Differential response of some nematode-resistant and susceptible tomato genotypes to Meloidogyne javanica infection
More details
Hide details
Department of Biology, Faculty of Science and Art-Khulais, University of Jeddah, Saudi Arabia
Department of Plant Pathology, Faculty of Agriculture, Ain Shams University, Egypt
Dean of Scientific Research, University of Jeddah, Saudi Arabia
A - Research concept and design; B - Collection and/or assembly of data; C - Data analysis and interpretation; D - Writing the article; E - Critical revision of the article; F - Final approval of article
Mohamed Youssef Banora   

Department of Biology, Faculty of Science and Art-Khulais, University of Jeddah, Saudi Arabia
Online publish date: 2019-04-12
Submission date: 2018-10-18
Acceptance date: 2019-03-13
Journal of Plant Protection Research 2019;59(1):113–123
Resistance genes in response to root-knot nematode (Meloidogyne javanica) infection suppress one or more of several critical steps in nematode parasitism and their reproduction rate. The reaction of seven commercial tomato genotypes to M. javanica infection was investigated under greenhouse conditions. Current results classified these genotypes as: three resistant (Jampakt, Malika and Nema Guard), one moderately resistant (Fayrouz), and three susceptible (Castle Rock, Super Marmande and Super Strain B). Except Nema Guard, nematode infection significantly reduced plant height, fresh and dry weights of shoots of the other tomato genotypes. Leaf area was significantly reduced for all examined tomato genotypes except Malika and Nema Guard. Total chlorophyll was reduced in all tested tomato genotypes except Jampakt. Infection parameters of M. javanica and their population were significantly reduced on all nematode-resistant tomato genotypes compared to the susceptible genotypes. Also, the maturation rate of M. javanica was suppressed in the resistant genotypes compared to the susceptible genotypes. These results were confirmed by histological study that illustrated a delay in nematode development and their maturation. Total phenolic content significantly increased in nematode infected roots of both resistant and susceptible genotypes except Malika. Among non-infected roots, Malika showed the highest level of total phenols while after M. javanica infection, Nema Guard revealed the highest level of total phenols. Among infected roots, the highest level of total phenols was recorded in Castle Rock. These results suggested that using nematode-resistant tomato genotypes could provide an efficient and nonpolluting method to control root-knot nematodes.
The authors have declared that no conflict of interests exist.
Abad P., Favery B., Rosso M., Castagnone-Sereno P. 2003. Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Molecular Plant Pathology 4 (4): 217–224. DOI: https://doi.org/10.1046/j.1364....
Abd-Elgawad M.M.M., Askary T.H. 2015. Impact of phytonematodes on agriculture economy. In: “Agents of Phytonematodes “(T.H. Askary, P.R.P. Martinelli, eds). Biocontrol, CAB International, 23 pp.
Abdul-Baki A., Haroon A.S.A., Chitwood D.J. 1996. Temperature effects on resistance to Meloidogyne spp. in excised tomato roots. Horticultural Science 4 (23): 147–149.
Ahmad G., Khan A.A., Ansari S. 2017. Interaction of a fly ash and root-knot nematode pathogens on Pumpkin (Cucurbita moschata Duch. ex Lam.). Tropical Plant Research 4 (3): 449–455. DOI: 10.22271/tpr. 2017.v4.i3.059.
Anwar S.A., McKenry M.V. 2010. Incidence and reproduction of Meloidogyne incognita on vegetable crop genotypes. Pakistan Journal of Zoology 42 (2): 135−141.
Araujo M.T., Bassett M.J., Augustine J.J., Dickson D.W. 1982. Effect of diurnal changes in soil temperatures on resistance to Meloidogyne incognita in tomato. Journal of Nematology 14 (3): 414–416.
Atamian H.S., Eulgem T., Kaloshian I. 2012. SlWRKY70 is required for Mi1-mediated resistance to aphids and nematodes in tomato. Planta 235 (2): 299–309. DOI: 10.1007/s00425-011-1509-6.
Bai Y., Sunarti S., Kissoudis C., Visser R.G.F., van der Linden C.G. 2018. The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses. Frontiers in Plant Science 9: 801. DOI: 10.3389/fpls.2018.00801.
Bajaj K.L., Mahajan R. 1977. Phenolic compounds in tomato susceptible and resistant to Meloidogyne incognita (Kofoid & White) Chitwood. Nematologia Mediterranea 5 (2): 329–333.
Bhattarai K.K., Atamian H.S., Kaloshian I., Eulgem T. 2010. WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. The Plant Journal 63 (2): 229–240. DOI: 10.1111/j.1365-313X.2010.04232.x.
Bali S., Kaur P., Sharma A., Ohri P., Bhardwaj R., Alyemeni M.N., Wijaya L., Ahmad P. 2018. Jasmonic acid-induced tolerance to root-knot nematodes in tomato plants through altered photosynthetic and antioxidative defense mechanisms. Protoplasma 255 (2): 471−484. DOI: 10.1007/s00709-017-1160-6.
Banora M.Y. 2015. Pathogenic variability among eight populations of Meloidogyne javanica isolates on tomato plants. Egyptian Journal of Phytopathology 43 (1): 79−87.
Banora M.Y., Rodiuc N., Baldacci-Cresp F., Smertenko A., Bleve-Zacheo T., Mellilo M.T., Karimi M., Hilson P., Evrard J., Favery B., Engler G., Abad P., Engler J. 2011. Feeding cells induced by phytoparasitic nematodes require γ-tubulin ring complex for microtubule reorganization. PLoS Pathogens 7 (12): e1002343. DOI: 10.1371/journal.ppat.1002343.
Barker K.R. 1985. Nematode extraction and bioassays. In: “An Advanced Treatise on Meloidogyne: 2. Methodology” (K.R. Barker, C.C. Carter, J.N. Sasser, eds.). North Carolina State University, 30 pp.
Bendezu I.F., Starr J. 2003. Mechanism of resistance to Meloidogyne arenaria in the peanut genotype COAN. Journal of Nematology 35 (1): 115–118.
Bhau B.S., Borah B., Ahmed R., Phukon P., Gogoi B., Sarmah D.K., Lal M., Wann S.B. 2016. Influence of root-knot nematode infestation on antioxidant enzymes, chlorophyll content and growth in Pogostemon cablin (Blanco) Benth. Indian Journal of Experimental Biology 54 (4): 254−261.
Bleve-Zacheo T., Melillo M.T., Castagnone-Sereno P. 2007. The contribution of biotechnology to root-knot nematode control in tomato plants. Pest Technology 1 (1): 1−16.
Chin S., Behm C.A., Mathesius U. 2018. Functions of flavonoids in plant-nematode interactions. Plants 7 (4): 85−102. DOI: 10.3390/plants7040085.
Corbett B.P., Jia l., Sayler R. J., Arevalo-Soliz M., Goggin F. 2011. The effects of root-knot nematode infection and Mi-mediated nematode resistance in tomato on plant fitness. Journal of Nematology 43 (2): 82–89.
Demmig-Adams B., Adams W.W. 1992. Carotenoid composition in sun and shade leaves of plants with different life forms. Plant Cell and Environment 15 (4): 411–419. DOI: https://doi.org/10.1111/j.1365....
Devran Z., Sogut M.A., Mutlu N. 2010. Response of tomato rootstocks with the Mi resistance gene to Meloidogyne incognita race 2 at different soil temperatures. Phytopathologia Mediterranea 49 (1): 11–17. DOI: http://dx.doi.org/10.14601/Phy....
Di Vito M., Volvos N., Castillo P. 2004. Host parasite relationship of Meloidogyne incognita on spinach. Plant Pathology 53 (4): 508−514.
Dropkin V.H. 1969. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: reversal by temperature. Phytopathology 59 (12): 1632–1637.
Fortnum B.A., Kasperbauer M.J., Hunt P.G., Bridges W.C. 1991. Biomass partitioning in tomato plants infected with Meloidogyne incognita. Journal of Nematology 23 (3): 291–297.
Giné A., López-Gómez M., Vela M.D., Ornat C., Talavera M., Verdejo-Lucas S., Sorribas F.J. 2014. Thermal requirements and population dynamics of root-knot nematodes on cucumber and yield losses under protected cultivation. Plant Pathology 63 (6): 1446–1453. DOI: https://doi.org/10.1111/ppa.12....
Hadisoeganda W.W., Sasser J.N. 1982. Resistance of tomato, bean, southern pea, and garden pea cultivars to root-knot nematodes based on host suitability. Plant Disease 66 (1): 145–150.
Haseeb A., Srivastava N.K., Pandey R. 1990. The influence of Meloidogyne incognita on growth, physiology, nutrient concentration and alkaloid yield of Hyoscyamus niger. Nematologia Mediterranea 18 (2): 127–129.
Heikal A.M., Solliman M., Aboul-Enein A.A., Ahmed F.A., Abbas A., Taha H.S., Handa A.K. 2008. Tfg-Mi, a root-knot nematode resistance gene from fenugreek (Trigonella foenum-graecum) confers nematode resistance in tomato. Arab Journal of Biotechnology 11 (2): 139−158.
Hung C.G., Rohde R.A. 1973. Phenol accumulation related to resistance in tomato to infection by root-knot and lesion nematodes. Journal of Nematology 5 (4): 253−258.
Hussey R.S. 1985. Host-parasite relationships and associated physiological changes. In: “An Advanced Treatise on Meloidogyne. Vol. I: Biology and Control” (J.N. Sasser, C.C. Carter eds), North Carolina State University Graphics, Raleigh, NC, USA, 143 pp.
Hussey R.S., Williamson V.M. 1998. Physiological and molecular aspects of nematode parasitism. In: “Plant and Nematode Interactions” (K.R. Barker, G.A. Pederson, G.L. Windham, eds). American Society of Agronomy, Madison, WI, USA, 87 pp.
Hwang C.F., Bhakta A.V., Truesdell G.M., Pudlo W.M., Williamson V.M. 2000. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12 (8): 1319–1329. DOI: https://doi.org/10.1105/tpc.12....
Irshad U., Mukhtar T., Ashfaq M., Kayani M.Z., Kayani S.B., Hanif M., Aslam S. 2012. Pathogenicity of citrus nematode (Tylenchulus semipenetrans) on Citrus jambhiri. Journal of Animal and Plant Science 22 (4): 1014−1018.
Jacquet M., Bongiovanni M., Martinez M., Verschave P., Wajnberg E., Castagnone-Sereno P. 2005. Variation in resistance to the root-knot nematode Meloidogyne incognita in tomato genotypes bearing the Mi gene. Plant Pathology 54 (2): 93–99. DOI: 10.1111/j.1365-3059.2005.01143.x.
Jansky S.H., Simon R., Spooner D.M. 2008. A test of taxonomic predictivity: Resistance to early blight in wild relatives of cultivated potato. Phytopathology 98 (6): 680–687. DOI: 10.1094/PHYTO-98-6-0680.
Kaloshian I., Yaghoobi J., Liharska T., Hontelez J., Hanson D. 1998. Genetic and physical localization of the root-knot nematode-resistance locus Mi in tomato. Molecular and General Genetics 257 (3): 376–385.
Karkute S.G., Gujjar R.S., Rai A., Akhtar M., Singh M. 2018. Genome wide expression analysis of WRKY genes in tomato (Solanum lycopersicum) under drought stress. Plant Gene 13 (1): 8–17. DOI: 10.1016/j.plgene.2017.11.002.
Karpinski S., Gabrys H., Mateo A., Karpinska B., Mullineaux P.M. 2003. Light perception in plant disease defense signaling. Current Opinion in Plant Biology 6 (4): 390–396. DOI: https://doi.org/10.1016/S1369-....
Karssen G., Moens M. 2006. Root-knot nematodes. In: “Plant Nematology” (R.N. Perry, M. Moens, eds). CABI Publishing, 59 pp.
Khan M.R., Khan M.W. 1997. Effects of the root-knot nematode, Meloidogyne incognita, on the sensitivity of tomato to sulfur dioxide and ozone. Environmental and Experimental Botany 38 (2): 117−130. DOI: https://doi.org/10.1016/S0098-....
Korves T., Bergelson J. 2004. A novel cost of R gene resistance in the presence of disease. The American Naturalist 163 (4): 489−504. DOI: 10.1086/382552.
Loveys R.R., Bird A.F. 1973. The influence of nematodes on photosynthesis in tomato plants. Physiological Plant Pathology 3 (4): 525–529. DOI: https://doi.org/10.1016/0048-4....
Lu P., Davis R.F., Kemerait R.C., Van Iersel M.W., Scherm H. 2014. Physiological effects of Meloidogyne incognita infection on cotton genotypes with differing levels of resistance in the greenhouse. Journal of Nematology 46 (4): 352–359.
Maleita C.M., dos Santos M.C.V., Curtis R.H.C., Powers S.J., Abrantes I.M.D.O. 2011. Effect of the Mi-gene on reproduction of Meloidogyne hispanica on tomato genotypes. Nematology 13 (8): 939−949. DOI: 10.1163/138855411X566449.
Mantelin S., Bhattarai K.K., Jhaveri T.Z., Kaloshian I. 2013. Mi-1-mediated resistance to Meloidogyne incognita in tomato may not rely on ethylene but hormone perception through ETR3 participates in limiting nematode infection in a susceptible host. PLoS One 8 (5): 1–8. DOI: https://doi.org/10.1371/journa....
Mekete T., Mandefro W., Greco N. 2003. Relationship between initial population densities of Meloidogyne javanica and damage to pepper and tomato in Ethiopia. Nematologia Mediterranea 31 (2): 169‒171.
Melakeberhan H., Brook R.C., Webster J.M. 1986. Relationship between physiological response of French beans of different age to Meloidogyne incognita and subsequent yield loss. Plant Pathology 35 (2): 203–213. DOI: https://doi.org/10.1111/j.1365....
Melakeberhan H., Webster J.M., Brooke R.C., D’Auria J.M., Cackette M. 1987. Effect of Meloidogyne incognita on plant nutrient concentration and its influence on the physiology of beans. Journal of Nematology 19 (3): 324–330.
Messeguer R., Ganal M., de Vicente M.C., Young N.D., Bolkan H., Tanksley S.D. 1991. High resolution RFLP map around the root knot nematode resistance gene (Mi) in tomato. Theoretical Applied Genetics 82 (5): 529–536.
Milligan S.B., Bodeau J., Yaghoobi J., Kaloshian I., Zabel P., Williamson V.M. 1998. The root-knot resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10 (8): 1307–1319. DOI: https://doi.org/10.1105/tpc.10....
Molinari S. 2011. Natural genetic and induced plant resistance, as a control strategy to plant-parasitic nematodes alternative to pesticides. Plant Cell Reports 30 (3): 311−323.
Mukhtar T., Hussain M.A., Kayani M.Z., Aslam M.N. 2014. Evaluation of resistance to root-knot nematode (Meloidogyne incognita) in okra cultivars. Crop Protection 56 (1): 25−30. DOI: https://doi.org/10.1016/j.crop....
Ohri P., Pannu S.K. 2010. Effect of phenolic compounds on nematodes − A review. Journal of Applied and Natural Science 2 (2): 344−350. DOI: https://doi.org/10.31018/jans.....
Ornat C., Verdejo-Lucas S., Sorribas F.J. 2001. A population of Meloidogyne javanica from Spain virulent to the Mi resistance gene in tomato. Plant Disease 85 (3): 271–276.
Patel V.S., Shukla Y.M., Dhruve J.J. 2017. Influence of root knot nematode (Meloidogyne spp.) on phenolic acid profile in root of tomato (Solanum lycopersicum L.). International Journal of Current Microbiology and Applied Sciences 6 (10): 840−848. DOI: https://doi.org/10.20546/ijcma....
Reddy P.P. 1983. Plant Nematology. Agricole publishing academy (APA), New Delhi, 10 pp.
Roberts P.A., Thomason I.J. 1986. Variability in reproduction of isolates of Meloidogyne incognita and M. javanica on resistant tomato genotypes. Plant Disease 70 (4): 547–551.
Sas institute. 1992. SAS Proprietary Software Release 6.08 TS 404 Licensed to Mcgill University Computing Centre, Site 0009211001. Sas institute Inc., Cary, N.C., 27513, USA.
Rodiuc N., Vieira P., Banora M.Y., de Almeida Engler J. 2014. On the track of transfer cell formation by specialized plantparasitic nematodes. Frontiers in Plant Science 5 (5): 160. DOI: 10.3389/fpls.2014.00160.
Sasser J.N., Carter C.C., Hartman K.M. 1984. Standardization of Host Suitability Studies and Reporting of Resistance to Root-knot Nematodes. North Carolina State Graphics, Raleigh, NC, USA, 7 pp.
Sharma J.L., Trevidi P.C., Sharma M.K., Jiagi B. 1990. Alteration in prolin and phenol content of Meloidogyne incognita infected bringal cultivars. Pakistan Journal of Nematology 8 (1): 33–38.
Singleton V.L., Orthofer R., Lamuela-Raventos R.M. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 299 (1): 152−178. DOI: https://doi.org/10.1016/S0076-....
Strajnar P., Širca S., Urek G., Šircelj H., Železnik P., Vodnik D. 2012. Effect of Meloidogyne ethiopica parasitism on water management and physiological stress in tomato. European Journal of Plant Pathology 132 (1): 49–57. DOI 10.1007/s10658-011-9847-6.
Swain B., Prasad J.S. 1988. Chlorophyll content in rice as influenced by the root-knot nematode, Meloidogyne graminicola infection. Current Science 57 (16): 895–896.
Taiz L., Zeiger E. 2002. Plant Physiology. 3rd ed. Sinaur Associates Inc, Sunderland, MA, USA, 290 pp.
Talavera M., Verdejo-Lucas S., Ornat C., Torres J., Vela M.D., Macias F.J., Cortada L., Arias D.J., Valero J., Sorribas F.J. 2009. Crop rotations with Mi gene resistant and susceptible tomato cultivars for management of root-knot nematodes in plastic houses. Crop Protection 28 (8): 662–667. DOI: https://doi.org/10.1016/j.crop.....
Taylor A.L., Sasser J.N. 1978. Biology, identification and control of root-knot nematodes (Meloidogyne Species). Raleigh, North Carolina State University, and US/AID, 111 pp.
Tzortzakakis E.G., Gowen S.R. 1996. Occurrence of resistance breaking pathotypes of Meloidogyne javanica on tomatoes in Crete, Greece. Fundamental and Applied Nematology 19 (3): 283–288.
Tzortzakakis E.A., Trudgill D.L., Phillips M.S. 1998. Evidence for a dosage effect of the Mi gene on partially virulent isolates of Meloidogyne javanica. Journal of Nematology 30 (1): 76–80.
Verdejo-Lucas S., Blanco M., Cortada L., Javier Sorribas F. 2013. Resistance of tomato rootstocks to Meloidogyne arenaria and Meloidogyne javanica under intermittent elevated soil temperatures above 28°C. Crop Protection 46 (1): 57–62. DOI: https://doi.org/10.1016/j.crop....
Williamson V.M. 1999. Plant nematode resistance genes. Current Opinion in Plant Biology 2 (4): 327‒331. DOI: 10.1016/S1369-5266(99)80057-0.
Williamson V.M., Kumar A. 2006. Nematode resistance in plants: The battle underground. Trends in Genetics 22 (7): 396−403. DOI: https://doi.org/10.1016/j.tig.....