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Pratylenchus vulnus infecting apple rootstock MM106: Defense reaction, plant nutrient alterations and pathogenic potential

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Abstract

The aim of this study was at investigating biochemical changes and plant nutrient alterations in roots and leaves of apple rootstock MM106 following nematode infection. The pathogenic potential of Pratylenchus vulnus at increasing inoculum doses was also investigated. Three tests were carried out using apple plants of different ages (3 months, 1 year, and 3 years) under greenhouse conditions. The enzymatic activity of Catalase (CAT), Peroxidase (POX), Polyphenol-Oxidase (PPO), and Ascorbate peroxidase (APX) were measured in roots of 3-month-old apple plants at 7 days post-inoculation (dpi). Total phenol, total protein content, the lipid peroxidation marker (MDA) and the content of N, P, K, Fe, and Zn were quantified in roots of 3- and 36-month-old plants by atomic spectrometry at 135 dpi and 11 months after inoculation, respectively. The activity of POX, PPO and APX increased after pathogen infection in 3-month-old plants whereas CAT activity decreased. Total protein content and MDA augmented, but total phenols were reduced in 3- and 36-month-old plants inoculated with 1000 or 5000 nematodes. The content of P, K, and Zn in leaves decreased but Fe content increased at the highest dose tested (5000 nematodes/plant). Changes in the enzymatic activities induced in apple roots in response to P. vulnus are part of the defense mechanisms of the host against nematode attack. The nematode reproduced in rootstocks MM106, MM111 and Ba29 and population densities increased on rootstock MM106 as the initial dose did.

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References

  • Abd-Allah, A. S. E. (2006). Effect of spraying some micro and macronutrients in fruit set, yield and fruit quality of Washington navel orange tree. Applied Science - Research, 11, 1059–1063.

    Google Scholar 

  • Acedo, J. (1968). Dissertation. Univ. of Massachusetts Amherst.

    Google Scholar 

  • Ahuja, S., & Ahuja, S. P. (1980). Effects of root-knot nematode Meloidogyne incognita infection on the peroxidase and polyphenoloxidase activities in the roots of selected vegetables crops. Nematologia Mediterranea, 8, 207–210.

    Google Scholar 

  • Almagro, L., Gómez, L. V., Belchi-Navarro, S., Bru, R., Ros-Barceló, A., & Pedreño, M. A. (2009). Class III peroxidases in plant defence reactions. Journal of Experimental Botany, 60(2), 377–390.

    Article  CAS  PubMed  Google Scholar 

  • Arrigoni O. (1979). A biological defense mechanism in plants. Dans: Lamberti, F. & Taylor, C. E. (Eds) Root-knot nematodes (Meloidogyne species). Systematics, biology and control. London: Academic Press, 457–467.

  • Askary, T. H., Banday, S. A., Iqbal, U., Khan, A. A., Mir, M. M. & Waliullah, M. I. S. (2012). Plant parasitic nematode diversity in pome, stone and nut fruits, in Lichtfouse, E. (Eds), Agroecology and strategies for climate change: Sustainable agriculture reviews 8, Springer, Dordrecht.

  • Avallone, S., Guiraud, J. P., Brillouet, J. M., & Teisson, C. (2003). Enzymatic browning and biochemical alterations in black spots of pineapple. Current Microbiology, 47, 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Baldridge, G. D., O’Neill, N. R., & Samac, D. A. (1998). Alfalfa (Medicago sativa L.) resistance to the root-lesion nematode, Pratylenchus penetrans: Defense-response gene mRNA and isoflavonoid phytoalexin levels in roots. Plant Molecular Biology, 38, 999–1010.

    Article  CAS  PubMed  Google Scholar 

  • Bonner, J. (1950). Plant Biochemistry (p. 537). Academic Press.

    Google Scholar 

  • Borden, S., & Higgins, V. J. (2002). Hydrogen peroxide plays a critical role in the defense response of tomato to Cladosporium fulvum. Physiological and Molecular Plant Pathology, 61, 227–236.

    Article  CAS  Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for quantitation or microgram quantities of protein utilizing the principle of protein-dye hinding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Castillo, P. & Vovlas, N. (2007). Pratylenchus (Nematoda: Pratylenchidae): Diagnosis, Biology, Pathogenicity and Management. Vol. 6. Brill, Leiden-Boston. Pp. 529.

  • Chihani-Hammas, N., Hajji- Hedfi, L., Regaieg, H., Larayedh, A., Badiss, A., Qing, Y., & Horrigue-Raouani, N. (2018). First report of Pratylenchus vulnus associated with apple in Tunisia. Journal of Nematology., 50(4), 579–586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Culver, D., Ramm, D. W., & Mckenry, M. V. (1989). Procedures for field and greenhouse screening of Prunus genotypes for resistance and tolerance to root-lesion nematode. Journal of the American Society for Horticultural Science, 114, 30–35.

    Article  Google Scholar 

  • De Grisse, A. T. (1969). Redescription ou modification de quelques techniques utilisées dans l’étude des nématodes phytoparasitaires. Mededelingen Rijksfaculteti der Landbouveten Gent, 34, 351–359.

  • Dhindsa, R. H., Dhindsa, R. P., & Thorpe, T. A. (1981). Leaf senescence correlated with increased level of membrane permeability, lipid peroxidation and decreased level of SOD and CAT. Journal of Experimental Botany, 32, 93–101.

    Article  CAS  Google Scholar 

  • El-Beltagi, H. S., Farahat, A. A., Alsayed, A. A., & Mahfoud, N. M. (2012). Response of antioxidant substances and enzymes activities as a defense mechanism against root knot nematode infection. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 40(1), 132–142.

  • Feldman, A. W., & Hanks, R. W. (1964). Quantitative changes in the free and protein amino acids in roots of healthy, Radopholus similis infected, and recovered grapefruit seedling. Phytopathology, 54, 1210–1215.

    CAS  Google Scholar 

  • Fernández, C., Pinochet, J., & Dolcet, R. (1992). Host parasite relationship of Pratylenchus vulnus on apple and pear rootstocks. Nematropica, 22, 227–236.

    Google Scholar 

  • Filipjev, I. N. (1936). On the classification of the Tylenchinae. Proceedings of the Helminthological Society of Washington, 3, 80–82.

  • Fosu-Nyarko, J., & Jones, M. G. K. (2016). Advances in understanding the molecular mechanisms of root lesion nematode host interactions. Annual Review of Phytopathology, 54, 253–278.

    Article  CAS  PubMed  Google Scholar 

  • Foyer, C. H., & Noctor, G. (2005). Oxidant and antioxidant signaling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell and Environment, 28, 1056–1071.

    Article  CAS  Google Scholar 

  • Giebel, J. (1970). Phenolic content in roots of some Solanaceae and its influence on IAA-oxidase activity as an indicator of resistance to Heterodera rostochiensis. Nematologica, 16, 22–32.

    Article  CAS  Google Scholar 

  • Giebel, J. (1982). Mechanism of resistance to plant nematodes. Annual Review of Phytopathology, 20, 257–279.

    Article  CAS  Google Scholar 

  • Glorieux, C., & Calderon, P. B. (2017). Catalase, a remarkable enzyme: Targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biological Chemistry, 398, 1095–1108.

    Article  CAS  PubMed  Google Scholar 

  • Hajji, L., Elouaer, M. A., Regaieg, H., M’Hamdi-Boughalleb, N., & Horrigue-Raouani, N. (2017). Biochemical and plant nutrient alterations induced by Meloidogyne javanica and Fusarium oxysporum f. sp. radicis lycopersici co-infection on tomato cultivars with differing level of resistance to M. javanica. European Journal of Plant Pathology, 148, 463–472.

    Article  Google Scholar 

  • Haraguchi, H., Saito, T., Okamura, N., & Yagi, A. (1995). Inhibition of lipid peroxidation and superoxide generation by diterpenoids from Rosmarinus officinalis. Planta Medica, 61(4), 333–336.

    Article  CAS  PubMed  Google Scholar 

  • Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives in Biochemistry and Biophysics, 125, 189–198.

    Article  CAS  Google Scholar 

  • Huber, D. M., & Graham, R. D. (1999). The role of nutrition in crop resistance and tolerance to diseases. In Z. Rengel (Ed.), Mineral nutrition of crops: Fundamental mechanisms and implications (pp. 169–206). Food Products Press.

    Google Scholar 

  • Jaffee, B. A., & Mai, W. F. (1979). Growth reduction of apple seedlings by Pratylenchus penetrans as influenced by seedling and age at inoculation. Journal of Nematology, 11(2), 163–165.

    Google Scholar 

  • Jaffee, B. A., Abawi, G., & Mai, W. (1982). Role of soil microflora and Pratylenchus penetrans in an apple replant disease. Phytopathology, 72, 247–251.

    Article  Google Scholar 

  • Janssen, T., Karssen, G., Orlando, V., Subbotin, S. A. & Bert, W. (2017). Molecular characterization and species delimiting of plant-parasitic nematodes of the genus Pratylenchus from the Penetrans group (Nematoda: Pratylenchidae). Molecular Phylogenetics and Evolution, 117, 30–48. Available at: https://doi.org/10.1016/j.ympev.2017.07.027

  • Jones, J. T., Haegeman, A., Danchin, E. G. J., Gaur, H. S., Helder, J., Jones, M. G. K., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J. E., Wesemael, W. M. I., & Perry, R. N. (2013). Top 10 plant- parasitic nematodes in molecular plant pathology. Molecular Plant Pathology, 14(9), 946–961.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirkpatrick, J. D., Mai, W. F., Parker, T. C. G., & Fisher, E. G. (1964). Effect of phosphorus and potassium nutrition of sour cherry on the soil population levels of five plant-parasitic nematodes. Phytopathology, 54, 706–712.

    CAS  Google Scholar 

  • Kubalt, K. (2016). The role of phenolic compounds in plant resistance. Biotechnology and Food Sciences, 80(2), 97–108.

  • Lamberti, F., & Baines, R. C. (1969). Pathogenicity of four species of Meloidogyne on three varieties of olive trees. Journal of Nematology, 1, 111–115.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leeman, M., den Ouden, F. M., van Pelt, J. A., Dirkx, F. P. M., Steijl, H., Bakker, P. A. H. M., & Schippers, B. (1996). Iron availability affects induction of systemic resistance to fusarium wilt of radish by Pseudomonas fluorescens. Phytopathology, 86, 149–155.

    Article  CAS  Google Scholar 

  • Linsell, K. J., Riley, I. T., Davies, K. A., & Oldach, K. H. (2014). Characterization of resistance to Pratylenchus thornei (nematoda) in wheat (Triticum aestivum): Attraction, penetration, motility, and reproduction. Phytopathology, 104, 174–187.

    Article  PubMed  Google Scholar 

  • Mai, W. F., & Parker, K. G. (1967). Root diseases of fruit trees in New York State. I: Populations of Pratylenchus penetrans and growth of cherry in response to soil treatment with nematicides. Plant Disease Reporter, 51, 398–401.

    Google Scholar 

  • Mai, W. F., & Parker, K. G. (1972). Root diseases of fruit trees in New York State. IV." Influence of preplant treatment with a nematicide, charcoal from burned brush, and complete mineral nutrition on growth and yield of sour cherry trees and numbers of Pratylenchus penetrans. Plant Disease Reporter, 56, 141–145.

    Google Scholar 

  • Malik, C. P., & Singh, M. B. (1980). Plant enzymology and histo enzymology (pp. 30–84). New Delhi: Kalyani publishers.

    Google Scholar 

  • Matern, U., & Kneusel, R. E. (1988). Phenolic compounds in plant disease resistance. Phytoparasitica, 16, 153–170.

    Article  CAS  Google Scholar 

  • McDonald, S., Prenzler, P. D., Autolovich, M., & Robards, K. (2001). Phenolic content and antioxidant activity of olive extracts. Food Chemistry, 73, 73–84.

    Article  CAS  Google Scholar 

  • Mellersh, D. G., Foulds, I. V., Higgins, V. J., & Heath, M. (2002). H2O2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant Journal, 29, 257–268.

    Article  CAS  Google Scholar 

  • Miller, G., Suzuki, N., Ciftci-Yilmaz, S., & Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment, 33, 453–467.

    Article  CAS  Google Scholar 

  • 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(2), 235–239.

    Google Scholar 

  • Moody, E. H., Lownsbery, B. F., & Ahmed, J. M. (1973). Culture of the root lesion nematode Pratylenchus vulnus on carrot disks. Journal of Nematology, 19, 125–134.

    Google Scholar 

  • Nakano, Y., & Asada, K. (1981). Hydrogen Peroxide Is Scavenged by Ascorbate-Specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology, 22, 867–880.

    CAS  Google Scholar 

  • Nico, A., Jiménez-Dı́az, R. M., & Castillo, P. (2003). Host Suitability of the Olive Cultivars Arbequina and Picual for Plant-Parasitic Nematodes. Journal of Nematology, 35(1), 29–34.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pinochet, J., Raski, D. J., & Goheen, A. C. (1976). Effects of Pratylenchus vulnus and Xiphinema index singly and combined on vine growth of Vitis vinifera. Journal of Nematology, 8, 330–335.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pinochet, J., Verdejo, S., Soler, A., & Canals, J. (1992). Host range of a population of Pratylenchus vulnus in commercial fruit, nut, citrus, and grape rootstocks in Spain. Journal of Nematology, 24(4S), 693–698.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pinochet, J., Camprubí, A., & Calvet, C. (1993). Effects of the root lesion nematode Pratylenchus vulnus and the mycorrhizal fungus Glomus mosseae on the growth of EMLA-26 apple rootstocks. Mycorrhiza, 4, 79–83.

    Article  Google Scholar 

  • Pinochet, J., Calvet, C., Camprubi, A., & Fernández, C. (1995). Interaction between the root-lesion nematode Pratylenchus vulnus and the mycorrhizal association of Glomus intraradices and Santa Lucia 64 cherry rootstock. Plant and Soil, 170, 323–329.

    Article  CAS  Google Scholar 

  • Pinochet, J., Anglés, M., Dalmau, E., Fernandez, C., & Felipe, A. (1996). Prunus rootstock evaluation to root-knot and lesion nematodes in Spain. Journal of Nematology, 28, 616–623.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pinta, M. (1973). Méthodes de références pour détermination des éléments dans végétaux : Détermination des éléments Ca, Mg, Fe, Mn, Zn et Cu par absorption atomique. Oléagineuse, 28, 87–92.

    CAS  Google Scholar 

  • Pitcher, R. S., Patrick, Z. A., & Mountain, W. B. (1960). Studies on the host-parasite relations of Pratylenchus penetrans (Cobb) to apple seedlings. I. Pathogenicity under Sterile Conditions. Nematologica, 5, 309–314.

    Article  Google Scholar 

  • Pourcel, L., Routaboul, J. M., Cheynier, V., Lepiniec, L., & Debeaujon, I. (2006). Flavonoid oxidation in plants: From biochemical properties to physiological functions. Plant Science, 12(1), 1360–1385.

    Google Scholar 

  • Prabhu, A. S., Fageria, N. K., Berni, R. F., & Rodrigues, F. A. (2007). Phosphorus and plant disease. In L. E. Datnoff, W. H. Elmer, & D. M. Huber (Eds.), Mineral Nutrition and Plant Disease (pp. 45–55). APS Press.

    Google Scholar 

  • Schmid-Siegert, E. S., Stepushchenko, O., Glauser, G., & Farmer, E. E. (2016). Membranes as structural antioxidants: Recycling of malondialdehyde to its source in oxidation-sensitive chloroplast fatty acids. The Journal of Biological Chemistry, 291(25), 13005–13013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma, P., Jha, A. B., Dubey, R. S & Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany, 1, 1–26. Available at: https://doi.org/10.1155/2012/217037

  • Siddiqui, I. A., Shaukat, S. S., & Hamid, M. (2002). Role of zinc in rhizobacteria mediated suppression of root-infecting fungi and root-knot nematode. Journal of Phytopathology, 150, 569–575.

    Article  CAS  Google Scholar 

  • Sogut, M. A., Devran, Z., Arici, S. E., San, B., & Yildirim, A. N. (2013). Host reactions of root lesion nematodes (Pratylenchus spp.) on the rootstocks of pome and stone fruits. Turkish Journal of Entomology, 37(2), 239–248.

    Google Scholar 

  • Stewart, R. J., Sawyer, B. J. B., & Robinson, S. P. (2002). Blackheart development following chilling in fruit of susceptible and resistant pineapple cultivars. Australian Journal of Experimental Agriculture, 42, 195–199.

    Article  Google Scholar 

  • Sundararaj, P., & Mehta, U. K. (1991). Effect of Pratylenchus zeae Graham, 1951 on the enzymes and amino acid content of sugarcane roots. Indian Journal of Nematology, 21(1), 78–84.

    Google Scholar 

  • Townshend, J. L., & Stobbs, L. (1981). Histopathology and histochemistry of lesions caused by Pratylenchus penetrans in roots of forage legumes. Canadian Journal of Plant Pathology, 3, 123–128.

    Article  CAS  Google Scholar 

  • Vaganan, M. M., Ravi, I., Nandakumar, A., Sarumathi, S., Sundararaju, P., & Mustaffa, M. M. (2014). Phenylpropanoid enzymes, phenolic polymers and metabolites as chemical defenses to infection of Pratylenchus coffeae in roots of resistant and susceptible bananas (Musa spp.). Indian Journal of Experimental Biology, 52, 252–260.

    CAS  PubMed  Google Scholar 

  • Valette, C., Andary, C., Geiger, J. P., Sarah, J. L., & Nicole, M. (1998). Histochemical and cytochemical investigations of phenols in roots of banana infected by the burrowing nematode Radopholus similis. Phytopathology, 88, 1141–1148.

    Article  CAS  PubMed  Google Scholar 

  • Whish, J. P. M., Thompson, J. P., Clewett, T. G., Lawrence, J. L., & Wood, J. (2014). Pratylenchus thornei populations reduce water uptake in intolerant wheat cultivars. Field Crops Research., 161, 1–10.

    Article  Google Scholar 

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Chihani-Hammas, N., Verdejo-Lucas, S. & Horrigue-Raouani, N. Pratylenchus vulnus infecting apple rootstock MM106: Defense reaction, plant nutrient alterations and pathogenic potential. Eur J Plant Pathol 167, 169–181 (2023). https://doi.org/10.1007/s10658-023-02694-z

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