Biochemical defense response of the greenhouse cucumber (Cucumis sativus L.) to complex disease caused by a root-knot nematode and Fusarium wilt fungus
Subject Areas : Genetic
Mehdi Mohamadian Sarcheshmeh
1
,
Saeed Rezaee
2
,
Alireza Iranbakhsh
3
1 - Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran, Iran.
2 - Department of Plant Protection, Faculty of Agricultural Sciences and Food Industries, Science and Research Branch, Islamic Azad University, Tehran, Iran
3 - Department of Biology, . Science and Research Branch, Islamic Azad University, Tehran, Iran.
Keywords: interaction, root-knot nematode, Meloidogyne javanica, cucumber, peroxidase, phenolic compounds, Fusarium oxysparum f. sp. radicis-cucumerinum,
Abstract :
Complex disease caused by the root-knot nematode, Meloidogyne javanica, and the fungus, Fusarium oxysporum f. sp. radicis-cucumerinum, has limited cucumber cultivation in Iran. Therefore, access to the nematode-resistant cultivars has a crucial role in disease control. The Assessment of plant defense compounds in the Complex disease helps understand the molecular mechanisms of resistance and the production of nematode-resistant cultivars. After inoculation of the plants in a greenhouse, the peroxidase enzyme and the phenolic compounds were measured using spectrophotometric method. The experiment was conducted based on a factorial completely randomized designed with 14 treatments, including control, fungi alone, nematode alone in four inoculations level viz. 1500, 3000, 4500, and 6000 J2s, fungus + nematode simultaneously, and fungus a week after nematode inoculation with 4 replications. Phenolic compounds increased by %54.74 and %92.34 and peroxidase enzyme activity increased by %50.64 and %63.31 in plants inoculated with fungus alone and nematode alone (6000 larvae) compared to the control, showing that these substances act as defensive compounds in cucumber. Results showed that increasing the nematode population in inoculated plants improved the defense compounds levels. Inoculation of nematode (6000 larvae) followed by fungus led to %80 and %54.48 increases in phenolic compounds and peroxidase activity, respectively as compared with the control which might be attributed to the synergistic effects of pathogens. The fungi had a more active role than nematodes in increasing the peroxidase compared to the phenolic compounds, which indicated the complex nature of nematode parasitism in the nematode-plant interaction. Decrease in the defense compounds in Negin cultivar (susceptible to Fusarium) and increase in the level of these compounds in Khasib (tolerant to Fusarium) and Dastjerdi (tolerant to nematode) cultivars showed that the production of the defensive compounds may be related to the cucumber resistance to pathogens.
Anterola, A. and Lewis, N G. (2002). Trends in lignification: a comprehensive analysis of the facts of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry. 61: 221-294.
Arnao, M.B. and Hernández-Ruiz, J. (2019). Melatonin: a new plant hormone and/or a plant master regulator?. Trends in Plant Science, 24(1): 38-48.
Bolwell, G.P. and Daudi, A. (2009). Reactive oxygen species in plant–pathogen interactions. In Reactive oxygen species in plant signaling. (pp. 113-133). Springer, Berlin, Heidelberg
Cao, J., Jiang, W. and He, H. (2005). Induced resistance in yali pear (Pyrus bretschneideri Rehd.) fruit against infection by Penicillium expansum by postharvest infiltration of acibenzolar‐S‐methyl. Journal of Phytopathology. 153: 640-646.
Chin, S., Behm, C.A. and Mathesius, U. (2018). Functions of flavonoids in plant–nematode interactions. Planta, 7(4): 85.
Cosio, C., Vuillemin, L., De Meyer, M., Kevers, C., Penel, C. and Dunand, C. (2009). An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta, 229(4): 823-836
D’Addabbo, T., Carbonara, T., Argentieri, M., Radicci, V., Leonetti, P. and Villanova, L. (2013). Nematicidal potential of Artemisia annua and its main metabolites. European Journal of Plant Pathology. 137(2): 295–304.
Dhakshinamoorthy, S., Mariama, K., Elsen, A. and De Waele, D. (2014). Phenols and lignin are involved in the defence response of banana (Musa) plants to Radopholus similis infection. Nematology, 16: 565–576.
Eisenback, J.D. (1985). Detailed morphology and anatomy of second-stage juveniles, males, and females of the genus Meloidogyne (root-knot nematodes). An advanced treatise on Meloidogyne, 1: 47-77.
Gheysen, G. and Mitchum, M.G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion on Plant Biology. 14(4): 415–421.
Hiraga, S. (2001). A large family of class III plant peroxidases,” Plant Cell and Physiology. 42: 462–468.
Hussey, R.S. and Barker, K.R. (1973). Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique, Plant Disease Reporters. 75: 1025-1028.
Jones J.T., Haegeman A., Danchin E.G., Gaur H.S., Helder J., Jones M.G. and Perry, R.N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathology. 14: 946–961.
Kadota, Y., Shirasu, K. and Zipfel, C. (2015). Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiology. 56(8): 1472–1480.
Maehly, A.C. and Chance, B. (1954). The assay of catalases and peroxidases., Methods of biochemical analysis. 1: 357–424.
Malik, C.P. and Singh, M B. (1980). Plant Enzymology and Histo Enzymology. Kalyani Publishers. New Delhi. 286pp
Mazzafera, P., Gonçalves, W. and Fernandes, J. (1989). Phenols, peroxidase and polyphenol oxidase in the resistance of coffee to Meloidogyne incognita. Bragantia. 48: 131-142.
Mishra, C. and Mohanty, K. (2007). Role of phenolics and enzymes in imparting resistance to rice plants against root-knot nematode, Meloidogyne graminicola, Indian journal of Nematology. 37: 131-134.
Mohamadian-Sarcheshmeh, M. and Ahmadi, A. (2014). The 1st international conference on new ideas in agriculture, The 1st international conference on new ideas in agriculture. p. 658.
Mohammadi, M. and Kazemi, H. (2002). Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance, Plant Sciencese. 162: 401-408.
Molinari, S. (1995). Role of oxidative and peroxidative processes in the plant-nematode interaction. Nematologia Mediterranea. 23: 69-73.
Moosavi, S.S., Karegar, A. and Deljoo, A. (2006). Responses of some common cucumber cultivars in Iran to root-knot nematode, Meloidogyne incognita, under greenhouse conditions. Iranian Journal of Plant Pathology. 42: 37-50.
Morkunas, I. and Gmerek, J. (2007). The possible involvement of peroxidase in defense of yellow lupine embryo axes against Fusarium oxysporum, Journal of Plant Physiology. 164: 185–194.
Niebel, A., Almeida, J. D., Tire, C., Engler, C., Van Montagu, G. and Gheysen, G. (1993). Induction Patterns of an extensin gene in tobacco upon nematode infection., Plant Cell. 5: 1697–1710.
Noel, G.R. and McClure, M.A. (1987). Peroxidase and 6-Phosphogluconate Dehydrogenase in resistant and susceptible cotton infected by Meloidogyne incognita. Journal of Nematology. 10: 34–38.
Oka, Y., Cohen, Y. and Spiegel, Y. (1999). Local and systemic induced resistance to the root-knot nematode in tomato by DL- β -amino- n -butyric acid. Phytopathology. 89: 1138–1143.
Ones, J.T., Haegeman, A., Danchin, E.G., Gaur, H.S., Helder, J. and Jones, M.G. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology. 14(9): 946–961.
Patel, B.A., Patel, D.J., Patel, N.B. and Patel, R.G. (2001). Determination of damaging threshold level of root-knot nematode Meloidogyne javanica pathotype 1 on chickpea, Int. Chickpea Pigeonpea Newsletter. 8: 9–11.
Pegard, A., Brizzard, G., Fazari, A., Soucaze, O., Abad, P. and Djian-Caporalino, C. (2005). Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology. 95: 158–165.
Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andrés, M. F., Emiliozzi, M. and Resnick, N. (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(4): 1276-1290
Qin, X. and Xiaoyan, Z. (2008). The relationship between resistance to Meloidogyne incognita and phenyl propanes in roots of egg plant rootstock, Acta Phytophylacica Sinica. 35 : 43-46.
Reuveni, M. (1998). Relationships between leaf age, peroxidase and beta-1,3-glucanase activity, and resistance to downy mildew in grapevines. Journal of Phytopathology. 146: 525–530.
Saeedizadeh, A., Kheiri, A., Zad, J. and Etebarian, H.R. (2009). A Study of the changes in total Phenol content in olive cultivars during the interaction between Verticillium wilt, Verticillium, and nematode. Iranian Journal Plant Protection Science. 42: 125–135.
Sahebani, N., Zad, J., Sharifitehrani, A. and Kheiri, A. (2008). A study of changes in peroxidase activity in the interaction between root-knot nematode (Meloidogyne javanica) and tomato Fusarium wilt agent (Fusarium oxysporium f. sp. lycopersisci), Tehran University. College of Agriculture. 39: 127–138.
Sari, E., Etebarian, H. R. and Aminian, H. (2008). Effects of Pseudomonas fluorescens CHA0 on the Resistance of wheat seedling roots to the take-all fungus Gaeumannomyces graminis var. tritici. Plant Protection Science. 11: 298–306.
Sari., E., Etebarian, H. R. and Aminian, H. (2007). The effects of Bacillus pumilus, isolated from wheat rhizosphere, on resistance in wheat seedling roots against the take-all fungus, Gaeumannomyces graminis var. tritici. Jornal of Phytopathology. 155: 720–727.
Sato, K., Kadota, Y. and Shirasu, K. (2019). Plant immune responses to plant parasitic nematodes. Frontiers in plant science, 10: 1165.
Shahriari D., Molavi, E., Aminian, H. and Etebarian, H.R. (2011). Histopathological response of resistant and susceptible cultivars of cucumber to Fusarium oxysporum f. sp. radicis-cucumerinum, the causal agent of fusarium stem and root rot. Seed Plant Improvement Journal. 27: 375–391.
Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. and Yoshimura, K. (2002). Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53(372): 1305-1319
Shokoohi, E., Kheiri, A., Etebarian, H.R. and Roostaei, A. (2003). Interactions between root-knot nematode Meloidogyne javanica and Fusarium wilt disease, Fusarium oxysporum f. sp. Melonis in different varieties of melon. Communication in Agriculture Applied Biology Sciencese. 69: 387–391.
Siddique, S., Matera, C., Radakovic, Z.S., Hasan, M.S., Gutbrod, P., Rozanska, E. and Grundler, F.M. (2014). Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Science Signaling, 7(320): ra33-ra33.
Singh, R.K. (2003). Studies on and predacity and biocontrol potential of Arthrobotrys oligospora. Ph.D Thesis. Banaras Hindu University. Varanasi, India. 353pp.
Sundararaju, P. and Suba, K. (2006). Biochemical and molecular changes in banana plants induced by Pratylenchus coffeae and Meloidogyne incognita, Indian Journal of Nematology. 36: 256-259.
Tarek Hewezi, J.J. and Baum, T.J. (2011). Arabidopsis peroxidase AtPRX53 influences cell elongation and susceptibility to Heterodera schachtii. Plant Signaling and Behavior, 6: 1778-1786.
Taylor, D. and Netscher, C. (1974). An improved technique for preparing perineal patterns of Meloidogyne spp. Nematologica. 20: 268-269.
Teixeira, M.A., Wei, L. and Kaloshian, I. (2016). Root-knot nematodes induce pattern-triggered immunity in Arabidopsis thaliana roots. New Phytopathology. 211(1): 276–287.
Torres, M.A., Jones, J.D. and Dangl, J.L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiology. 141(2): 373–378.
Vakalounakis D.J., Doulis, A.G. and Klironomou, E. (2005). Characterization of Fusarium oxysporum f. sp. radicis-cucumerinum attacking melon under natural conditions in Greece. Plant Pathology. 54: 339–346
VanderMolen, G.E., Beckman,C. H. and Rodehorst, E. (1977). Vascular gelation: a general response phenomenon following infection. Physiological Plant Pathology. 11(1): 95-100
Whitehead, A.G. and Hemming, J.R. (1965). A comparison of some quantitative methods of extracting small vermiform nematodes from the soil, Annual Applied Biology. 55: 25–38.
Wong, E. (1973). Plant phenolics, Chemistry and Biochemestry of Herb. 1: 265–322.
Yang, S., Dai, Y., Chen, Y., Yang, J., Yang, D. and Liu, Q. (2019). A novel G16B09-like effector from Heterodera avenae suppresses plant defenses and promotes parasitism. Frontier Plant Science. 10: 66.
Zacheo, G., Blevezacheo, T., Pacoda, C., Orlando, D. and Durbin, R. D. (1995). The Association between Heat-Induced Susceptibility of Tomato to Meloidogyne-Incognita and Peroxidase-Activity. Physiology and Molecular Plant Pathology. 46: 491–507.
Zhou, J., Xu, X.C., Cao, J.J., Yin, L.L., Xia, X.J. and Shi, K. (2018). Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production. Plant Physiology. 176(3): 2456–2471.
_||_
Anterola, A. and Lewis, N G. (2002). Trends in lignification: a comprehensive analysis of the facts of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry. 61: 221-294.
Arnao, M.B. and Hernández-Ruiz, J. (2019). Melatonin: a new plant hormone and/or a plant master regulator?. Trends in Plant Science, 24(1): 38-48.
Bolwell, G.P. and Daudi, A. (2009). Reactive oxygen species in plant–pathogen interactions. In Reactive oxygen species in plant signaling. (pp. 113-133). Springer, Berlin, Heidelberg
Cao, J., Jiang, W. and He, H. (2005). Induced resistance in yali pear (Pyrus bretschneideri Rehd.) fruit against infection by Penicillium expansum by postharvest infiltration of acibenzolar‐S‐methyl. Journal of Phytopathology. 153: 640-646.
Chin, S., Behm, C.A. and Mathesius, U. (2018). Functions of flavonoids in plant–nematode interactions. Planta, 7(4): 85.
Cosio, C., Vuillemin, L., De Meyer, M., Kevers, C., Penel, C. and Dunand, C. (2009). An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta, 229(4): 823-836
D’Addabbo, T., Carbonara, T., Argentieri, M., Radicci, V., Leonetti, P. and Villanova, L. (2013). Nematicidal potential of Artemisia annua and its main metabolites. European Journal of Plant Pathology. 137(2): 295–304.
Dhakshinamoorthy, S., Mariama, K., Elsen, A. and De Waele, D. (2014). Phenols and lignin are involved in the defence response of banana (Musa) plants to Radopholus similis infection. Nematology, 16: 565–576.
Eisenback, J.D. (1985). Detailed morphology and anatomy of second-stage juveniles, males, and females of the genus Meloidogyne (root-knot nematodes). An advanced treatise on Meloidogyne, 1: 47-77.
Gheysen, G. and Mitchum, M.G. (2011). How nematodes manipulate plant development pathways for infection. Current Opinion on Plant Biology. 14(4): 415–421.
Hiraga, S. (2001). A large family of class III plant peroxidases,” Plant Cell and Physiology. 42: 462–468.
Hussey, R.S. and Barker, K.R. (1973). Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique, Plant Disease Reporters. 75: 1025-1028.
Jones J.T., Haegeman A., Danchin E.G., Gaur H.S., Helder J., Jones M.G. and Perry, R.N. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Mol. Plant Pathology. 14: 946–961.
Kadota, Y., Shirasu, K. and Zipfel, C. (2015). Regulation of the NADPH oxidase RBOHD during plant immunity. Plant Cell Physiology. 56(8): 1472–1480.
Maehly, A.C. and Chance, B. (1954). The assay of catalases and peroxidases., Methods of biochemical analysis. 1: 357–424.
Malik, C.P. and Singh, M B. (1980). Plant Enzymology and Histo Enzymology. Kalyani Publishers. New Delhi. 286pp
Mazzafera, P., Gonçalves, W. and Fernandes, J. (1989). Phenols, peroxidase and polyphenol oxidase in the resistance of coffee to Meloidogyne incognita. Bragantia. 48: 131-142.
Mishra, C. and Mohanty, K. (2007). Role of phenolics and enzymes in imparting resistance to rice plants against root-knot nematode, Meloidogyne graminicola, Indian journal of Nematology. 37: 131-134.
Mohamadian-Sarcheshmeh, M. and Ahmadi, A. (2014). The 1st international conference on new ideas in agriculture, The 1st international conference on new ideas in agriculture. p. 658.
Mohammadi, M. and Kazemi, H. (2002). Changes in peroxidase and polyphenol oxidase activities in susceptible and resistant wheat heads inoculated with Fusarium graminearum and induced resistance, Plant Sciencese. 162: 401-408.
Molinari, S. (1995). Role of oxidative and peroxidative processes in the plant-nematode interaction. Nematologia Mediterranea. 23: 69-73.
Moosavi, S.S., Karegar, A. and Deljoo, A. (2006). Responses of some common cucumber cultivars in Iran to root-knot nematode, Meloidogyne incognita, under greenhouse conditions. Iranian Journal of Plant Pathology. 42: 37-50.
Morkunas, I. and Gmerek, J. (2007). The possible involvement of peroxidase in defense of yellow lupine embryo axes against Fusarium oxysporum, Journal of Plant Physiology. 164: 185–194.
Niebel, A., Almeida, J. D., Tire, C., Engler, C., Van Montagu, G. and Gheysen, G. (1993). Induction Patterns of an extensin gene in tobacco upon nematode infection., Plant Cell. 5: 1697–1710.
Noel, G.R. and McClure, M.A. (1987). Peroxidase and 6-Phosphogluconate Dehydrogenase in resistant and susceptible cotton infected by Meloidogyne incognita. Journal of Nematology. 10: 34–38.
Oka, Y., Cohen, Y. and Spiegel, Y. (1999). Local and systemic induced resistance to the root-knot nematode in tomato by DL- β -amino- n -butyric acid. Phytopathology. 89: 1138–1143.
Ones, J.T., Haegeman, A., Danchin, E.G., Gaur, H.S., Helder, J. and Jones, M.G. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology. 14(9): 946–961.
Patel, B.A., Patel, D.J., Patel, N.B. and Patel, R.G. (2001). Determination of damaging threshold level of root-knot nematode Meloidogyne javanica pathotype 1 on chickpea, Int. Chickpea Pigeonpea Newsletter. 8: 9–11.
Pegard, A., Brizzard, G., Fazari, A., Soucaze, O., Abad, P. and Djian-Caporalino, C. (2005). Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology. 95: 158–165.
Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andrés, M. F., Emiliozzi, M. and Resnick, N. (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(4): 1276-1290
Qin, X. and Xiaoyan, Z. (2008). The relationship between resistance to Meloidogyne incognita and phenyl propanes in roots of egg plant rootstock, Acta Phytophylacica Sinica. 35 : 43-46.
Reuveni, M. (1998). Relationships between leaf age, peroxidase and beta-1,3-glucanase activity, and resistance to downy mildew in grapevines. Journal of Phytopathology. 146: 525–530.
Saeedizadeh, A., Kheiri, A., Zad, J. and Etebarian, H.R. (2009). A Study of the changes in total Phenol content in olive cultivars during the interaction between Verticillium wilt, Verticillium, and nematode. Iranian Journal Plant Protection Science. 42: 125–135.
Sahebani, N., Zad, J., Sharifitehrani, A. and Kheiri, A. (2008). A study of changes in peroxidase activity in the interaction between root-knot nematode (Meloidogyne javanica) and tomato Fusarium wilt agent (Fusarium oxysporium f. sp. lycopersisci), Tehran University. College of Agriculture. 39: 127–138.
Sari, E., Etebarian, H. R. and Aminian, H. (2008). Effects of Pseudomonas fluorescens CHA0 on the Resistance of wheat seedling roots to the take-all fungus Gaeumannomyces graminis var. tritici. Plant Protection Science. 11: 298–306.
Sari., E., Etebarian, H. R. and Aminian, H. (2007). The effects of Bacillus pumilus, isolated from wheat rhizosphere, on resistance in wheat seedling roots against the take-all fungus, Gaeumannomyces graminis var. tritici. Jornal of Phytopathology. 155: 720–727.
Sato, K., Kadota, Y. and Shirasu, K. (2019). Plant immune responses to plant parasitic nematodes. Frontiers in plant science, 10: 1165.
Shahriari D., Molavi, E., Aminian, H. and Etebarian, H.R. (2011). Histopathological response of resistant and susceptible cultivars of cucumber to Fusarium oxysporum f. sp. radicis-cucumerinum, the causal agent of fusarium stem and root rot. Seed Plant Improvement Journal. 27: 375–391.
Shigeoka, S., Ishikawa, T., Tamoi, M., Miyagawa, Y., Takeda, T., Yabuta, Y. and Yoshimura, K. (2002). Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany, 53(372): 1305-1319
Shokoohi, E., Kheiri, A., Etebarian, H.R. and Roostaei, A. (2003). Interactions between root-knot nematode Meloidogyne javanica and Fusarium wilt disease, Fusarium oxysporum f. sp. Melonis in different varieties of melon. Communication in Agriculture Applied Biology Sciencese. 69: 387–391.
Siddique, S., Matera, C., Radakovic, Z.S., Hasan, M.S., Gutbrod, P., Rozanska, E. and Grundler, F.M. (2014). Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Science Signaling, 7(320): ra33-ra33.
Singh, R.K. (2003). Studies on and predacity and biocontrol potential of Arthrobotrys oligospora. Ph.D Thesis. Banaras Hindu University. Varanasi, India. 353pp.
Sundararaju, P. and Suba, K. (2006). Biochemical and molecular changes in banana plants induced by Pratylenchus coffeae and Meloidogyne incognita, Indian Journal of Nematology. 36: 256-259.
Tarek Hewezi, J.J. and Baum, T.J. (2011). Arabidopsis peroxidase AtPRX53 influences cell elongation and susceptibility to Heterodera schachtii. Plant Signaling and Behavior, 6: 1778-1786.
Taylor, D. and Netscher, C. (1974). An improved technique for preparing perineal patterns of Meloidogyne spp. Nematologica. 20: 268-269.
Teixeira, M.A., Wei, L. and Kaloshian, I. (2016). Root-knot nematodes induce pattern-triggered immunity in Arabidopsis thaliana roots. New Phytopathology. 211(1): 276–287.
Torres, M.A., Jones, J.D. and Dangl, J.L. (2006). Reactive oxygen species signaling in response to pathogens. Plant Physiology. 141(2): 373–378.
Vakalounakis D.J., Doulis, A.G. and Klironomou, E. (2005). Characterization of Fusarium oxysporum f. sp. radicis-cucumerinum attacking melon under natural conditions in Greece. Plant Pathology. 54: 339–346
VanderMolen, G.E., Beckman,C. H. and Rodehorst, E. (1977). Vascular gelation: a general response phenomenon following infection. Physiological Plant Pathology. 11(1): 95-100
Whitehead, A.G. and Hemming, J.R. (1965). A comparison of some quantitative methods of extracting small vermiform nematodes from the soil, Annual Applied Biology. 55: 25–38.
Wong, E. (1973). Plant phenolics, Chemistry and Biochemestry of Herb. 1: 265–322.
Yang, S., Dai, Y., Chen, Y., Yang, J., Yang, D. and Liu, Q. (2019). A novel G16B09-like effector from Heterodera avenae suppresses plant defenses and promotes parasitism. Frontier Plant Science. 10: 66.
Zacheo, G., Blevezacheo, T., Pacoda, C., Orlando, D. and Durbin, R. D. (1995). The Association between Heat-Induced Susceptibility of Tomato to Meloidogyne-Incognita and Peroxidase-Activity. Physiology and Molecular Plant Pathology. 46: 491–507.
Zhou, J., Xu, X.C., Cao, J.J., Yin, L.L., Xia, X.J. and Shi, K. (2018). Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production. Plant Physiology. 176(3): 2456–2471.