Effect of disease complex of Meloidogyne incognita and Fusarium solani on fungus root rot incidence, nematode reproduction, and enzyme activities involved in defense mechanisms of grafted cucurbit hybrids

Authors

  • Hosny H. KESBA King Faisal University, College of Agricultural and Food Sciences, Department of Arid Land Agriculture, P.O. Box 420, Al-Ahsa 31982; Cairo University, Faculty of Agriculture, Department of Zoology and Agricultural Nematology, Giza-12613 (SA) https://orcid.org/0000-0001-9396-2214
  • Sherif M. EL-GANAİNY King Faisal University, College of Agricultural and Food Sciences, Department of Arid Land Agriculture, P.O. Box 420, Al-Ahsa 31982 (SA)
  • Ali H.H. ALI Cairo University, Faculty of Agriculture, Department of Zoology and Agricultural Nematology, Giza-12613 (EG)
  • Nourhan M.M. HASSNIN Cairo University, Faculty of Agriculture, Department of Zoology and Agricultural Nematology, Giza-12613 (EG)

DOI:

https://doi.org/10.15835/nbha52413933

Keywords:

cucurbit hybrids, disease complex, enzyme activities, Fusarium solani, Meloidogyne incognita, nematode development

Abstract

This study investigated the interplay between the root-knot nematode, Meloidogyne incognita (Mi), and the fungal pathogen, Fusarium solani (Fs) in grafted cucurbit hybrids (watermelon and sweet melon). Results revealed that Fs root rot incidence was exacerbated when combined with Mi. Nonetheless, the existence of Fs caused a noteworthy decline in Mi reproduction, affecting hosts that were both resistant and susceptible. Additionally, plant growth suffered more from combined infection than from single pathogens, with the susceptible sweet melon showing greater growth reduction. The study further explored the impact of the disease complex on antioxidant defence mechanisms. Leaf tissues from both grafted hybrids displayed elevated levels of lipid peroxidation (MDA) and antioxidant enzyme activities (SOD and APX) upon infection with Fs alone, Mi alone, or both. Interestingly, the susceptible sweet melon exhibited a stronger increase in these defence responses compared to the resistant watermelon. Notably, combined Fs and Mi infection led to the highest levels of MDA, SOD, and APX activity. These findings highlight the complex interplay between Fs and Mi in cucurbit hybrids. While Fs virulence increased with coinfection, Mi reproduction was suppressed. Furthermore, the study suggests that susceptible plants may have a more pronounced activation of antioxidant defence mechanisms when confronted with the combined stress of these pathogens.

References

Abawi GS, Barker KR (1984). Effects of cultivar, soil temperature, and population levels of Meloidogyne incognita on root necrosis and Fusarium wilt of tomatoes. Phytopathology 74(4):433. https://doi.org/10.1094/phyto-74-433

Abawi GS, Chen J (1998). Concomitant pathogen and pest interactions. In: Barker KR, Pederson GA, Windham, GL (Eds). Plant and nematode interactions. American Society Agronomy Monographs pp 135-158. https://doi.org/https://doi.org/10.2134/agronmonogr36.c7

Agrios GN (2004). Plant Pathology (5th ed.). Academic Press, San Diego, CA.

Alcalá-García FJ, López-Galindo A, Martín-Martín M (2002). The Paleocene of the high chain (Betic cordillera) and implications for the geodynamic evolution of the south Iberian paleomargin. EstudiosGeologicos 58(3-4):75-85. https://doi.org/10.3989/egeol.02583-4

Arrigoni O, Zacheo G, Arrigoni-Liso R, Bleve-Zacheo T, Lamberti F (1979). Relationship between ascorbic acid and resistance in tomato plants to Meloidogyne incognita. Phytopathology 69(6):579. https://doi.org/10.1094/phyto-69-579

Asada K (1992). Ascorbate peroxidase – a hydrogen peroxide‐scavenging enzyme in plants. Physiologia Plantarum 85(2):235-241. https://doi.org/10.1111/j.1399-3054.1992.tb04728.x

Asada K, Takahashi M (1987). Production and scavenging of active oxygen in chloroplasts. In: Kyle DJ, Osmond CB, Arntzen CJ (Eds). Photoinhibition. Elsevier pp 227-287

Bakker E, Dees R, Bakker J, Goverse A (2006). Mechanisms involved in plant resistance to nematodes. In: Tuzum S, Bent E (Eds). Multigenic and induced systemic resistance in plants. Springer US pp 314-334. https://doi.org/10.1007/0-387-23266-4_14

Barnett HL, Hunter BB (1986). Illustrated genera of imperfect fungi (Fourth). Macmillan Publishers Co. https://doi.org/10.1002/fedr.4911000913

Beauchamp C, Fridovich I (1971). Superoxide dismutase: improved assays and assay applicable to acrylamide gels. Analytical Biochemistry 44:276-287. https://doi.org/10.1016/0003-2697(71)90370-8

Beckman CH (1987). The nature of root rot diseases of plants. American Phytopathological Society.

Bergeson GB (1975). The effect of Meloidogyne incognita on the resistance of musk melon varieties to Fusarium root rot disease. Plant Disease Reporter 59:410-413.

Bertrand B, Nuñez C, Sarah JL (2000). Disease complex in coffee involving Meloidogyne arabicida and Fusarium oxysporum. Plant Pathology 49(3):383-388. https://doi.org/10.1046/j.1365-3059.2000.00456.x

Bletsos FA (2005). Use of grafting and calcium cyanamide as alternatives to methyl bromide soil fumigation and their effects on growth, yield, quality and Fusarium wilt control in melon. Journal of Phytopathology 153(3):155-161. https://doi.org/https://doi.org/10.1111/j.1439-0434.2005.00945.x

Bradford MM (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3

Caperton M, Martin RD, Starr JL (1986). Effects of Fusarium inoculum density and root-knot nematodes on wilt resistance in summer squash. Plant Disease 70(3):207. https://doi.org/10.1094/pd-70-207

Chavan V, Bhargava S, Kamble A (2013). Temporal modulation of oxidant and antioxidative responses in Brassica carinata during β-aminobutyric acid-induced resistance against Alternaria brassicae. Physiological and Molecular Plant Pathology 83:35-39. https://doi.org/10.1016/j.pmpp.2013.03.002

Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015). Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Scientific Reports 5:12516. https://doi.org/10.1038/srep12516

Chitwood BG (1949). “Root-knot nematodes” - Part 1. A revision of the genus Meloidogyne goeldi, 1887. Proceedings of the Helminthological Society of Washington 16:90-104.

Cohen R, Horev C, Burger Y, Shriber S, Hershenhorn J, Katan J, Edelstein M (2002). Horticultural and pathological aspects of Fusarium wilt management using grafted melons. HortScience 37(7):1069-1073. https://doi.org/10.21273/hortsci.37.7.1069

Crews LJ, McCully ME, Canny MJ (2003). Mucilage production by wounded xylem tissue of maize roots — time course and stimulus. Functional Plant Biology 30(7):755. https://doi.org/10.1071/fp03052

Davis AR, Perkins-Veazie P, Sakata Y, López-Galarza S, Maroto JV, Lee SG, Huh, … Lee JM (2008). Cucurbit grafting. Critical Reviews in Plant Sciences 27(1):50-74. https://doi.org/10.1080/07352680802053940

Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, Rosso MN, Abad P (2000). Nematode parasitism genes. Annual Review of Phytopathology 38(1):365-396. https://doi.org/10.1146/annurev.phyto.38.1.365

Debona D, Rodrigues FÁ, Rios JA, Nascimento KJT (2012). Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 102(12):1121-1129. https://doi.org/10.1094/phyto-06-12-0125-r

Duncan DB (1955). Multiple Range and Multiple F Tests. Biometrics 11(1):1. https://doi.org/10.2307/3001478

Egel DS, Martyn RD (2007). Fusarium root rot disease of watermelon and other cucurbits. The Plant Health Instructor. http://dx.doi.org/10.1094/phi-i-2007-0122-01

El-Zahaby HM (1995). Effects of powdery mildew infection of barley on the ascorbate-glutathione cycle and other antioxidants in different host-pathogen interactions. Phytopathology 85(10):1225. https://doi.org/10.1094/phyto-85-1225

Farahani AS, Taghavi M (2016). Changes of antioxidant enzymes of mung bean [Vigna radiata (L.) R. Wilczek] in response to host and non-host bacterial pathogens. Journal of Plant Protection Research 56(1):95-99. https://doi.org/10.1515/jppr-2016-0016

France RA, Abawi GS (1994). Interaction between Meloidogyne incognita and Fusarium oxysporum f. sp. phaseoli on selected bean genotypes. Journal of Nematology 26:467-474.

Gherbawy Y, El-Tayeb M, Maghraby T, Shebany Y, El-Deeb B (2012). Response of antioxidant enzymes and some metabolic activities in wheat to Fusarium spp. Infections. Acta AgronomicaHungarica 60(4):319-333. https://doi.org/10.1556/aagr.60.2012.4.3

Gill SS, Tuteja N (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48(12):909-930. https://doi.org/10.1016/j.plaphy.2010.08.016

Griffin GD, Thyr BD (1986). The importance of nematode resistance on the 87 interaction of Meloidogyne hapla and Fusarium oxysporum on alfalfa. Phytopathology 76:843-844. https://doi.org/10.1094/phyto-78-421

Guida G, Zacheo G, Bleve-Zacheo T (1992). Activation of detoxifying enzymes in tomato roots following paraquat treatment and nematode infection. Nematologia Mediterranea 20:203-209.

Hall C, Heath R, Guest DI (2011). Rapid and intense accumulation of terpenoid phytoalexins in infected xylem tissues of cotton (Gossypium hirsutum) resistant to Fusarium oxysporum f.sp. vasinfectum. Physiological and Molecular Plant Pathology 76(3-4):182-188. https://doi.org/10.1016/j.pmpp.2011.09.002

Heath RL, Packer L (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125:189-198. https://doi.org/10.1016/0003-9861(68)90654-1

Hernández JA, Ferrer MA, Jimenez A, Barcelo AR, Sevilla F (2001). Antioxidant systems and o2.-/h2o2 production in the apoplast of pea leaves. its relation with salt-induced necrotic lesions in minor veins. Plant Physiology 127(3):817-831. https://doi.org/10.1104/pp.127.3.817

Hodges DM, DeLong JM, Forney CF, Prange RK (1999). Improving the thiobarbuturic acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604-611.

Huang G, Dong R, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2004). Use of solid‐phase subtractive hybridization for the identification of parasitism gene candidates from the root‐knot nematode Meloidogyne incognita. Molecular Plant Pathology 5(3):217-222. https://doi.org/10.1111/j.1364-3703.2004.00220.x

Inch S, Ploetz R, Held B, Blanchette R (2012). Histological and anatomical responses in avocado, Persea americana, induced by the vascular wilt pathogen, Raffaelea lauricola. Botany 90(7):627-635. https://doi.org/10.1139/b2012-015

Jonathan E, Rajendran G (1998). Interaction of Meloidogyne incognita and Fusarium oxysporum f. sp. cubense on banana. Nematologia Mediterranea 26:9-11.

Jones MGK (1981). Host cell responses to endoparasitic attack: Structure and function of giant cells and syncytia. Annals of Applied Biology 7:353-372. https://doi.org/10.1111/aab.12103

Kaplan DT, Keen NT (1980). Mechanisms conferring plant incompatibility to nematodes. Revue de Nematologica 3:123-134.

Kesba HH, El-Beltagi HS (2012). Biochemical changes in grape rootstocks resulted from humic acid treatments in relation to nematode infection. Asian Pacific Journal of Tropical Biomedicine 2(4):287-293. https://doi.org/10.1016/S2221-1691(12)60024-0

Khan M, Muller J (1982). Interaction between Rhizoctonia solani and Meloidogyne hapla on radish in gnotobiotic culture. Libyan Journal of Agricultural Sciences 11:133-140.

Kofoid CA, White AW (1919). A new nematode infection of man. Journal of the American Medical Association 72(8):567. https://doi.org/10.1001/jama.1919.02610080033010

Lee JM (1994). Cultivation of grafted vegetables I. Current status, grafting methods, and benefits. HortScience 29(4):235-239. https://doi.org/10.21273/hortsci.29.4.235

Lee JM, Oda M (2003). Grafting of herbaceous vegetable and ornamental crops. In: Janick J (Ed). Horticultural reviews. Wiley pp 61-124. https://doi.org/10.1002/9780470650851.ch2

Leslie JF, Summerell BA (2006). The Fusarium laboratory manual. Blackwell Publishing.

Liu B, Ren J, Zhang Y, An J, Chen M, Chen H, Xu C, Ren H (2015). A new grafted rootstock against root-knot nematode for cucumber, melon, and watermelon. Agronomy for Sustainable Development 35(1):251-259. https://doi.org/10.1007/s13593-014-0234-5

Mandal PK, Biswas AK, Choi K, Pal UK (2011). Methods for rapid detection of foodborne pathogens: An Overview. American Journal of Food Technology 6(2):87-102. https://doi.org/10.3923/ajft.2011.87.102

Maninder K, Sharma S, Sukhjeet K (2013). Screening of tomato germplasm against root-knot nematode (Meloidogyne incognita) and biochemical characterization of selected tomato genotypes. Plant Disease Research 28(2):191-196.

McLean KS, Lawrence GW (1993). Interrelationship of Heterodera glycines and Fusarium solani in sudden-death syndrome of soybean. Journal of Nematology 25:434-439.

Meléndez PL, Powell NT (1970). Histological studies of the Pythium-root knot complex in tobacco. Phytopathology 60:1303.

Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002). H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. The Plant Journal 29(3):257-268. https://doi.org/10.1046/j.0960-7412.2001.01215.x

Mitkowski NA, Abawi GS (2003). Root-knot nematodes. The Plant Health Instructor. https://doi.org/10.1094/phi-i-2003-0917-01

Montes MJ, López-Braña I, Delibes A (2004). Root enzyme activities associated with resistance to Heterodera avenae conferred by gene Cre7 in a wheat/Aegilops triuncialis introgression line. Journal of Plant Physiology 161(4):493-495. https://doi.org/10.1078/0176-1617-01165

Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004). Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat‐induced photooxidative stress and to nitric oxide‐induced cell death. The Plant Journal 38(6):940-953. https://doi.org/10.1111/j.1365-313x.2004.02092.x

Nakano Y, Asada K (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology 22:867-880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

Pavlou GC, Vakalounakis DJ, Ligoxigakis EK (2002). Control of root and stem rot of cucumber, caused by Fusarium oxysporum f. sp. radicis-cucumerinum, by grafting onto resistant rootstocks. Plant Disease 86(4):379-382. https://doi.org/10.1094/pdis.2002.86.4.379

Peltzer D, Dreyer E, Polle A (2002). Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiology and Biochemistry 40(2):141-150. https://doi.org/10.1016/s0981-9428(01)01352-3

Plume ML (2003). SPSS (Statistical Package for the Social Sciences). Encyclopedia of Information Systems. Elsevier pp 187-196. https://doi.org/https://doi.org/10.1016/B0-12-227240-4/00166-0

Roberts PA, Dalmasso A, Cap GB, Castagnone-Sereno P (1990). Resistance in Lycopersicon peruvianum to isolates of Mi gene-compatible Meloidogyne populations. Journal of Nematology 22(4):585-589.

Sasser JN, Carter CC, Hartman KM (1984). Standardization of host suitability studies and reporting of resistance to root-knot nematodes. Department of Plant Pathology, North Carolina State University, pp 1-7.

Seo Y, Kim YH (2017). Potential reasons for prevalence of Fusarium wilt in oriental melon in Korea. The Plant Pathology Journal 33(3):249-263. https://doi.org/10.5423/PPJ.OA.02.2017.0026

Sgherri C, Ranieri A, Quartacci MF (2013). Antioxidative responses in Vitis vinifera infected by grapevine fanleaf virus. Journal of Plant Physiology 170(2):121-128. https://doi.org/10.1016/j.jplph.2012.09.016

Sharma GC, Rastogi KB, Shukla YR, Khan ML (1995). Reaction of cucumber varieties to root-knot nematode Meloidogyne incognita. Annals of Agricultural Research 16:33-35.

Shepherd RL, Huck MG (1989). Progression of root-knot nematode symptoms and infection on resistant and susceptible cottons. Journal of Nematology 21(2):235-241.

Siddiqui ZA, Mir RA, Mahmood I (1999). Effects of Meloidogyne incognita, Fusarium oxysporum f. sp. pisi, Rhizobium sp., and different soil types on growth, chlorophyll, and carotenoid pigments of pea. Israel Journal of Plant Sciences 47(4):251-256. https://doi.org/10.1080/07929978.1999.10676781

Sijmons PC, Atkinson HJ, Wyss U (1994). Parasitic strategies of root nematodes and associated host cell responses. Annual Review of Phytopathology 32(1):235-259. https://doi.org/10.1146/annurev.py.32.090194.001315

Smith CL, Freeman JH, Kokalis-Burelle N, Wechter WP (2019). Screening cucurbit rootstocks for resistance to Meloidogyne spp. and Rotylenchulus reniformis. HortScience 54(1):125-128. https://doi.org/10.21273/hortsci13094-18

Song M, Yun HY, Kim YH (2014). Antagonistic Bacillus species as a biological control of ginseng root rot caused by Fusarium cf. incarnatum. Journal of Ginseng Research 38(2):136-145. https://doi.org/10.1016/j.jgr.2013.11.016

Suleman P, Sardanelli S, Krusberg LR, Straney DC (1997). Variability among Fusarium oxysporum f.sp. lycopersici isolates in their ability to interact with Meloidogyne incognita race1. Kuwait Journal of Science and Engineering 24:299-307.

Traka-Mavrona E, Koutsika-Sotiriou M, Pritsa T (2000). Response of squash (Cucurbita spp.) as rootstock for melon (Cucumis melo L.). Scientia Horticulturae 83(3-4):353-362. https://doi.org/10.1016/s0304-4238(99)00088-6

Vanacker H, Carver TL, Foyer CH (1998). Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiology 117(3):1103-1114. https://doi.org/10.1104/pp.117.3.1103

White TJ, Bruns T, Lee SJWT, Taylor JL (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (Eds). PCR Protocols: A guide to methods and applications. Academic Press, New York pp 315-322.

Yan HX, Xu BL, Liang QL, Xue YY, Chen RX, Liang ZF (2009). Effects of chlorophyll content and stoma density on pumpkin resistance to powdery mildew. Plant Protection 35:79-81.

Zacheo G, Bleve-Zacheo T (1988). Involvement of superoxide dismutases and superoxide radicals in the susceptibility and resistance of tomato plants to Meloidogyne incognita attack. Physiological and Molecular Plant Pathology 32(2):313-322. https://doi.org/10.1016/s0885-5765(88)80026-2

Zacheo G, Orlando C, Bleve-Zacheo T (1993). Characterization of anionic peroxidases in tomato isolines infected by Meloidogyne incognita. Journal of Nematology 25(2):249-256.

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2024-11-11

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KESBA, H. H., EL-GANAİNY, S. M., ALI, A. H., & HASSNIN, N. M. (2024). Effect of disease complex of Meloidogyne incognita and Fusarium solani on fungus root rot incidence, nematode reproduction, and enzyme activities involved in defense mechanisms of grafted cucurbit hybrids. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(4), 13933. https://doi.org/10.15835/nbha52413933

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DOI: 10.15835/nbha52413933