Investigating the Inhibitory Effect of Some Plant Crude Extracts against Root-Knot Nematode (Meloidogyne javanica) in Cucumber Plant

Document Type : Original Research

Authors
1 Department of Horticultural Sciences, Faculty of Agriculture & Natural Resources, Ardakan University, P.O. Box 184, Ardakan 8951895491, Iran,
2 Extension Department, Agricultural Jahad of Yazd Province, Yazd, Islamic Republic of Iran.
Abstract
Some plant extracts contain elicitors for inducing systemic resistances in treated plants like the lavender extract, whose protective effects against pathogen proved to be by activating the SAR systemic defense pathway. In this study, plant crude extracts including Azadirachta indica (neem), Tagetes erecta (marigold), Thymus daenensis (thymus), and Carum carvi (caraway) were used to control Root-Knot Nematode (RNK) Meloidogyne javanica in cucumber. First, the effect of these extracts on egg hatching and juvenile mortality was investigated, then, the effect of plant extracts on characters such as numbers of egg masses, nematode galls, and eggs per plant root was evaluated under greenhouse conditions. In the third part of this study, the effect of plant extracts on Polyphenol Oxidase (PPO), Peroxidase (POX), Catalase (CAT), Phenylalanine Ammonia-Lyase (PAL) and β(1,3) Glucanase (β-1, 3-Glu) enzyme activities was studied. Finally, the expression level of three stress enzymes genes including CAT, PPO, and β-1, 3-Glu β-1, 3-glu was evaluated by Real-time RT-PCR method. Results showed that, on the second day after treatment, 500 and 2,500 ppm concentrations of aqueous neem extract inhibited 64.79 and 73.48% of eggs hatching, respectively. In the greenhouse conditions, the four studied plant extracts (neem, marigold, Thymus, and caraway) at 1,500 ppm concentration significantly suppressed the development and reproduction of M. javanica terms of eggs/plant root, egg-masses, numbers of galls, nematode population in soil and, consequently, enhanced growth of the plants. In addition to the activity of the enzymes, the expression levels of these defense enzymes were also increased by the use of plant extracts.

Keywords

Subjects


Abasi Manesh, A., Fazeli, A., beige, S. 2019. The effect of Marjrom medicinal herb extract on the expression of some genes involve in resistance to Septoria tritici leaf blotch in two wheat Chamran and Yavarous cultivars. Iranian Journal of Plant Biology, 10 (4) : 20-34.
Abubakar, U., Adamu T. and Manga S.B. 2004. Control of Meloidogyne incognita (kofoid and white) chitwood (root-knot nematode) of Lycopersicon esculentus (tomato) using cowdung and urine. Afr. J. Biotechnol., 3 (8) (2004), pp. 379-381.
Afify AMR, El-Beltagi HS (2011a). Effect of the insecticide cyanophos on liver function in adult male rats. Fresen Environ Bull 20(4a):1084-1088.
Aly AA, El-Beltagi HS (2010). Influence of ionizing irradiation on the antioxidant enzymes of Vicia faba L. Grasas y Aceites 61(3):288-294.
Anuja, and Sharma, S. 2007. Effect of Some Plant Extracts on the Hatch of Meloidogyne incognita Eggs. International Journal of Botany 3(3): 251-256.
Anwar, S., Javed, N., Zia, Z., Javed, M. 2007. Root Knot Nematode reproduction and galling severity on thirteen vegetable crops. International Symposium on Prospects of Horticultural Industry in Pakistan. 310P.
Anwar, S., Javed, N., Zia, Z., Javed, M. 2009. Meloidogyne incognita infection of five weed genotypes. Pakistan Journal of Zoology [online], vol. 41, pp. 95-100.
Archidona-Yuste A, Cantalapiedra-Navarrete C, Lie’banas G, Rapoport HF, Castillo P, Palomares-Rius JE (2018) Diversity of root-knot nematodes of the genus MeloidogyneGoeldi, 1892 (Nematoda: Meloidogynidae) associated with olive plants and environmental cues regarding their distribution in southern Spain. PLoS One 13(6):e0198236.
Arioli T, Mattner SW, Winberg PC (2015) Applications of seaweed extracts in Australian agriculture: past, present and future. J Appl Phycol 27(5): 2007–2015.
Ashwell G (1957). Colorimetric analysis of sugars. Methods Enzymol 3: 73-105.
Asif, M., Khan, A., Tariq, Siddiqui M.A. 2014. Sustainable management of root knot nematode Meloidogyne incognita through organic amendment on Solanum lycopersicum L. Asian J. Biol., 1 (2016), pp. 1-8.
Aydinli, G., and Mennan, M. .2014. Effect of some plant extracts on Meloidogyne arenaria Neal, 1889 (Tylenchida: Meloidogynidae) and tomato. Türk. entomol. derg., 38 (3): 323-332
Baidoo, R., Yan, G., Nagachandrabose, S., Skantar, A. 2017. Developing a Real-Time PCR Assay for Direct Identification and Quantification of Pratylenchus penetrans in Soil. Plant Disease 101(8): 110-117.
Banani H., Olivieri,L., Garibaldi, A., Lodovica Gullino, M., Spadaro., D. 2018. Thyme and Savory Essential Oil Efficacy and Induction of Resistance against Botrytis cinerea through Priming of Defense Responses in Apple. Foods, 7(2): 78-89.
Cabrera, J., Diaz-Manzano, F.E., Sanchez, M., Rosso, M.N., Melillo, T., Goh, T., Fukaki, H., Cabello, S., Hofmann, J., Fenoll, C. and Escobar, C. (2014). A role for Lateral Organ Boundaries-domain 16during the interaction Arabidopsis – Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development.New Phytol.203, 632–645.
Castagnone-Sereno, P., 2002. Genetic variability in parthenogenetic root-knot nematodes, Meloidogyne spp., and their ability to overcome plant resistance genes. Nematology, vol. 4, no. 5, pp. 605-608.
Chin LS, Singh SK, Wang Q, Murray SF (2000) Identification of Okadaic-acid-induced genes by mRNA differential display in glioma cells. J Biomed Sci 7:152–159.
Cobb, N. A. 1918. Filter-bed nemas: nematodes of the slow sand filter-beds of American cities (including new genera and species).Contrib. Sci. Nematol. 7:189-212.
El-Beltagi HS, Mohamed AA (2010). Changes in non protein thiols, some antioxidant enzymes activities and ultrastructural alterations in Radish plants (Raphanus Sativus L.) grown under lead toxicity. Not Bot Horti Agrobo 38(3):76-85.
El-Beltagi HS, Salama ZA, El-Hariri DM (2008). Some Biochemical Markers for Evaluation of Flax Cultivars under Salt Stress conditions. J Nat Fibers 5(4):316-330.
Faizi S, Fayyaz S, Bano S, Iqbal EY, Lubna, Siddiqi H, Naz A (2011). Isolation of nematicidal compounds fromTagetes patulaL. yellow flowers: structure-activity relationship studies against cyst nematodeHeterodera zeaeinfective stage larvae. J Agric Food Chem 59(17):9080–9093
Farahat AA, Alsayed AA, El-Beltagi HS, Mahfoud NM (2012). Impact of organic and inorganic fertilizers on nematode reproduction and biochemical alterations on tomato. Not Sci Biol 4(1): 58-66.
Feng, B., Shan, L. 2014. ROS Open Roads to Roundworm Infection. Science Signaling, 7(320):pe10. DOI: 10.1126/scisignal.2005273.
Fudali SL,Wang CL,Williams on VM. Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla.Mol Plant-Microbe Interact. 2013; 26:75–86.
Ganai, M.A., Rehman, B., Parihar, M., Siddiqui M.A. 2014. Phytotherapeutic approach for the management of Meloidogyne incognita affecting Abelmoschus esculentus (L.) Moench. Arch. Phytopathol. Plant Prot., 47 (15) (2014), pp. 1797-1805.
Gholamnejad J. Studies on biological control of blue mold in apple by some yeast isolates and their mechanisms of antagonism, M. Sc. dissertation, University of Tehran. 2009; P 152.(In Farsi).
Gholamnezhad J. 2017. Effect of plant extracts against apple gray mold caused by Botrytis cinerea. Applied Microbiology In Food Industries, 3(1): 53-66.
Gholamnezhad J. Effect of plant extracts on activity of some defense enzymes of apple fruit in interaction with Botrytis cinerea. Journal of Integrative Agriculture, 2019; 17(0): 1-10.
Gholamnezhad J., Sanjarian F., Mohammadi goltapeh E., Safaei N. & Razavi Kh. 2016. Effect of salicylic acid on enzyme activity in wheat in immediate early time after infection with Mycosphaerella graminicola. Scientia agriculturae bohemica, 47(1): 1-8.
Gholamnezhad J., Sanjarian F., Mohammadi goltapeh E., Safaei N. & Razavi Kh. 2013. The evaluation of salicylic acid effect on septorios disease by Mycospharella graminicola, Research in Plant Pathology 2(2):35-46.
Gholamnezhad J., Sanjarian F., Mohammadi goltapeh E., Safaei N. and Razavi Kh. 2016. Study of defense genes expression profile pattern of wheat in response to infection by Mycosphaerella graminicola, Iranian Journal of Plant Biology, 8(30): 43-55.
Gill, S. S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. doi: 10.1016/j.plaphy.2010.08.016.
Gimenez MJ, Fernando P, Atienza SG (2010) Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta, DOI 10.1007/s00425-010-1290-y.
Gommers, F. J. 1973. Nematicidal principles in Compositae. Mededelingen Landbouwhogeschool, Wageningen, The Netherlands, 17: 71 -73.
Hammerschmidt, R. 2012. Secondary metabolites and defense: the story continues. Physiological and Molecular Plant Pathology 80: 3-4.
Holbrook C.C., Knouft D.A. and Dickson D.W. 1983. A technique for screening peanuts for resistance to Meloidogyne arenaria. Plant Disease. 67: 957-958.
Hussain M.A., Mukhtar and T. Kayani. M.Z. 2011. Efficacy evaluation of Azadirachta indica, Calotropis procera, Datura stramonium and Tagetes erecta against root-knot nematodes Meloidogyne incognita. Pak. J. Bot., 43 (1) (2011), pp. 197-204
Hussey, R. S., and Barker, K. R. 1973. A comparison of methods of collecting inocula of Meloidogynespp., including a new technique. Plant Disease Reporter 57:1025–1028.
Khan AM, Naz S, Abid M (2016). Evaluation of marine red alga Melanothamnus afaqhusainii against Meloidogyne incognita, fungus and as fertilizing potential on okra. Pak J Nematol 34(1):91–100 (Pakistan Society of Nematologists)
Khan, S.A., Anjum, S.A., Ansari, M.J., UllahKhan, M.H. et al. 2019. Antimicrobial potentials of medicinal plant’s extract and their derived silver nanoparticles: A focus on honey bee pathogen. Saudi Journal of Biological Sciences, 26(7): 1815-1834.
Kuźniak E, Skłodowska M. 2001. Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Science160, 723–731.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (−Delta Delta C (T) method. Methods, 25:402–408.
Medeiros, F., Resende., M.L., Medeiros, F.H.V., Pare. P. 2009.Defense gene expression induced by a coffee-leaf extract formulation in tomato. Physiological and Molecular Plant Pathology 74(2):175-183.
Mishra CD, Mohanty KC (2007). Role of phenolics and enzymes in imparting resistance to rice plants against root-knot nematode, Meloidogyne graminicola. Ind J Nematol 37(2):131-134.
Molinari S (1995). Difference in isoperoxidase activities of tomato roots susceptible and resistant to root-knot nematodes. Nematologia Mediterranea 23(2):271-281.
Molinari S (1995). Difference in isoperoxidase activities of tomato roots susceptible and resistant to root-knot nematodes. Nematologia Mediterranea 23(2):271-281.
Molinari S, Miacola C (1997). Catalase induction in galls produced by Meloidogyne sp. tomato root interactions in vitro. Nematologia Mediterranea 25(2):299-303.
Molinari, S. 2009. Bioassays on plant-nematode interactions. Pp. 293-326 inS. S. Narwal, D. A. Sampietro, C. A. N. Catalàn, M. A. Vattuone, and B. Politycka, co-eds. Plant bioassays. Studium Press LLC, New Delhi, India.
Naserinasab, F., Sahebani, N., Etebarian, H.R. 2011. Biological Control of Meloidogyne javanica by Trichoderma harzianum BI and Salicylic Acid on Tomato, African Journal of Food Science 5 (3), 276-280.
Naserinasab, F., Sahebani, N., Etebarian, H.R. 2011. Biological Control of Meloidogyne javanica by Trichoderma harzianum BI and Salicylic Acid on Tomato, African Journal of Food Science 5 (3), 276-280.
Neeraj, S., Goel, R., Kumar, A., Singh G., Madan. V.K. 2017. Effect of Plant Extracts on Hatching and Mortality of Root-Knot Nematode, Meloidogyne Incognita Larvae (in-Vitro). Biosciences Biotechnology Research Asia, 14(1): 467-471.
Noling, J. W. 2009. Nematode management in tomatoes, pepper, and eggplant. ENY-032, Florida Cooperative Extension Service, University of Florida, Gainesville, FL. http://edis.ifas.ufl.edu/ng032.
Okeniyi, M. O. 2010. Effect of botanical extracts on root-knot nematode (Meloidogyne incognita) infection and growth of cacao seedlings. Journal of Applied Biosciences, 36 : 2346-2352.
Paolacci A, Tanzarella O, Porceddu E, Ciaffi M. 2009. Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Mol Biol 10:11 Gimenez, M.J., Piston, F., Martin, A., Atienza, S.G. 2010. Application of real-time PCR on the development of molecular markers and to evaluate critical aspects for olive oil authentication. Food Chem 118:482–487.
Patel BA, Patel DJ, Patel RG, Talati JG (2001). Biochemical changes induced by infection of Meloidogyne spp. in chickpea. ICPN (8):13-14.
Patel DS, Nath K, Patel RL, Patel SI (2008) Management of fruit rot of Aonla caused by Aspergillus niger. 38: 658-651.
Pavaraj, M., Bakavathiappan , G., Baskaran. S. 2012. Evaluation of some plant extracts for their nematicidal properties against root-knot nematode, Meloidogyne incognita. Journal of Biopesticides, 5: 106-110.
Picard, K., Ponchet, M., Blein, J.P., Rey, P., Tirilly, N. 2004.Benhamon, Oligandrin. A proteinaceous molecule produced by the mycoparasitePythium oligandruminduces resistance toPhytophthora parasiticainfection in tomato plants, Plant Physiol. 124(1) 379–396.
Portillo, M., Cabrera, J., Lindsey, K., Topping, J., Andres, M.F., Emiliozzi, M., Oliveros, J.C., Gracia-Casado, G., Solano, R., Koltai, H., Resnick, N. and Escobar, C. (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared withArabidopsis:a functional role for gene repression.New Phytol.197, 1276–1290.
Radwan, M.A., Farrag, S.A., Abu-Elamayem, M.M., Ahmed. N.S. 2012. Biological Control of the Root-Knot Nematode, Meloidogyne incognita on Tomato Using Bioproducts of Microbial Origin. Applied Soil Ecology 56:58–62.
Saad, M.G., Ghareeb, R.Y., Saeed, A.A. 2019. The potential of endophytic fungi as bio-control agents against the cotton leafworm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). Egyptian Journal of Biological Pest Control. (2019) 29:7 https://doi.org/10.1186/s41938-019-0108-x.
Sharma, i.p., Sharma, A.K. 2015. .Effects of initial inoculums levels of Meloidogyne incognita J2 on development and growth of Tomato cv. PT-3 under control conditions. African journal of microbiology research 9(20):1376-1380.
Siddiqui I.A., Ehetshamul‐Haque, S., Shahid Shaukat, S. 2001. Use of Rhizobacteria in the Control of Root Rot–Root Knot Disease Complex of Mungbean. Journal of Phytopathology 149(6):337 – 346.
Sundararaju P, Suba KP (2006). Biochemical changes in banana plants induced by Pratylenchus coffeaeand Meloidogyne incognita. Ind J Nematol 36(2):256-259.
Tariq, M., Siddiqui M.A., Khan, A., Asif, M., Khan, F. 2018. Nematode suppressive effect of botanicals against the root-knot nematode M. Incognita infesting Solanum melongena L. Trends in Biosciences (2018), p. 2570.
Taylor, A. L., and Sasser, J. N. 1978. Biology, identification and control of root-knot nematodes (Meloidogyne species). N.C. State University Graphics: Raleigh, N.C.
Tsay, T.T., Wu, S.T., Lin, Y.Y. 2004. Evaluation of Asteraceae Plants for Control of Meloidogyne incognita. J Nematol. 36(1):36-41.
Uhlenbroek J. H., Bijloo. J. D. 2010. Investigations on nematicides: I. Isolation and structure of a nematicidal principe occurring in Tagetes roots.
Wuyts, n., Swennen, R., Waele D. 2006. Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 8(1):89-101.
Xu, Xiao Ming, Xu Kun, Yu Qin, Zhang-Xiaoyan (2008). The relationship between resistance to Meloidogyne incognita and phenylpropanes metabolism in roots of eggplant root-stock. Acta Phytophylacica Sinica 35(1):43-46.
Yedida, I., Benhamou, N., Chet, I. 1999. Induction of defenses in cucumber plants (Cucumis sativusL.) by the biocontrol agentTrichoderma harzianum, Appl. Environ. Microbiol. 65 (3) 1061–1070.
Zacheo, G., Arrigoni-Liso, R., Belve-Zacheo, T., Lamberti, F., and Arrigoni, O. 1983. Mitochondria peroxidase and superoxidase dismutase activities during infection by Meloidogyne incognita of susceptible and resistant tomato plants. Nematologia Mediterranea, 11:107–114.