Evaluation of Chitosan, Gamma-Aminobutyric Acid and Potassium Silicate on some Biochemical Parameters of Pistachio Tree to Induce Resistance against Pistachio Psyllid (Agonoscena pistaciae)

Document Type : Research Article

Authors

1 Department of Plant Protection, Faculty of Agriculture,Shahid bahonar university of Kerman, Kerman, Iran

2 Mohaghegh Ardabili University

Abstract

Introduction
Pistachio (Pistacia vera L.), is a small tree native to Iran and Central Asia, grown for its edible seeds. The pistachio nut is an important export product and has a special value among agricultural products. The pistachio psylla, Agonoscena pistaciae Burckhardt and Lauterer (Hemiptera, Psyllidae), is one of the key pests of pistachio trees. It is distributed in Turkey, Greece, Iran, Armenia, and Tajikistan. In both adult and nymphal stages, it directly damages trees by absorbing plant sap. Moreover, psyllids are usually involved in the transmission of pathogens and cause significant losses to the host. The stimulation of the same plant defense mechanisms by specific inducing agents (elicitors) is an alternative tool to protect plants against pests. Natural or synthetic elicitors make induced systemic resistance (ISR). In recent years, researchers have been interested in finding efficient and environmentally friendly methods to prevent biotic agents that damage plants, such as the application of potential ISR elicitors. Elicitors can influence the secondary metabolite contents in plants in response to herbivores and induce defense mechanisms, thereby increasing the resistance of plants against pests. Further, secondary metabolites can affect oxidative stress through producing free radicals and modifying the antioxidant enzyme systems. The catalase and peroxidase enzymes play an important role in the defense system of plants. Thus, the present research was conducted to evaluate the effects of chitosan, gamma-aminobutyric acid and potassium silicate on the contents of secondary metabolites and biochemical compounds in pistachio leaves and the resultant effects on the pest population control.
 
Materials and Methods
The field experiments were conducted on 30-year-old pistachio trees (cv. Fandoghi) in a 1-hectare orchard located in Najaf Shahr, Sirjan, Kerman, Iran during 2023. In this research, the effect of various compounds including chitosan (0.5%), potassium silicate (2%), and gamma-aminobutyric acid (GABA) (10 mM) were studied on the population reduction rate of pistachio psyllid nymphs in field conditions. The distilled water was applied as control treatment. Furthermore, the amount of enzymatic and biochemical compounds including antioxidant enzymes (catalase and peroxidase), hydrogen peroxide, proline, total phenol and flavonoids were determined in the leaves of the treated pistachio trees. Finally, variables evaluated using the one-way analysis of variance in SPSS. Then, the Tukey test was done for mean comparisons.
 
Results and Discussion
In this study, spraying various compounds, especially chitosan on pistachio trees, reduced the population of the psyllid nymphs. The control efficiency (%) of studied inducers showed an increasing trend in treatments of GABA (23.76%), potassium silicate (34.39%) and chitosan (46.23%), respectively. No significant difference was observed in the flavonoid contents among different treatments. Indeed, the level of total phenol in the chitosan treatment was significantly higher than others. Therefore, the difference in the control effect percentage of the psyllid nymph population between the tested treatments can be related to the presence of phenolic compounds and other secondary metabolites. Some studies have proved a negative correlation between the presence of phenolic compounds in the host plant and the population of insects. On the other hand, pistachio trees treated with different compounds in terms of hydrogen peroxide, proline, enzymes of catalase and peroxidase showed a significant difference. The highest amounts of catalase and peroxidase enzymes were significantly observed in trees treated with chitosan (1.73 and 0.031 U.min-1.mg-1 protein, respectively). Peroxidase and catalase enzymes are important antioxidants which destroy free radicals. Also, the highest and lowest amount of proline was significantly recorded in the control (52.48 μM.g-1 FW) and chitosan (42.40 μM.g-1 FW) treatments, respectively. In addition, the amount of hydrogen peroxide in the GABA treatment (128.71 μM.g-1 DW) was significantly higher than other treatments, which related to the peroxidase enzyme (0.016 U.min-1.mg-1 protein) decrease in the plant. Peroxidase enzyme is activated by biological stress and plays an important role in protecting the cell against different toxic concentrations of hydrogen peroxide. The findings of this research showed the lower population of the psyllid nymphs in chitosan treatment was related to the higher relative content of phenol and more activity of antioxidant enzymes (catalase and peroxidase) in pistachio trees.
 
Conclusion
This study showed that treatment of pistachio trees with different plant resistance inducers, especially chitosan, causes physiological changes in the plant and subsequently the reduction of pistachio psyllid damage. After complementary tests on the quality and quantity of the product, these compounds can be used in integrated management programs of A. pistaciae to minimize the use of insecticides.



 
 



 

Keywords

Main Subjects


©2025 The author(s). This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source

  1. Abdou, N.M., El-Saadony, F.M. A., Roby, M.H.H., Mahdy, A.A., El-Shehawi, A.M., Elseehy, M.M., El-Tahan, A.M., Abdalla, H.S., Ahmed, M., & AbouSreea, A.I.B. (2022). Foliar spray of potassium silicate, aloe extract composite and their effect on growth and yielding capacity of roselle (Hibiscus sabdariffaL.) under water deficit stress conditions. Saudi Journal of Biological Sciences, 33(2), 1-12. https://doi.org/10.1016/j.sjbs.2022.02.033
  2. Aparecida De Assis, F., Campos-Moraes, J., Paterno-Silveira, L.C., Françoso, J., Maria-Nascimento, A., & Silveira-Antunes, C. (2012). Inducers of resistance in potato and its effects on defoliators and predatory insects. Revista Colombiana de Entomología, 38(1), 30–34. https://doi.org/10.25100/socolen.v38i1.8914
  3. Asghari, M. (2019). Impact of jasmonates on safety, productivity and physiology of food crops. Trends in Food Science & Technology91, 169-183. https://doi.org/1016/j.tifs.2019.07.005
  4. Assis, F.A., Moraes, J.A., Assis, G.A., & Parolin, F.J.T. (2015). Induction of caterpillar resistance in sunflower using silicon and acibenzolar-S-methyl. Journal of Agricultural Science and Technology, 17, 543-550
  5. Badawy, M.E. I.; & El-Aswad, A.F. (2012). Insecticidal activity of chitosans of different molecular weights and chitosan-metal complexes against cotton leaf worm Spodoptera littoralis and oleander aphid Aphis nerii. Plant Protection Science, 48, 131–141. https://doi.org/10.17221/67/2010-pps
  6. Balakhnina, T.I. (2013). Effects of silicon on plant resistance to environmental stresses. Review of [International Agrophysics], 27, 225-232. https://doi.org/2478/v10247-012-0089-4
  7. Bao, H., Chen, X., Lv, S., Jiang, P., Feng, J.J., Fan, P.X., Nie, L.L., & Li, Y.X. (2015). Virus induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by γ-aminobutyric acid metabolic pathway. Plant Cell & Environment, 38, 600–613. https://doi.org/10.1111/pce.12419
  8. Barbosa, J.M., Singh, N.K., Cherry, J.H., & Locy, R.D. (2010). Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thalianaPlant Physiology and Biochemistry48(6), 443-450.‏ https://doi.org/10.1016/j.plaphy.2010.01.020
  9. Bates, L.S., Waldren, R.P.A., & Teare, I.D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil39, 205-207.‏ https://doi.org/10.1007/bf00018060
  10. Bernays, E.A., Driver, G.C., & Bilgener, M. (1989). Herbivores and plant tannins. Advances in Ecological Research19, 263-302.‏ https://doi.org/10.1016/S0065-2504(08)60160-9
  11. Bidart‐Bouzat, M.G., & Imeh‐Nathaniel, A. (2008). Global change effects on plant chemical defenses against insect herbivores. Journal of Integrative Plant Biology50(11), 1339-1354.‏ https://doi.org/10.1111/j.1744-7909.2008.00751.x
  12. Boroujerdnia, M., Bihamta, M.R., AlamiSaid, K.H., & Abdossi, V. (2016). Effect of drought tension on proline content, soluble carbohydrates, electrolytes leakage and relative water content of bean (Phaseolus vulgaris). Crop Physiology Journal8(29), 23-41. (In Persian)‏
  13. Bown, A.W., Hall, D.E., & MacGregor, K.B. (2002). Insect footsteps on leaves stimulate the accumulation of 4-aminobutyrate and can be visualized through increased chlorophyll fluorescence and superoxide production. Plant Physiology129(4), 1430-1434.‏ https://doi.org/10.1104/pp.006114
  14. Cakmak, I., & Marschner, H. (1992). Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiology98(4), 1222-1227. https://doi.org/10.1104/pp.98.4.1222
  15. Chen, D., Cao, B., Wang, S., Liu, P., Deng, X., Yin, , & Zhang, S. (2016). Silicon moderated the K deficiency by improving the plant-water status in sorghum. Scientific Reports, 6, 22882. https://doi.org/10.1038/srep22882
  16. Chen, W.P., Li, P.H., & Chen, T.H.H. (2000). Glycinebetaine increases chilling tolerance and reduces chilling‐induced lipid peroxidation in Zea maysPlant, Cell & Environment23(6), 609-618.‏ https://doi.org/10.1046/j.1365-3040.2000.00570.x
  17. Correa, R.S., Moraes, J.C., Auad, A.M., & Carvalho, G.A. (2005). Silicon and acibenzolar-S-methyl as resistance inducers in cucumber, against the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B. Neotropical Entomology34, 429-433.‏ https://doi.org/10.1590/S1519-566X2005000300011
  18. Egea, C., Ahmed, A.S., Candela, M., & Candela, M.E. (2001). Elicitation of peroxidase activity and lignin biosynthesis in pepper suspension cells by Phytophthora capsiciJournal of Plant physiology158(2), 151-158. https://doi.org/10.1078/0176-1617-00079
  19. El Hadrami, A., Adam, L.R., El Hadrami, I., & Daayf, F. (2010). Chitosan in plant protection. Marine Drugs, 8, 968-987. https://doi.org/10.3390/md8040968
  20. Fahmy, N.M., Amin, T.R., & Khedr, M. (2022). Changes in antioxidant enzymes during the development of the cotton leafworm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae). Egyptian Academic Journal of Biological Sciences. A, Entomology15(3), 151-163.‏ https://doi.org/10.21608/eajbsa.2022.264624
  21. Ferry, N., Stavroulakis, S., Guan, W., Davison, G.M., Bell, H.A., Weaver, R.J., & Gatehouse, A.M. (2011). Molecular interactions between wheat and cereal aphid (Sitobion avenae): analysis of changes to the wheat proteome. Proteomics11(10), 1985-2002.‏ https://doi.org/10.1002/pmic.200900801
  22. Ganji, Z., Hosseini Naveh, V., Ashouri, A., & Maali Amiri, R. (2019). Some biochemical responses of pistachio to feeding of the common pistachio psylla, Agonoscena pistaciaePlant Pest Research9(3), 15-27.
  23. Gantner, M., Najda, A., & Piesik, D. (2019). Effect of phenolic acid content on acceptance of hazel cultivars by filbert aphid. Plant Protection Science55(2), 116–122. https://doi.org/10.17221/150/2017-PPS
  24. Ghasemzadeh, A., Jaafar, H.Z., & Rahmat, A. (2010). Antioxidant activities, total phenolics and flavonoids content in two varieties of Malaysia young ginger (Zingiber officinale Roscoe). Molecules15(6), 4324-4333. https://doi.org/10.3390/molecules15064324
  25. Gliñski, J. (2011). Agrophysical Objects (Soils, Plants, Agricultural Products, and Food). Encyclopedia of Agrophysics. In J. Gliñski, J. Horabik, and J. Lipiec (Eds), Springer Dordrecht, Heidelberg, London, New York. 1100pp. https://doi.org/10.1007/978-90-481-3585-1_9.
  26. ‏Goldberg, R., Imberty, A., Liberman, M., & Prat, R. (1986). Relationships Between Peroxidatic Activities and Cell Wall Plasticity. Molecular and physiological aspects of plant peroxidases. In H. Greppin, C. Penel, and Th. Gaspar (Eds), ‏ Botanical Center, University of Geneva, Switzerland, pp. 209-220. https://www.researchgate.net/publication/228127847
  27. Gomaa, M., Kandil, E.E., El-Dein, A.A.Z. Abou-Donia, E.M. , Ali, H.M., & Abdelsalam N.R. (2021). Increase maize productivity and water use efficiency through application of potassium silicate under water stress. Scientific Reports, 11, 1–8. https://doi:10.1038/s41598-020-80656-9
  28. Gomez, S.K., Oosterhuis, D.M., Rajguru, S.N., & Johnson, D.R. (2004). Foliar antioxidant enzyme responses in cotton after aphid herbivory.‏ Journal of Cotton Science, 8(2), 99-104.
  29. Hafez, E.M., Osman, H.S., El-Razek, U.A.A., Elbagory M., El-Dein Omara, A., Eid, A.M.M., Gowayed, S., & Elbagory, M. (2021). Foliar-applied potassium silicate coupled with plant growth-promoting Rhizobacteria improves growth, physiology, nutrient uptake and productivity of faba bean (Vicia faba) irrigated with saline water in salt-affected soil. Plants, 10, 894. https://doi.org/10.3390/plants10050894
  30. Hassanvand, F., & Rezaei Nejad, A. (2018). Effect of potassium silicate on growth, physiological and biochemical characteristics of Pelargonium graveolens under salinity stress. Iranian Journal of Horticultural Science, 48(4) 743-752. (in Persian with English abstract). https://doi.org/10.22059/ijhs.2018.210950.1040
  31. Hayyan, M., Hashim, M.A., & AlNashef, I.M. (2016). Superoxide ion: Generation and chemical implications. Chemical Reviews116(5), 3029-3085. https://doi.org/10.1021/acs.chemrev.5b00407
  32. Henderson, C.F., & Tilton, E.W. (1955). Tests with acaricides against the brown wheat mite. Journal of Economic Entomology, 48(2), 157-61. https://doi.org/10.1093/jee/48.2.157
  33. Jafari, F.J., & Javadi, A. (2020). The Effect of chitosan coating incorporated with walnut leaf extract on shelf life of pistachio. Food Research Journal30(3), 221-232. (in Persian with English abstract)
  34. Jin, X., Liu, T., Xu, J., Gao, Z., & Hu, X. (2019). Exogenous GABA enhances muskmelon tolerance to salinity-alkalinity stress by regulating redox balance and chlorophyll biosynthesis. BMC Plant Biology, 19, 48. https://doi.org/10.1186/s12870-019-1660-y.
  35. Justyna, P.G., & Ewa, K. (2013). Induction of resistance against pathogens by β -aminobutyric acid. Acta Physiologiae Plantarum, 35, 1735-1748. https://doi.org/10.1007/s11738-013-1215-z
  36. Katiyar, D., Hemantaranjan, A., & Singh, B. (2015). Chitosan as a promising natural compound to enhance potential physiological responses in plant: a review. Indian Journal of Plant Physiology, 20, 1–9. https://doi.org/10.1007/s40502-015-0139-6
  37. Khattab, H. (2007). The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae). Australian Journal of Basic and Applied Sciences1(1), 56-62.‏
  38. Khavari-Nejad, S. (2018). A review on plant peroxidases. Nova Biologica Reperta, 5(4), 428-437. https://doi.org/10.29252/nbr.5.4.428
  39. Khayat Moghadam, M.S., Gholami, A., Shirani Rad, A.H., BaradaranFiroozabadi, M., & Abbasdokht, H. (2021). The effect of potassium silicate and late-season drought stress on the physiological characters of canola. Journal of Crops Improvement23(4), 776-761. (in Persian with English abstract). https://doi: 10.22059/jci.2021.306872.2424
  40. Lang, J., Gonzalez-Mula, A., Taconnat, L., Clement, G., & Faure, D. (2016). The plant GABA signaling downregulates horizontal transfer of the Agrobacterium tumefaciens virulence plasmid. New Phytology, 210, 974–983. https://doi.org/10.1111/nph.13813
  41. Mahanil, S., Attajarusit, J., Stout, M.J., & Thipyapong, P. (2008). Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Science174(4), 456-466. https://doi.org/10.1016/j.plantsci.2008.01.006
  42. Mahmoudi Meimand, J., & Ghanbari Adivi, A. (2013). A new approach to the management of pistachio planting and harvesting. Newshe Publications, Shahrekord, Iran, 128 p. (In Persian)
  43. Mai, V.C., Bednarski, W., Borowiak-Sobkowiak, B., Wilkaniec, B., Samardakiewicz, S., & Morkunas, I. (2013). Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisumPhytochemistry93, 49-62. https://doi.org/10.1016/j.phytochem.2013.02.011
  44. Mehrnejad, M.R. (2001). The current status of pistachio pests in Iran. Cahiers Options Méditerranéennes56(1), 315-322.
  45. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science7(9), 405-410.‏ https://doi.org/10.1016/s1360-1385(02)02312-9
  46. Molinari, H.B.C., Marur, C.J., Daros, E., de Campos, M.K.F., de Carvalho, J., Bespalhok, J.C., Pereira, L.F.P., & Vieira, L.G.E. (2007). Evaluation of the stress‐inducible production of proline in transgenic sugarcane (Saccharum): Osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum130(2), 218-229. https://doi.org/10.1111/j.1399-3054.2007.00909.x
  47. Naderi, S., Esmaeilzadeh Bahabadi, S., & Fakheri, B. (2015). The effect of chitosan on some physiological and biochemistry characterization in basil (Ocimum basilicum). Journal of Plant Process and Function. Iranian Society of Plant Physiology, 4(12), 29-41. (In Persian)
  48. Parida, A.K., & Das, A.B. (2005). Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety60(3), 324-349. https://doi.org/10.1016/j.ecoenv.2004.06.010
  49. Pereira, R.R.C., Moraes, J.C., Prado, E., & DaCosta, R.R. (2010). Resistance inducing agents on the biology and probing behaviour of the greenbug in wheat. Scientia Agricola, 67, 430-434. https://doi.org/10.1590/s0103-90162010000400009
  50. Polle, A., Otter, T., & Seifert, F. (1997). Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies). Plant Physiology106(1), 53-60.‏ https://doi.org/10.1104/pp.106.1.53
  51. Reynolds, O.L., Keeping, M.G., & Meyer, J.H. (2009). Silicon‐augmented resistance of plants to herbivorous insects: A review. Annals of Applied Biology155(2), 171-186. https://doi.org/10.1111/j.1744-7348.2009.00348.x
  52. Rouhani, M., & Samih, M.A. (2012). Mortality effect of plant extracts with pesticide on common pistachio psylla, Agonoscena pistaciaeArchives Des Sciences65(8), 452-460. https://doi.org/10.1080/03235408.2019.1570589
  53. Sabbour, M.M. (2019). Effect of chitosan and nano-chitosan on Saissetia oleae (Hemiptera: Coccidae). Journal of Applied Sciences, 19(2), 128-132. https://doi.org/10.3923/jas.2019.128.132
  54. Sabbour, M.M., & Abdel-Hakim, E.A. (2018). Control of Cassida vittata (Vill) (Coleoptera: Chrysomelidae) using chitosan and nano chitosan. Middle East Journal of Applied Sciences, 8(1), 141-144.
  55. Saed-Moucheshi, A., Sohrabi, F., & Shirkhani, A. (2023). A review on reactive oxygen species (ROS): production, function, and their influence on plants. Crop Biotechnology13(2), 53-70.‏ (in Persian with English abstract)
  56. Sattari Nasab, R., Pahlavan Yali, M., & Bozorg-Amirkalaee, M. (2019) Effects of humic acid and plant growth-promoting rhizobacteria (PGPR) on induced resistance of canola to Brevicoryne brassicae Bulletin of Entomological Research, 109(4), 479-489. https://doi.org/10.1017/s0007485318000779
  57. Shabani, Z., Samih, M.A., Irannezad, M.A., & Mirzaii, F. (2011). Insecticidal efficacy of acetamiprid, hexaflumuron and Calotropis procera extract on Agonoscena pistaciae Burckhardt and Lauterer under laboratory conditions. Global Conference on Entomology, March 5-9, Chiang Mai, Thailand. 481p. https://doi.org/10.5604/01.3001.0014.7877
  58. Shahid, M., Pourrut, B., Dumat, C., Nadeem, M., Aslam, M., & Pinelli, E. (2014). Heavy-metal induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Reviews of Environmental Contamination and Toxicology, 232, 1-44. https://doi.org/10.1007/978-3-319-06746-9_1
  59. Shahrokhy, M., Pahlavan Yali, M., & Bozorg-Amirkalaee, M. (2024). Role of exogenous elicitors in canola plant defense against cabbage aphid by regulating physiological balance and secondary metabolite biosynthesis. Journal of Agricultural Science and Technology, 26(1), 165-176. https://doi.org/10.21203/rs.3.rs-1575991/v1
  60. Sheikha, S.A.A., & AL-Malki, F.M. (2015). Chitosan influence on the amino acids and proline content in the plants under drought stress. Journal of Plant Production6(4), 447-455.‏ https://doi.org/10.21608/jpp.2018.49344
  61. Soland, S.F., & Laima, S.K. (1999). Phenolics and cold tolerance of Brassica napusPlant Agriculture1, 1-5.
  62. Tahami Zarandi, S.M.R., Askarianzadeh, A., & Karimi, J. (2022). Evaluation of the chemical and cultural control methods of the common pistachio psylla, Agonoscena pistaciae (Hem.: Psyllide) in laboratory and field conditions. Iranian Journal of Plant Protection Science. 53(2), 271-282. (in Persian with English abstract). https://doi: 10.22059/IJPPS.2023.350634.1007013
  63. Taheri, F., Dahmardeh, M., Salari, M., & Bagheri, R. (2018). Evaluate the effect of chitosan on the activities of antioxidant enzymes in ajwain(Carum copticum ) under drought stress. Iranian Journal of Horticultural Sciences, 48(3), 575-584. (in Persian with English abstract)
  64. Taghipour, S., Ehtesham, N.A., & Hokmabadi, H. (2024). The effect of pre-harvest chitosan and nano-chitosan application on the shelf life and quality of fresh pistachio (Pistacia vera Cv. 'Ahmad-Aghaei').‏ Iranian Journal of Horticultural Science and Technology, 25(1), 149-162. (in Persian with English abstract) https://doi.org/10.2139/ssrn.4397721
  65. Taiz, L., & Zeiger, E. (2002). Plant Physiology. Sinauer Associates Inc Publishers. Sunderland, MA, 690 ‏
  66. Todd, G.W., Getahun, A., & Cress, D.C. (1971). Resistance in barley to the greenbug, Schizaphis graminum. 1. Toxicity of phenolic and flavonoid compounds and related substances. Annals of the Entomological Society of America64(3), 718-722.‏ https://doi.org/10.1093/aesa/64.3.718
  67. Toscano, N.C., & Prabhaker, N. (2011). Spiromesifen: A New Pest Management Tool for Whitefly Management. Available at .http://www.insectscience.org /8.04/ref/ abstract 78.html.
  68. Usha Rani, P., & Jyothsna, Y. (2010). Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiologiae Plantarum32, 695-701.‏ https://doi.org/10.1007/s11738-009-0449-2
  69. Velikova, V., Yordanov, I., & Edreva, A.J.P.S. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science151(1), 59-66.‏ https://doi.org/10.1016/s0168-9452(99)00197-1
  70. Wang, C.Y., Fan, L.Q., Gao, H.B., Wu, X.L., Li, J.R., Lv, G.Y., & Gong, B.B. (2014). Polyamine biosynthesis and degradation are modulated by exogenous gamma-aminobutyric acid in root-zone hypoxia-stressed melon roots, Plant Physiologyand Biochemistry, 82, 17–26. https://doi.org/10.1016/j.plaphy.2014.04.018
  71. War, A.R., Buhroo, A.A., Hussain, B., Ahmad, T., Nair, R.M., & Sharma, H.C. (2020). Plant defense and insect adaptation with reference to secondary metabolites. Reference Series in PhytochemistryCo-evolution of Secondary Metabolites, Springer International Publishing. 795-822.‏ https://doi.org/1007/978-3-319-96397-6_60
  72. Wójcicka, A. (2010). Cereal phenolic compounds as biopesticides of cereal aphids. Polish Journal of Environmental Studies19(6), 1337-1343.‏
  73. Zhen, A., Zhang, Z., Jin, X.Q., Liu, T., Ren, W.Q., & Hu, X.H. (2018). Exogenous GABA application improves the NO3 -N absorption and assimilation in Ca(NO3)2 treated muskmelon seedlings. Science of Horticulture, 227, 117–123. https://doi.org/10.1016/j.scienta.2017.09.025
  74. Zhishen, J., Mengcheng, T., & Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry64(4), 555-559.‏ https://doi.org/10.1016/s0308-8146(98)00102-2
  75. Zhu-Salzman, K., Salzman, R.A., Ahn, J.E., & Koiwa, H. (2004). Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiology134(1), 420-431.‏ https://doi.org/10.1104/pp.103.028324
  76. Ziaaddini, F., Yali, M.P., & Bozorg-Amirkalaee, M. (2022). Foliar spraying of elicitors in pear trees induced resistance to Cacopsylla bidensJournal of Asia-Pacific Entomology25(4), 101969. https://doi.org/10.1016/j.aspen.2022.101969‏  
CAPTCHA Image