 pubmed: 24170741
Dutta TK, Khan MR, Phani V (2019) Plant-parasitic nematode management via bio fumigation using brassica and non-brassica plants: current status and prospects. Curr Plant Biol 17:17–32. https://doi.org/10.1016/j.cpb.2019.02.001
doi: 10.1016/j.cpb.2019.02.001
Ehwaeti ME, Elliott MJ, McNicol JM, Phillips MS, Trudgill DL (2000) Modeling nematode population growth and damage. Crop Protect 19:739–745. https://doi.org/10.1016/S0261-2194(00)00098-3
doi: 10.1016/S0261-2194(00)00098-3
Elling AA (2013) Major emerging problems with minor Meloidogyne species. Phytopathology 103:1092–1102. https://doi.org/10.1094/PHYTO-01-13-0019-RVW
doi: 10.1094/PHYTO-01-13-0019-RVW pubmed: 23777404
Fairbarn DJ, Cavallaro AS, Bernerd 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. https://doi.org/10.1007/s00425-007-0588-x
doi: 10.1007/s00425-007-0588-x
Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44. https://doi.org/10.1111/j.1469-8137.2008.02508.x
doi: 10.1111/j.1469-8137.2008.02508.x pubmed: 18564304
Hada A, Dutta TK, Singh N, Singh B, Rai V, Singh NK, Rao U (2020a) A genome-wide association study in Indian wild rice accessions for resistance to the root-knot nematode Meloidogyne graminicola. PLoS ONE 15(9):e0239085. https://doi.org/10.1371/journal.pone.0239085
doi: 10.1371/journal.pone.0239085 pubmed: 32960916 pmcid: 7508375
Hada A, Kumari C, Phani V, Singh D, Chinnusamy V, Rao U (2020b) 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. https://doi.org/10.3389/fpls.2020.00894
doi: 10.3389/fpls.2020.00894 pubmed: 32765539 pmcid: 7379849
Hada A, Patil BL, Bajpai A, Kesiraju K, Dinesh-Kumar S, Paraselli B et al (2021) Micro RNA-induced gene silencing strategy for the delivery of siRNAs targeting Meloidogyne incognita in a model plant Nicotiana benthamiana. Pest Manag Sci. https://doi.org/10.1002/ps.6384
doi: 10.1002/ps.6384 pubmed: 33786977
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 40:2287–2302. https://doi.org/10.1007/s00299-021-02767-5
doi: 10.1007/s00299-021-02767-5 pubmed: 34387737
Hada A, Singh D, Satyanarayana KKVV, Chatterjee M, Phani V, Rao U (2021) Effect of fluensulfone on different functional genes of root-knot nematode Meloidogyne incognita. J Nematol 53:e2021-73. https://doi.org/10.21307/jofnem-2021-073
doi: 10.21307/jofnem-2021-073 pubmed: 34414375 pmcid: 8371937
Hada A, Singh D, Banakar P et al (2023) 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. https://doi.org/10.1007/s00299-022-02934-2
doi: 10.1007/s00299-022-02934-2 pubmed: 36462028
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. https://doi.org/10.1093/jxb/ers058
doi: 10.1093/jxb/ers058 pubmed: 22442414 pmcid: 3388836
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. https://doi.org/10.1105/tpc.108.063065
doi: 10.1105/tpc.108.063065 pubmed: 19001564 pmcid: 2613657
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. https://doi.org/10.1104/pp.109.150557
doi: 10.1104/pp.109.150557 pubmed: 19965964 pmcid: 2815906
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. https://doi.org/10.1073/pnas.0604698103
doi: 10.1073/pnas.0604698103 pubmed: 16985000 pmcid: 1570184
Ibrahim HM, Alkharouf NW, Meyer SL, Aly MA, Gamal El-Din AL et al (2011) Post transcriptional gene silencing of root knot nematodes in transformed soybean roots. Exp Parasitol. https://doi.org/10.1016/j.exppara.2010.06.037
doi: 10.1016/j.exppara.2010.06.037 pubmed: 21044626
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. https://doi.org/10.1111/j.1469-8137.2012.04164.x
doi: 10.1111/j.1469-8137.2012.04164.x pubmed: 22540860
Johnston MJG, McVeigh P, McMaster S, Fleming CC, Maule AG (2010) FMRFamide-like peptides in root knot nematodes and their potential role in nematode physiology. J Helminthol 84(3):253–265. https://doi.org/10.1017/S0022149X09990630
doi: 10.1017/S0022149X09990630 pubmed: 19843350
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057
doi: 10.1111/mpp.12057 pubmed: 23809086 pmcid: 6638764
Joshi I, Kumar A, Singh AK, Kohli D, Raman KV, Sirohi A, Chaudhury A, Jain PK (2019) Development of nematode resistance in Arabidopsis by HD-RNAi-mediated silencing of the effector gene Mi-msp2. Sci Rep 9(1):1–11. https://doi.org/10.1038/s41598-019-53485-8
doi: 10.1038/s41598-019-53485-8
Joshi I, Kumar A, Kohli D et al (2020) Conferring root-knot nematode resistance via host-delivered RNAi-mediated silencing of four Mi-msp genes in Arabidopsis. Plant Sci 298:110592. https://doi.org/10.1016/j.plantsci.2020.110592
doi: 10.1016/j.plantsci.2020.110592 pubmed: 32771150
Kassam R, Yadav J, Chawla G, Kundu A, Hada A, Jaiswal N et al (2021) Identification, characterization, and evaluation of nematophagous fungal species of Arthrobotrys and Tolypocladium for the management of Meloidogyne incognita. Front Microbiol 12:790223. https://doi.org/10.3389/fmicb.2021.790223
doi: 10.3389/fmicb.2021.790223 pubmed: 34956156 pmcid: 8702965
Kassam R, Yadav J, Jaiswal N, Chatterjee M, Hada A, Chawla G et al (2022) Identification and potential utility of Metarhizium anisopliae (ITCC9014) for the management of root-knot nematode. Meloidogyne Incognita Indian Phytopathol 75(3):875–881. https://doi.org/10.1007/s42360-022-00498-5
doi: 10.1007/s42360-022-00498-5
Kassam R, Jaiswal N, Hada A, Phani V, Yadav J, Budhwar R et al (2023a) Evaluation of Paecilomyces tenuis producing Huperzine A for the management of root-knot nematode Meloidogyne incognita (Nematoda: Meloidogynidae). J Pest Sci 96(2):723–743. https://doi.org/10.1007/s10340-022-01521-4
doi: 10.1007/s10340-022-01521-4
Kassam R, Kranti KV, Yadav J, Chatterjee M, Chawla G, Kundu A, Hada A et al (2023) Exploration of rhizosphere-dwelling nematophagous Trichoderma spp. using novel ‘bait technique’with root-knot nematode Meloidogyne incognita. Biol Control. 186:105327. https://doi.org/10.1016/j.biocontrol.2023.105327
doi: 10.1016/j.biocontrol.2023.105327
Kerschen A, Napoli CA, Jorgensen RA, Muller AE (2004) Effectiveness of RNA interference in transgenic plants. FEBS Lett 566:223–228. https://doi.org/10.1016/j.febslet.2004.04.043
doi: 10.1016/j.febslet.2004.04.043 pubmed: 15147899
Khanal C, Land J (2023) Study on two nematode species suggests climate change will inflict greater crop damage. Sci Rep 13:14185. https://doi.org/10.1038/s41598-023-41466-x
doi: 10.1038/s41598-023-41466-x pubmed: 37648720 pmcid: 10468521
Kimber MJ, Fleming CC, Bjourson AJ, Halton DW, Maule AG (2001) FMRFamide-related peptides in potato cyst nematodes. Mol Biochem Parasitol 116:199–208. https://doi.org/10.1016/S0166-6851(01)00323-1
doi: 10.1016/S0166-6851(01)00323-1 pubmed: 11522352
Kimber MJ, Fleming CC, Prior A, Jones JT, Halton DW, Maule AG (2002) Localisation of Globodera pallida FMRFamide-related peptide encoding genes using in situ hybridisation. Int J Parasitol 32:1095–1105. https://doi.org/10.1016/S0020-7519(02)00084-X
doi: 10.1016/S0020-7519(02)00084-X pubmed: 12117492
Kimber MJ, McKinney S, McMaster S, Day TA, Fleming CC, Maule AG (2007) flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J 21:1233–1243. https://doi.org/10.1096/fj.06-7343com
doi: 10.1096/fj.06-7343com pubmed: 17200420
Kumar A, Joshi I, Changwal C et al (2022) Host-delivered RNAi-mediated silencing of the root-knot nematode (Meloidogyne incognita) effector genes, Mi-msp10 and Mi-msp23, confers resistance in Arabidopsis and impairs reproductive ability of the root-knot nematode. Planta 256:74. https://doi.org/10.1007/s00425-022-03977-1
doi: 10.1007/s00425-022-03977-1 pubmed: 36083352
Kumari C, Dutta TK, Banakar P, Rao U (2016) Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice. Sci Rep 6:22846. https://doi.org/10.1038/srep22846
doi: 10.1038/srep22846 pubmed: 26961568 pmcid: 4785349
Lahm GP, Desaeger J, Smith BK, Pahutski TF, River MA, Meloro T et al (2017) The discovery of fluazaindolizine: a new product for the control of plant parasitic nematodes. Bioorg Med Chem Lett 27:1572–1575. https://doi.org/10.1016/j.bmcl.2017.02.029
doi: 10.1016/j.bmcl.2017.02.029 pubmed: 28242274
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. https://doi.org/10.1104/pp.110.167197
doi: 10.1104/pp.110.167197 pubmed: 21156858
Li XQ, Wei JZ, Tan A, Aroian RV (2007) Resistance to rootknot nematode in tomato roots expressing a nematicidal Bacillus thuringiensis crystal protein. Plant Biotechnol J 5:455–464. https://doi.org/10.1111/j.1467-7652.2007.00257.x
doi: 10.1111/j.1467-7652.2007.00257.x pubmed: 17451491
Lilley CJ, Davies LJ, Urwin PE (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139:630–640. https://doi.org/10.1017/S0031182011002071
doi: 10.1017/S0031182011002071 pubmed: 22217302
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. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262 pubmed: 11846609
Magrane M, UniProt Consortium (2011) UniProt knowledgebase: a hub of integrated protein data. Database. https://doi.org/10.1093/database/bar009
doi: 10.1093/database/bar009 pubmed: 21447597 pmcid: 3070428
Majumdar R, Rajasekaran K, Cary JW (2017) RNA Interference (RNAi) as a potential tool for control of mycotoxin contamination in crop plants: concepts and considerations. Front Plant Sci 8:200. https://doi.org/10.3389/fpls.2017.00200
doi: 10.3389/fpls.2017.00200 pubmed: 28261252 pmcid: 5306134
McCarter JP, Bird DM, Mitreva M (2005) Nematode gene sequences: update for December 2005. J Nematol 37:417
pubmed: 19262885 pmcid: 2620984
McCulloch KA, Zhou K, Jin Y (2020) Neuronal transcriptome analyses reveal novel neuropeptide modulators of excitation and inhibition imbalance in C. elegans. PLoS ONE 15(6):e0233991. https://doi.org/10.1371/journal.pone.0233991
doi: 10.1371/journal.pone.0233991 pubmed: 32497060 pmcid: 7272019
McVeigh P, Geary TG, Marks NJ, Maule AG (2006) The FLP-side of nematodes. Trends Parasitol 22:385–396. https://doi.org/10.1016/j.pt.2006.06.010
doi: 10.1016/j.pt.2006.06.010 pubmed: 16824799
Morris R, Wilson L, Sturrock M, Warnock ND, Carrizo D, Cox D et al (2017) A neuropeptide modulates sensory perception in the entomopathogenic nematode Steinernema carpocapsae. PLoS Pathogen 13:e1006185. https://doi.org/10.1371/journal.ppat.1006185
doi: 10.1371/journal.ppat.1006185
Mutlu AS, Gao SM, Zhang H, Wang MC (2020) Olfactory specifcity regulates lipid metabolism through neuroendocrine signaling in Caenorhabditis elegans. Nat Commun 11(1):1–15. https://doi.org/10.1038/s41467-020-15296-8
doi: 10.1038/s41467-020-15296-8
Niu J, Jian H, Xu J, Chen C, Guo Q, Liu Q et al (2012) RNAi silencing of the Meloidogyne incognita Rpn7 gene reduces nematode parasitic success. Eur J Plant Pathol 134:131–144. https://doi.org/10.1007/s10658-012-9971-y
doi: 10.1007/s10658-012-9971-y
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. https://doi.org/10.1038/srep19443
doi: 10.1038/srep19443
Papaioannou S, Marsden D, Franks CJ, Walker RJ, Holden-Dye L (2005) Role of a FMRFamide-like family of neuropeptides in the pharyngeal nervous system of Caenorhabditis elegans. J Neurobiol 65(3):304–319. https://doi.org/10.1002/neu.20201
doi: 10.1002/neu.20201 pubmed: 16187307
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. https://doi.org/10.1371/journal.pone.0080603
doi: 10.1371/journal.pone.0080603 pubmed: 24223228
Park J, Choi W, Dar AR, Butcher RA, Kim K (2019) Neuropeptide signaling regulates pheromone-mediated gene expression of a chemoreceptor gene in C. elegans. Mol Cells. 42(1):28. https://doi.org/10.14348/molcells.2018.0380
doi: 10.14348/molcells.2018.0380 pubmed: 30453729
Peymen K, Watteyne J, Frooninckx L, Schoofs L, Beets I (2014) The FMRFamide-like peptide family in nematodes. Front Endocrinol 5:90. https://doi.org/10.3389/fendo.2014.00090
doi: 10.3389/fendo.2014.00090
Roderick H, Urwin PE, Atkinson HJ (2018) Rational design of biosafe crop resistance to a range of nematodes using RNA interference. Plant Biotechnol J 16:520–529. https://doi.org/10.1111/pbi.12792
doi: 10.1111/pbi.12792 pubmed: 28703405
Rogers C, Reale V, Kim K, Chatwin H, Li C, Evans P et al (2003) Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat Neurosci 6:1178–1185. https://doi.org/10.1038/nn1140
doi: 10.1038/nn1140 pubmed: 14555955
Rosso MN, Dubrana MP, Cimbolini N, Jauber S, Abad P (2005) Application of RNA interference to root-knot nematode genes encoding esophageal gland proteins. Mol Plant Microbe Interact 18:615–620. https://doi.org/10.1094/MPMI-18-0615
doi: 10.1094/MPMI-18-0615 pubmed: 16042006
Shingles J, Lilley CJ, Atkinson HJ, Urwin PE (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. https://doi.org/10.1016/j.exppara.2006.07.008
doi: 10.1016/j.exppara.2006.07.008 pubmed: 16996059
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 18:857–870. https://doi.org/10.1163/15685411-00003003
doi: 10.1163/15685411-00003003
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. https://doi.org/10.3389/fpls.2017.00473
doi: 10.3389/fpls.2017.00473 pubmed: 28424727 pmcid: 5371666
Shivakumara TN, Somvanshi VS, Phani V, Chaudhary S, Hada A, Budhwar R et al (2019) Meloidogyne incognita (Nematoda: Meloidogynidae) sterol binding protein Mi-SBP-1 as a target for its management. Int J Parasitol 49:1061–1073. https://doi.org/10.1016/j.ijpara.2019.09.002
doi: 10.1016/j.ijpara.2019.09.002 pubmed: 31733196
Thakur P, Sharma A, Rao SB, Kumar M, Prasad N, Tyagi N, Kamaraju D, Papolu P, Banakar P, Rao U (2012) Cloning and characterization of two neuropeptide genes from cereal cyst nematode Heterodera avanae from India. Bioinformation. 8(13):617–621. https://doi.org/10.6026/97320630008617
doi: 10.6026/97320630008617 pubmed: 22829742 pmcid: 3400987
Urwin PE, Lilley CJ, Atkinson HJ (2002) Ingestion of double stranded RNA by preparasitic juvenile cyst nematode leads to RNA interference. Mol Plant Microbe Interact 15:747–752. https://doi.org/10.1094/MPMI.2002.15.8.747
doi: 10.1094/MPMI.2002.15.8.747 pubmed: 12182331
Wang CL, Lower S, Williamson VM (2009) Application of pluronic gel to the study of root-knot nematode behaviour. Nematology 11:453–464. https://doi.org/10.1163/156854109X447024
doi: 10.1163/156854109X447024
Wang Y, Chen Z, Yang Y, Zhang F (2021) Transcriptional reprogramming caused by cold acclimation in Meloidogyne incognita eggs. Genes Genomics 43(5):533–541. https://doi.org/10.1007/s13258-021-01069-0
doi: 10.1007/s13258-021-01069-0 pubmed: 33725279
Warnock ND, Wilson L, Patten C, Fleming CC, Maule AG, Dalzell JJ (2017) Nematode neuropeptides as transgenic nematicides. PLoS Pathog 13:e1006237. https://doi.org/10.1371/journal.ppat.1006237
doi: 10.1371/journal.ppat.1006237 pubmed: 28241060 pmcid: 5344539
Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol 55:25–38. https://doi.org/10.1111/j.1744-7348.1965.tb07864.x
doi: 10.1111/j.1744-7348.1965.tb07864.x
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. https://doi.org/10.1094/PHYTO-07-12-0173-R
doi: 10.1094/PHYTO-07-12-0173-R pubmed: 23294405
Zhang F, Peng D, Ye X, Yu Z, Hu Z, Ruan L et al (2012) In vitro uptake of 140 kDa Bacillus thuringiensis nematicidal crystal proteins by the second stage juvenile of Meloidogyne hapla. PLoS ONE 7:e38534. https://doi.org/10.1371/journal.pone.0038534
doi: 10.1371/journal.pone.0038534 pubmed: 22737212 pmcid: 3380895
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. https://doi.org/10.1111/mpp.12160
doi: 10.1111/mpp.12160 pubmed: 24863562
Zhuo K, Chen J, Lin B, Wang J, Sun F, Hu L et al (2017) A novel Meloidogyne enterolobii effector MeTCTP promotes parasitism by suppressing programmed cell death in host plants. Mol Plant Pathol 18:45–54. https://doi.org/10.1111/mpp.12374
doi: 10.1111/mpp.12374 pubmed: 26808010

Auteurs

Divya Kamaraju (D)

Division of Nematology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India.
School of Biotechnology, Kalinga Institute of Industrial Technology, Bhubaneswar, 751024, India.

Madhurima Chatterjee (M)

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

Pradeep K Papolu (PK)

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

Tagginahalli N Shivakumara (TN)

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

Rohini Sreevathsa (R)

ICAR-National Institute for Plant Biotechnology, New Delhi, 110012, India.

Alkesh Hada (A)

Division of Nematology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India. alkeshhada@gmail.com.
Department of Entomology, Nematology and Chemistry Units, Agricultural Research Organization (ARO), The Volcani Center, 7505101, Bet Dagan, Israel. alkeshhada@gmail.com.

Uma Rao (U)

Division of Nematology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India. umanema@gmail.com.
Engrave Biolabs Pvt Ltd. , Shanthipuram, Kukatpally, Hyderabad, 500072, India. umanema@gmail.com.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH