Plants have an immune system that can be exerted by every cell against a vast array of pathogens and parasites. This immune system has several levels of specialisation. A first level induces a general basal defence, after which specific pathogen-associated molecular patterns (PAMPs) are recognised by plant receptors. Normally, this basal defence is overcome by specialised pests by secreting specific effectors that suppress this first line of defence. Plant-parasitic nematodes have been found to secrete several such effectors through amphid and cuticle secretions or directly into the cells through their stylets. Many studies carried out on endoparasitic sedentary nematodes (ESN), in particular, reported the suppression of plant defence, especially in terms of down-regulation of the genes involved in salicylic acid (SA)-mediated defence, in the very first stages of plant-nematode interaction. However, plants can be immunised or primed against nematode attacks. Immunised plants respond to nematode infection more rapidly and efficiently and let a minor number of invasive juveniles become sedentary, develop to gravid females and reproduce. Immunisation of plants can be achieved by pre-treatments with chemicals that are functional analogues of the phytohormones that mediate defence reactions, such as salicylic acid (SA). Moreover, plants provided with the beneficial microorganisms commonly present in a healthy rhizosphere, such as arbuscular mycorrhizal fungi or opportunistic symbiotic fungi, have been found to be immunised against ESN. Immunisation is mainly mediated by up-regulation of SA-dependent defence genes, such as pathogenesis-related genes (PR-genes). Immunisation is systemic and can also work against herbivorous insects.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Adam, M., Heuer, H. & Hallmann, J. (2014). Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS ONE, e90402. DOI: 10.1371/journal.pone.0090402
Amiard, V., Demmig-Adams, B., Mueh, K.E., Turgeon, R., Combs, A.F. & Adams III, W.W. (2007). Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development. New Phytologist 173, 722-731. DOI: 10.1111/j.1469-8137.2006.01954.x
Barcala, M., Garcia, A., Cabrera, J., Casson, S., Lindsey, K., Favery, B., García-Casado, G., Solano, R., Fenoll, C. & Escobar, C. (2010). Early transcriptomic events in microdissected Arabdopsis nematode-induced giant cells. Plant Journal of Cell Molecular Biology 61, 698-712. DOI: 10.1111/j.1365-313X.2009.04098.x
Bar-Or, C., Kapulnik, Y. & Koltai, H. (2005). A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. European Journal of Plant Pathology 111, 181-192. DOI: 10.1007/s10658-004-2134-z
Bhattarai, K.K., Xie, Q.-G., Mantelin, S., Bishnoi, U., Girke, T., Navarre, D.A. & Kaloshian, I. (2008). Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant – Microbe Interactions 21, 1205-1214. DOI: 10.1094/MPMI-21-9-1205
Broin, M., Cuiné, S., Eymery, F. & Rey, P. (2002). The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14, 1417-1432. DOI: 10.1105/tpc.001644
Burkett-Cadena, M., Kokalis-Burelle, N., Lawrence, K.S., van Santen, E. & Kloepper, J.W. (2008). Suppressiveness of root-knot nematodes mediated by rhizobacteria. Biological Control 47, 55-59. DOI: 10.1016/j.biocontrol.2008.07.008
Cameron, D.D., Neal, A.L., Van Wees, S.C.M. & Ton, J. (2013). Mycorrhiza-induced resistance: more than the sum of its parts? Trends in Plant Science 18, 539-545. DOI: 10.1016/j.tplants.2013.06.004
Cao, H., Bowling, S.A., Gordon, A.S. & Dong, X. (1994). Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583-1592. DOI: 10.1105/tpc.6.11.1583
Chronis, D., Chen, S., Lu, S., Hewezi, T., Carpenter, S.C.D., Loria, R., Baum, T.J. & Wang, X. (2013). A ubiquitin carboxyl extension protein secreted from a plant parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. The Plant Journal 74, 185-196. DOI: 10.1111/tpj.12125
Conrath, U., Beckers, G.J.M., Langenbach, C.J.G. & Jaskiewicz, M.R. (2015). Priming for enhanced defense. Annual Review of Phytopathology 53, 97-119. DOI: 10.1146/annurev-phyto-080614-120132
Dos Santos, C.V. & Rey, P. (2006). Plant thioredoxins are key actors in the oxidative stress response. Trends in Plant Science 11, 329-334. DOI: 10.1016/j.tplants.2006.05.005
Doyle, E.A. & Lambert, K.N. (2003). Meloidogyne javanica chorismate mutase 1 alters plant cell development. Molecular Plant-Microbe Interactions 16, 123-131. DOI: 10.1094/MPMI.2003.16.2.123
Druzhinina, I.S., Seidl-Seiboth, V., Herrera-Estrella, A., Horwitz, B.A., Kenerley, C.M., Monte, E., Mukherjee, P.K., Zeilinger, S., Grigoriev, I.V. & Kubicek, C.P. (2011). Trichoderma: the genomics of opportunistic success. Nature Reviews 9, 749-759. DOI: 10.1038/nrmicro2637
Durrant, W.E. & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology 42, 185-209. DOI: 10.1146/annurev.phyto.42.040803.140421
Fu, Z.Q. & Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64, 839-863. DOI: 10.1146/annurev-arplant-042811-105606
Fudali, S.L., Wang, C. & Williamson, V.M. (2013). Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla. Molecular Plant-Microbe Interactions 26, 75-86. DOI: 10.1094/MPMI-05-12-0107-R
Gheysen, G. & Mitchum, M.G. (2019). Phytoparasitic nematode control of plant hormone pathways. Plant Physiology 179, 1212-1226. DOI: 10.1104/pp.18.01067
Glazebook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205-227. DOI: 10.1146/annurev.phyto.43.040204.135923
Gutjahr, C. & Paszkowski, U. (2009). Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Molecular Plant-Microbe Interactions 22, 763-772. DOI: 10.1094/MPMI-22-7-0763
Haegeman, A., Mantelin, S., Jones, J.T. & Gheysen, G. (2012). Functional roles of effectors of plant-parasitic nematodes. Gene 492, 19-31. DOI: 10.1016/j.gene.2011.10.040
Jaouannet, M., Magliano, M., Arguel, M.J., Gourgues, M., Evangelisti, E., Abad, P. & Rosso, M.N. (2013). The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions 26, 97-105. DOI: 10.1094/MPMI-05-12-0130-R
Jones, J.D.G. & Dangl, J.L. (2006). The plant immune system. Nature 444, 323-329. DOI: 10.1038/nature05286
Kaloshian, I., Desmond, O. & Atamian, H. (2011). Disease resistance-genes and defense responses during incompatible interactions. In: Jones, J., Gheysen, G. & Fenoll, C. (Eds). Genomics and molecular genetics of plant-nematode interactions. Dordrecht, The Netherlands, Springer, pp. 309-324.
Kammerhofer, N., Radakovic, Z., Regis, J.M.A., Dobrev, P., Vankova, R., Grundler, F.M.W., Siddique, S., Hofmann, J. & Wieczorek, K. (2015). Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytologist 207, 778-789. DOI: 10.1111/nph.13395
Leonetti, P., Costanza, A., Zonno, M.C., Molinari, S. & Altomare, C. (2014). How fungi interact with nematode to activate the plant defence response in tomato plants. Communications in Agricultural and Applied Biology Science 79, 357-363.
Leonetti, P., Zonno, M.C., Molinari, S. & Altomare, C. (2017). Induction of SA-signaling pathway and ethylene biosynthesis in Trichoderma harzianum-treated tomato plants after infection of the root-knot nematode Meloidogyne incognita. Plant Cell Reports 36, 621-631. DOI: 10.1007/s00299-017-2109-0
Lin, B., Zhuo, K., Chen, S., Hu, L., Sun, L., Wang, X., Zang, L.-H. & Liao, J. (2016). A novel nematode effector suppresses plant immunity by activating host reactive oxygen species-scavenging system. New Phytologist 209, 1159-1173. DOI: 10.1111/nph.13701
Manohar, M., Tenjo-Castano, F., Chen, S., Zhang, Y.K., Kumari, A., Williamson, V.M., Wang, X., Klessig, D.F. & Schroeder, F.C. (2020). Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nature Communications 11, 208. DOI: 10.1038/s41467-019-14104-2
Manosalva, P., Manohar, M., von Reuss, S.H., Chen, S., Koch, A., Kaplan, F., Choe, A., Micikas, R.J., Wang, X., Kogel, K.-H. et al. (2015). Conserved nematode signalling molecules elicitplant defenses and pathogen resistance. Nature Communications 6, 7795. DOI: 10.1038/ncomms8795
Mantelin, S., Thorpe, P. & Jones, J.T. (2015). Suppression of plant defences by plant-parasitic nematodes. Advances in Botanical Research 73, 325-337. DOI: 10.1016/bs.abr.2014.12.011
Martínez-Medina, A., Fernandez, I., Lok, G.B., Pozo, M.J., Pieterse, C.M.J. & Van Wees, S.C.M. (2017). Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytologist 213, 1363-1377. DOI: 10.1111/nph.14251
Molinari, S. (1991). Role of alternative pathway respiration in tomato roots attacked by Meloidogyne incognita. Annals of Applied Biology 119, 373-379. DOI: 10.1111/j.1744-7348.1991.tb04877.x
Molinari, S. (2001). Inhibition of H2O2-degrading enzymes in the response of Mi-bearing tomato to root-knot nematodes and salicylic acid treatment. Nematologia Mediterranea 29, 235-239.
Molinari, S. (2007). New developments in understanding the role of salicylic acid in plant defence. CAB Reviews 2, 1-10. DOI: 10.1079/PAVSNNR20072067
Molinari, S. (2009). Antioxidant enzymes in (a)virulent populations of root-knot nematodes. Nematology 11, 689-697. DOI: 10.1163/156854108X399317
Molinari, S. (2011). Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Reports 30, 311-323. DOI: 10.1007/s00299-010-0972-z
Molinari, S. (2016). Systemic acquired resistance activation in Solanaceous crops as a management strategy against root-knot nematodes. Pest Management Science 72, 888-896. DOI: 10.1002/ps.4063
Molinari, S. & Leonetti, P. (2019). Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes. PLoS ONE 14, e0213230. DOI: 10.1371/journal.pone.0213230
Molinari, S. & Loffredo, E. (2006). The role of salicylic acid in defense response of tomato to root-knot nematodes. Physiological and Molecular Plant Pathology 68, 69-78. DOI: 10.1016/j.pmpp.2006.07.001
Molinari, S., Fanelli, E. & Leonetti, P. (2014). Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Molecular Plant Pathology 15, 255-264. DOI: 10.1111/mpp.12085
Moore, A.L., Albury, M.S., Crichton, P.G. & Affourtit, C. (2002). Function of the alternative oxidase: is it still a scavenger? Trends in Plant Science 7, 478-481. DOI: 10.1016/s1360-1385(02)02366-x
Nahar, K., Kyndt, T., De Vleesschauwer, D., Höfte, M. & Gheysen, G. (2011). The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiology 157, 305-316. DOI: 10.1104/pp.111.177576
Nürnberger, T. & Brunner, F. (2002). Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Current Opinion in Plant Biology 5, 1-7. DOI: 10.1016/S1369-5266(02)00265-0
Paszkowski, U. (2006). Mutualism and parasitism: the yin and yang of plant symbioses. Current Opinion in Plant Biology 8, 1-10. DOI: 10.1016/j.pbi.2006.05.008
Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees, S.C.M. & Bakker, P.A.H.M. (2014). Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology 52, 347-375. DOI: 10.1146/annurev-phyto-082712-102340
Pineda, A., Zheng, S.J., Van Loon, J.J.A., Pieterse, C.M.J. & Dicke, M. (2010). Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in Plant Science 15, 507-514. DOI: 10.1016/j.tplants.2010.05.007
Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andrés, M.F., Emiliozzi, M., Oliveros, J.C., García-Casado, G., Solano, R., Koltai, H. et al. (2013). Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. New Phytologist 197, 1276-1290. DOI: 10.1111/nph.12121
Pozo, M.J. & Azcón-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393-398. DOI: 10.1016/j.pbi.2007.05.004
Qiu, Y., Xi, J., Du, L., Roje, S. & Poovaiah, B.W. (2012). A dual regulatory role of Arabidopsis calreticulin-2 in plant innate immunity. The Plant Journal 69, 489-500. DOI: 10.1111/j.1365-313X.2011.04807.x
Shoresh, M., Harman, G.E. & Mastouri, F. (2010). Induced systemic resistance and plant responses to fungal biocontrol agents. Annual Review of Phytopathology 48, 21-43.
Shouteden, N., De Waele, D., Panis, B. & Vos, C.M. (2015). Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Frontiers in Microbiology 6, 1280. DOI: 10.3389/fmicb.2015.01280
Shukla, N., Yadav, R., Kaur, P., Rasmussen, S., Goel, S., Agarwal, M., Jagannath, A., Gupta, R. & Kumar, A. (2017). Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-infected tomato (Solanum lycopersicum) roots reveals complex gene expression profiles and metabolic networks of both host and nematode during susceptible and resistance responses. Molecular Plant Pathology 19, 615-633. DOI: 10.1111/mpp.12547
Siddiqui, I.A. & Shaukat, S.S. (2002). Rhizobacteria-mediated induction of systemic resistance (ISR) in tomato against Meloidogyne javanica. Journal of Phytopathology 150, 469-473. DOI: 10.1046/j.1439-0434.2002.00784.x
Song, Y., Chen, D., Lu, K., Sun, Z. & Zeng, R. (2015). Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science 6, 786. DOI: 10.3389/fpls.2015.00786
Spoel, S.H. & Dong, X. (2012). How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews 12, 89-100. DOI: 10.1038/nri3141
Szabó, M., Csepregi, K., Gálber, M., Virányi, F. & Fekete, C. (2012). Control plant-parasitic nematodes with Trichoderma species and nematode-trapping fungi: the role of chi18-5 and chi18-12 genes in nematode egg-parasitism. Biological Control 63, 121-128. DOI: 10.1016/j.biocontrol.2012.06.013
Torres, M.A. (2010). ROS in biotic interactions. Physiologia Plantarum 138, 414-429. DOI: 10.1111/j.1399-3054.2009.01326.x
Uehara, T., Sugiyama, S., Matsura, H., Arie, T. & Masuta, C. (2010). Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant & Cell Physiology 51, 1524-1536. DOI: 10.1093/pcp/pcq109
Vallad, G.E. & Goodman, R.M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science 44, 1920-1934. DOI: 10.2135/cropsci2004.1920
Vieira, P. & Gleason, C. (2019). Plant-parasitic nematode effectors – insights into their diversity and new tools for their identification. Current Opinion in Plant Biology 50, 37-43.
Vos, C., Schouteden, N., Van Tuinen, D., Chatagnier, O., Elsen, A., De Waele, D., Panis, B. & Gianinazzi-Pearson, V. (2013). Mycorrhiza-induced resistance against the root-knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biology & Biochemistry 60, 45-54. DOI: 10.1016/j.soilbio.2013.01.013
Walters, D.R. (2010). Induced resistance: destined to remain on the sidelines of crop protection? Phytoparasitica 38, 1-4. DOI: 10.1007/s12600-009-0067-y
Walters, D.R., Walsh, D., Newton, A.C. & Lyon, G.D. (2005). Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95, 1368-1373. DOI: 10.1094/PHYTO-95-1368
Wang, H., Huang, Z., Chen, Q., Zhang, Z., Zhang, H., Wu, Y., Huang, D. & Huang, R. (2004). Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Molecular Biology 55, 183-192. DOI: 10.1007/s11103-004-0113-6
Wondafrash, M., Van Dam, N.M. & Tytgat, T.O.G. (2013). Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Frontiers in Plant Science 4, 1-15. DOI: 10.3389/fpls.2013.00087
Woo, S.L., Ruocco, M., Vinale, F., Nigro, M., Marra, R., Lombardi, N., Pascale, A., Lanzuise, S., Manganiello, G. & Lorito, M. (2014). Trichoderma-based products and their widespread use in agriculture. The Open Mycology Journal 8, 127-139. DOI: 10.2174/1874437001408010071
Wubben, M.J.E., Jin, J. & Baum, T.J. (2008). Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Molecular Plant-Microbe Interactions 21, 424-432. DOI: 10.1094/MPMI-21-4-0424
Xie, J., Li, S., Mo, C., Wang, G., Xiao, X. & Xiao, Y. (2016). A novel Meloidogyne incognita effector Misp12 suppresses plant defence response at latter stages of nematode parasitism. Frontiers in Plant Science 7, 1-12. DOI: 10.3389/fpls.2016.00964
Zipfel, C. & Oldoryd, G.E.D. (2017). Plant signalling in symbiosis and immunity. Nature 543, 328-336. DOI: 10.1038/nature22009
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1176 | 352 | 37 |
| Full Text Views | 64 | 7 | 0 |
| PDF Views & Downloads | 79 | 4 | 0 |
Plants have an immune system that can be exerted by every cell against a vast array of pathogens and parasites. This immune system has several levels of specialisation. A first level induces a general basal defence, after which specific pathogen-associated molecular patterns (PAMPs) are recognised by plant receptors. Normally, this basal defence is overcome by specialised pests by secreting specific effectors that suppress this first line of defence. Plant-parasitic nematodes have been found to secrete several such effectors through amphid and cuticle secretions or directly into the cells through their stylets. Many studies carried out on endoparasitic sedentary nematodes (ESN), in particular, reported the suppression of plant defence, especially in terms of down-regulation of the genes involved in salicylic acid (SA)-mediated defence, in the very first stages of plant-nematode interaction. However, plants can be immunised or primed against nematode attacks. Immunised plants respond to nematode infection more rapidly and efficiently and let a minor number of invasive juveniles become sedentary, develop to gravid females and reproduce. Immunisation of plants can be achieved by pre-treatments with chemicals that are functional analogues of the phytohormones that mediate defence reactions, such as salicylic acid (SA). Moreover, plants provided with the beneficial microorganisms commonly present in a healthy rhizosphere, such as arbuscular mycorrhizal fungi or opportunistic symbiotic fungi, have been found to be immunised against ESN. Immunisation is mainly mediated by up-regulation of SA-dependent defence genes, such as pathogenesis-related genes (PR-genes). Immunisation is systemic and can also work against herbivorous insects.
| All Time | Past 365 days | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1176 | 352 | 37 |
| Full Text Views | 64 | 7 | 0 |
| PDF Views & Downloads | 79 | 4 | 0 |