Effects of different concentrations of chitosan bio-stimulant on some physiological and biochemical traits of Andrographis paniculate L.
Subject Areas : Medicinal Plants
Mozhdeh Jafari Lafoot
1
(Department of Biology, Islamshahr Branch, Islamic Azad University, Islamshahr, Iran)
Leila Pishkar
2
(Department of Biology, Islamshahr Branch, Islamic Azad University, Islamshahr, Iran)
Daryush Talei
3
(Medicinal Plants Research Center, Shahed University, Tehran, Iran)
Keywords: Photosynthetic pigments, Antioxidant capacity, Chitosan, Secondary metabolites, Andrographis paniculata L,
Abstract :
Chitosan is a nitrogen containing polysaccharide synthesized naturally by deacetylation reaction of chitin, which is confirmed as an efficient bio-stimulant to improve production of secondary metabolites in medicinal plants. In the present study, the effects of chitosan (0, 100, 200, 300, and 400 mg/L) on growth, photosynthetic pigments, secondary metabolites, antioxidant capacity, activity of antioxidant enzymes, quantity and quality of protein, and the expression of HMGS and HMGR genes were examined in Andrographis paniculata L. The results showed that application of chitosan significantly increased the chlorophyll and carotenoids and, as a result, increased plant growth and biomass. Chitosan treatments (300 and 400 mg/L) increased the expression of HMGS and HMGR genes in plant leaves, which was associated with a significant increase in the accumulation of total phenols and flavonoids. Also, chitosan improved the activity of superoxide dismutase and peroxidase enzymes and increased the antioxidant capacity of A. paniculata leaves. Examination of the quantity and quality of proteins showed that the intensity of protein bands with the molecular weight of 60 kD under 300 and 400 mg/L chitosan treatment and also the intensity of protein bands with the molecular weights of 35 and 20 kD under 300 mg/L chitosan treatment increased compared to the other concentrations. Therefore, these results revealed that application of chitosan can increase accumulation of secondary metabolites and the antioxidant capacity in the medicinal plant A. paniculata.
Abdel-Mawgoud, A.M.R., Tantawy, A.S., El-Nemr, M.A. and Sassine, Y.N. (2010). Growth and yield responses of strawberry plants to chitosan application. European Journal of Scientific Research. 39(1): 161-8.
Agrawal, G., Rakwal, R., Tamogami, S., Yonekurad, M., Kubo, A. and Saji, H. (2002). Chitosan activates defense/stress response(s) in the leaves of Oryza Sativa seedlings. Plant Physiology and Biochemistry. 40: 1061-9.
Arriola, O.C., Rocha, M.C., Hernandez, A.B., Brauer, J.M.E. and Jatomea, M.P. (2013). Controlled release matrices and micro/nanoparticles of chitosan with antimicrobial potential: development of new strategies for microbial control in agriculture. Journal of the Science of Food and Agriculture. 93(7): 1525-36
Benzie, I., and Strain, J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical Biochemistry. 239: 70-76.
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Annual Biochemistry. 72: 248-254
Cheng, X., Zhou, U. and Cui, X. (2006). Improvement of phenylethanoid glycosides biosynthesis in Cistanche deserticola cell suspension cultures by chitosan elicitor. Biotechnology Journal. 121: 253-60.
El-Tantawy E.M. (2009). Behavior of tomato plants as affected by spraying with chitosan and aminofort as natural stimulator substances under application of soil organic amendments. Pakistan Journal of Biological Sciences. 12(17): 1164-73.
Esmaeilzadeh Bahabadi, S., Sharifi, M., Safaie, N. and Behmanesh, M. (2012). Enhancement of lignan and phenylpropanoid compounds production by chitosan in Linum album cell culture. Iranian Journal of Plant Biology. 4(11): 13-26.
Fielding, J.L. and Hall, J. (1978). A biochemical and cytochemical study of peroxidase activity in root of Pisum sativam. Journal of Experimental Botany. 29: 981-989.
Gerami, M., Ghorbani, A., and Karimi, S. (2018). Role of salicylic acid pretreatment in alleviating cadmium-induced toxicity in Salvia officinalis L. Iranian Journal of Plant Biology. 10(1): 81–95.
Ghasemi-Omran, V.O., Ghorbani, A., and Sajjadi-Otaghsara, S.A. (2021). Melatonin alleviates NaCl-induced damage by regulating ionic homeostasis, antioxidant system, redox homeostasis, and expression of steviol glycosides-related biosynthetic genes in in vitro cultured Stevia rebaudiana Bertoni. In Vitro Cellular & Developmental Biology – Plant. 57: 319–331.
Ghorbani, A., Ghasemi Omran, V.O., Razavi, S.M., Pirdashti, H., and Ranjbar, M. (2019) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Reports 38: 1151–1163.
Ghorbani, A., Pishkar, L., Roodbari, N., Pehlivan, N., and Wu, C. (2021). Nitric oxide could allay arsenic phytotoxicity in tomato (Solanum lycopersicum L.) by modulating photosynthetic pigments, phytochelatin metabolism, molecular redox status and arsenic sequestration. Plant Physiology and Biochemistry 167: 337–348.
Ghorbani, A., Razavi, S.M., Ghasemi Omran, V.O. and Pirdashti, H. (2018a). Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russian Journal of Plant Physiology. 65: 898–907.
Ghorbani, A., Razavi, S.M., Ghasemi Omran, V.O., and Pirdashti, H. (2018b). Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biology 20: 729–736.
Giannopolitis, C.N. and Ries, S.K. (1977). Superoxide dismutase I. Occurrences in higher plants. Plant Physiology. 59(2): 309-414.
Goulas, V., and Manganaris, G.A. (2011). The effect of postharvest ripening on strawberry bioactive composition and antioxidant potential. Journal of the Science of Food and Agriculture. 91: 1907–1914.
Harish Prashanth, K.V., Dharmesh, S.M., Jagannatha Rao, K.S. and Tharanathan, R.N. (2007). Free radical-induced chitosan depolymerized products protect calf thymus DNA from oxidative damage. Carbohydrate Research. 342: 190-5.
Hussaini Begum, M., Taheri, G.H., Vaezi Kakhaki, M.R. and Tlaty, M. (2013). Foliar application of chitosan on growth and morphological characteristics of marigold (Calendula officinalis). National Conference of passive defense in the agricultural sector. 2013 November 30.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
Landi, L., De Miccolis Angelini, R.M., Pollastro, S., Feliziani, E., Faretra, F. and Romanazzi, G. (2017). Global transcriptome analysis and identification of differentially expressed genes in strawberry after preharvest application of Benzothiadiazole and chitosan. Frontiers in Plant Science. 8: 235.
Liao, P., Chen, X., Wang, M., Bach, T.J. and Chye, M.L. (2018). Improved fruit α-tocopherol, carotenoid, squalene and phytosterol contents through manipulation of Brassica juncea 3-HYDROXY-3-METHYLGLUTARYLCOA SYNTHASE1 in transgenic tomato. Plant Biotechnology Journal. 16: 784–796.
Liao, P., Wang, H., Wang, M., Hsiao, A.S., Bach, T.J. and Chye, M.L. (2014). Transgenic tobacco overexpressing Brassica juncea HMG-CoA synthase 1 shows increased plant growth, pod size and seed yield. PLoS One. 9: e98264
Lichtenthaler, H. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods of Enzymology. 148: 350-382.
Limpanavech, P., Chaiyasuta, S., Vongpromek, R., Pichyangkura, R., Khunwasi, C., Chadchawan, S., Lotrakul, P., Bunjongrat, R., Chaidee, A. and Bangyeekhun, T. (2008). Chitosan effects on floral production, gene expression, and anatomical changes in the Dendrobium orchid. Scientia Horticulturae. 116: 65–72
Lin, F.L., Wu, S.J., Lee, S.C. and Ng, L.T. (2009). Antioxidant, antioedema and analgesic activities of Andrographis paniculata extracts and their active constituent andrographolide. Phytotherapy Research. 23(7): 958‐964.
Liu, J., Tian, S., Meng, X. and Xu, Y. (2007). Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Journal of Postharvest Biology and Technology. 44: 300-306.
Marinova, D., Ribarov, F. and Atanassova, M. (2005). Total phenolics and total flavonoids in Bolgarian fruits and vegetables. Journal of the University of Chemical Technology and Metallurgy. 40: 255-260.
Martins, H.M., Martins M.L., Dias, M.I. and Bernardo, F. (2001). Evaluation of microbiological quality of medicinal plants used in natural infusions. International Journal of Food Microbiology. 58: 149-153.
Mehregan, M., Mehrafarin, A., Labbafi, M. and Naghdi Badi, H. (2017). Effect of different concentrations of chitosan biostimulant on biochemical and morphophysiological traits of stevia plant (Stevia rebaudiana Bertoni). Journal of Medicinal Plants. 16(62): 169-181
Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies. 15(4): 523-530.
Mishra, U.S., Mishra, A., Kumari, R., Murthy, P.N. and Naik, B.S. (2009). Antibacterial activity of ethanol extract of Andrographis paniculata. Indian Journal of Pharmaceutical Sciences. 71: 436‐438.
Mondal, M.A., Malek, M.A., Puteh, A.B., Ismail, M.R., Ashrafuzzaman, M. and Naher, L. (2012). Effect of foliar application of chitosan on growth and yield in okra. Australian Journal of Crop Science. 6(5): 918-921
Mukta, J.A., Rahman, M., Sabir, A.A., Gupta, D.R., Surovy, M.Z., Rahman, M. and Islama, M.T. (2017). Chitosan and plant probiotics application enhance growth and yield of strawberry. Biocatalysis and Agricultural Biotechnology. 11: 9-18.
Naderi, S., Esmaeilzadeh Bahabadi, S. and Fakheri, B. (2015). The effect of chitosan on some physiological and biochemictry characterization in basil (Ocimum basilicum). Plant Process and Function. 4(12); 29-41
Palida, S., Rath, P. and Supachitra, C. (2014). Chitosan increased phenolic compound contents in tea (Camellia sinensis) leaves by Pre- and Post-treatments. Journal of Chitin and Chitosan Science. 2(2): 93-98.
Pichynagkura, R. and Kudan, S. (2002). Quantitative production of 2-acetamido 2-deoxy-Dglucose from cryatallin chitin by bactrial Chitinase. Carbohydrate Research. 337: 1-9.
Pirbalouti, A.G., Malekpoor, F., Salimi, A., Golparvar, A. (2017). Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Scientia Horticulturae. 217: 114-122.
Portu, J., López, R., Baroja, E., Santamaría, P. and Garde-Cerdán, T. (2016). Improvement of grape and wine phenolic content by foliar application to grapevine of three different elicitors: Methyl jasmonate, chitosan, and yeast extract. Food Chemistry. 201: 213–221.
Rabea, E.I., Badawy, M.E., Stevens, C.V., Smagghe, G. and Steurbaut, W. (2003). Chitosan as antimicrobial agent: Aplications and mode of action. Biomacromolecules. 4(5): 1457-65.
Schaller, H., Grausem, B., Benveniste, P., Chye, M.L., Tan, C.T., Song, Y.H. and Chua, N.H. (1995). Expression of the Hevea brasiliensis (H.B.K.) Mull. Arg. 3-hydroxy-3-methylglutaryl-coenzyme A reductase 1 in tobacco results in sterol overproduction. Plant Physiology. 109: 761–770.
Silva, V., Singh, R.K., Gomes, N., Soares, B.G., Silva, A., Falco, V., Capita, R., Alonso-Calleja, C., Pereira, J.E., Amaral, J.S., Igrejas, G. and Poeta, P. (2020). Comparative insight upon chitosan solution and chitosan nanoparticles application on the phenolic content, antioxidant and antimicrobial activities of individual grape components of Sousão variety. Antioxidants. 9: 178.
Suwanmanee, P., Sirinupong, N. and Suvachittanont, W. (2013). Regulation of 3-hydroxy-3-methylglutaryl-CoA synthase and rubber biosynthesis of Hevea brasiliensis (B.H.K.) Mull. Arg. In: Bach TJ, Rohmer M, eds. Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. New York: Springer, 315–327.
Valdiani, A., Mihdzar, A.K., Tan, S.G., Talei, D., Puad, M.A. and Nikzad, S. (2012). Nain-e Havandi (Andrographis paniculata) present yesterday, absent today: A plenary review on underutilized herb of Iran’s pharmaceutical plants. Molecular Biology Reports. 39: 5409-5424.
Wang, H., Nagegowda, D.A., Rawat, R., Bouvier-Navé, P., Guo, D., Bach, T.J. and Chye, M.L. (2012). Overexpression of Brassica juncea wild-type and mutant HMG-CoA synthase 1 in Arabidopsis up-regulates genes in sterol biosynthesis and enhances sterol production and stress tolerance. Plant Biotechnology Journal. 10: 31–42
Xoca-Orozco, L.A.Â., Cuellar-Torres, E.A., GonzaÂlez-Morales, S., GutieÂrrez-MartõÂnez, P., LoÂpez-GarcõÂa, U., Herrera- Estrella, L., Vega-Arreguín, J. and Chacón-López, A. (2017). Transcriptomic analysis of avocado hass (Persea americana Mill) in the interaction system fruit-chitosan-Colletotrichum. Frontiers in Plant Science. 8: 956.
Zhao, J., Davis, L.C. and Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances. 23(4): 283–333
Zhishen, J., Mengcheng, T. and Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry. 64(4): 555-559
Zong, H., Liu, S., Xing, R., Chen, X. and Li, P. (2017). Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicology and Environmental Safety. 138: 271-278.
_||_Abdel-Mawgoud, A.M.R., Tantawy, A.S., El-Nemr, M.A. and Sassine, Y.N. (2010). Growth and yield responses of strawberry plants to chitosan application. European Journal of Scientific Research. 39(1): 161-8.
Agrawal, G., Rakwal, R., Tamogami, S., Yonekurad, M., Kubo, A. and Saji, H. (2002). Chitosan activates defense/stress response(s) in the leaves of Oryza Sativa seedlings. Plant Physiology and Biochemistry. 40: 1061-9.
Arriola, O.C., Rocha, M.C., Hernandez, A.B., Brauer, J.M.E. and Jatomea, M.P. (2013). Controlled release matrices and micro/nanoparticles of chitosan with antimicrobial potential: development of new strategies for microbial control in agriculture. Journal of the Science of Food and Agriculture. 93(7): 1525-36
Benzie, I., and Strain, J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical Biochemistry. 239: 70-76.
Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Annual Biochemistry. 72: 248-254
Cheng, X., Zhou, U. and Cui, X. (2006). Improvement of phenylethanoid glycosides biosynthesis in Cistanche deserticola cell suspension cultures by chitosan elicitor. Biotechnology Journal. 121: 253-60.
El-Tantawy E.M. (2009). Behavior of tomato plants as affected by spraying with chitosan and aminofort as natural stimulator substances under application of soil organic amendments. Pakistan Journal of Biological Sciences. 12(17): 1164-73.
Esmaeilzadeh Bahabadi, S., Sharifi, M., Safaie, N. and Behmanesh, M. (2012). Enhancement of lignan and phenylpropanoid compounds production by chitosan in Linum album cell culture. Iranian Journal of Plant Biology. 4(11): 13-26.
Fielding, J.L. and Hall, J. (1978). A biochemical and cytochemical study of peroxidase activity in root of Pisum sativam. Journal of Experimental Botany. 29: 981-989.
Gerami, M., Ghorbani, A., and Karimi, S. (2018). Role of salicylic acid pretreatment in alleviating cadmium-induced toxicity in Salvia officinalis L. Iranian Journal of Plant Biology. 10(1): 81–95.
Ghasemi-Omran, V.O., Ghorbani, A., and Sajjadi-Otaghsara, S.A. (2021). Melatonin alleviates NaCl-induced damage by regulating ionic homeostasis, antioxidant system, redox homeostasis, and expression of steviol glycosides-related biosynthetic genes in in vitro cultured Stevia rebaudiana Bertoni. In Vitro Cellular & Developmental Biology – Plant. 57: 319–331.
Ghorbani, A., Ghasemi Omran, V.O., Razavi, S.M., Pirdashti, H., and Ranjbar, M. (2019) Piriformospora indica confers salinity tolerance on tomato (Lycopersicon esculentum Mill.) through amelioration of nutrient accumulation, K+/Na+ homeostasis and water status. Plant Cell Reports 38: 1151–1163.
Ghorbani, A., Pishkar, L., Roodbari, N., Pehlivan, N., and Wu, C. (2021). Nitric oxide could allay arsenic phytotoxicity in tomato (Solanum lycopersicum L.) by modulating photosynthetic pigments, phytochelatin metabolism, molecular redox status and arsenic sequestration. Plant Physiology and Biochemistry 167: 337–348.
Ghorbani, A., Razavi, S.M., Ghasemi Omran, V.O. and Pirdashti, H. (2018a). Piriformospora indica alleviates salinity by boosting redox poise and antioxidative potential of tomato. Russian Journal of Plant Physiology. 65: 898–907.
Ghorbani, A., Razavi, S.M., Ghasemi Omran, V.O., and Pirdashti, H. (2018b). Piriformospora indica inoculation alleviates the adverse effect of NaCl stress on growth, gas exchange and chlorophyll fluorescence in tomato (Solanum lycopersicum L.). Plant Biology 20: 729–736.
Giannopolitis, C.N. and Ries, S.K. (1977). Superoxide dismutase I. Occurrences in higher plants. Plant Physiology. 59(2): 309-414.
Goulas, V., and Manganaris, G.A. (2011). The effect of postharvest ripening on strawberry bioactive composition and antioxidant potential. Journal of the Science of Food and Agriculture. 91: 1907–1914.
Harish Prashanth, K.V., Dharmesh, S.M., Jagannatha Rao, K.S. and Tharanathan, R.N. (2007). Free radical-induced chitosan depolymerized products protect calf thymus DNA from oxidative damage. Carbohydrate Research. 342: 190-5.
Hussaini Begum, M., Taheri, G.H., Vaezi Kakhaki, M.R. and Tlaty, M. (2013). Foliar application of chitosan on growth and morphological characteristics of marigold (Calendula officinalis). National Conference of passive defense in the agricultural sector. 2013 November 30.
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
Landi, L., De Miccolis Angelini, R.M., Pollastro, S., Feliziani, E., Faretra, F. and Romanazzi, G. (2017). Global transcriptome analysis and identification of differentially expressed genes in strawberry after preharvest application of Benzothiadiazole and chitosan. Frontiers in Plant Science. 8: 235.
Liao, P., Chen, X., Wang, M., Bach, T.J. and Chye, M.L. (2018). Improved fruit α-tocopherol, carotenoid, squalene and phytosterol contents through manipulation of Brassica juncea 3-HYDROXY-3-METHYLGLUTARYLCOA SYNTHASE1 in transgenic tomato. Plant Biotechnology Journal. 16: 784–796.
Liao, P., Wang, H., Wang, M., Hsiao, A.S., Bach, T.J. and Chye, M.L. (2014). Transgenic tobacco overexpressing Brassica juncea HMG-CoA synthase 1 shows increased plant growth, pod size and seed yield. PLoS One. 9: e98264
Lichtenthaler, H. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods of Enzymology. 148: 350-382.
Limpanavech, P., Chaiyasuta, S., Vongpromek, R., Pichyangkura, R., Khunwasi, C., Chadchawan, S., Lotrakul, P., Bunjongrat, R., Chaidee, A. and Bangyeekhun, T. (2008). Chitosan effects on floral production, gene expression, and anatomical changes in the Dendrobium orchid. Scientia Horticulturae. 116: 65–72
Lin, F.L., Wu, S.J., Lee, S.C. and Ng, L.T. (2009). Antioxidant, antioedema and analgesic activities of Andrographis paniculata extracts and their active constituent andrographolide. Phytotherapy Research. 23(7): 958‐964.
Liu, J., Tian, S., Meng, X. and Xu, Y. (2007). Effects of chitosan on control of postharvest diseases and physiological responses of tomato fruit. Journal of Postharvest Biology and Technology. 44: 300-306.
Marinova, D., Ribarov, F. and Atanassova, M. (2005). Total phenolics and total flavonoids in Bolgarian fruits and vegetables. Journal of the University of Chemical Technology and Metallurgy. 40: 255-260.
Martins, H.M., Martins M.L., Dias, M.I. and Bernardo, F. (2001). Evaluation of microbiological quality of medicinal plants used in natural infusions. International Journal of Food Microbiology. 58: 149-153.
Mehregan, M., Mehrafarin, A., Labbafi, M. and Naghdi Badi, H. (2017). Effect of different concentrations of chitosan biostimulant on biochemical and morphophysiological traits of stevia plant (Stevia rebaudiana Bertoni). Journal of Medicinal Plants. 16(62): 169-181
Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies. 15(4): 523-530.
Mishra, U.S., Mishra, A., Kumari, R., Murthy, P.N. and Naik, B.S. (2009). Antibacterial activity of ethanol extract of Andrographis paniculata. Indian Journal of Pharmaceutical Sciences. 71: 436‐438.
Mondal, M.A., Malek, M.A., Puteh, A.B., Ismail, M.R., Ashrafuzzaman, M. and Naher, L. (2012). Effect of foliar application of chitosan on growth and yield in okra. Australian Journal of Crop Science. 6(5): 918-921
Mukta, J.A., Rahman, M., Sabir, A.A., Gupta, D.R., Surovy, M.Z., Rahman, M. and Islama, M.T. (2017). Chitosan and plant probiotics application enhance growth and yield of strawberry. Biocatalysis and Agricultural Biotechnology. 11: 9-18.
Naderi, S., Esmaeilzadeh Bahabadi, S. and Fakheri, B. (2015). The effect of chitosan on some physiological and biochemictry characterization in basil (Ocimum basilicum). Plant Process and Function. 4(12); 29-41
Palida, S., Rath, P. and Supachitra, C. (2014). Chitosan increased phenolic compound contents in tea (Camellia sinensis) leaves by Pre- and Post-treatments. Journal of Chitin and Chitosan Science. 2(2): 93-98.
Pichynagkura, R. and Kudan, S. (2002). Quantitative production of 2-acetamido 2-deoxy-Dglucose from cryatallin chitin by bactrial Chitinase. Carbohydrate Research. 337: 1-9.
Pirbalouti, A.G., Malekpoor, F., Salimi, A., Golparvar, A. (2017). Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Scientia Horticulturae. 217: 114-122.
Portu, J., López, R., Baroja, E., Santamaría, P. and Garde-Cerdán, T. (2016). Improvement of grape and wine phenolic content by foliar application to grapevine of three different elicitors: Methyl jasmonate, chitosan, and yeast extract. Food Chemistry. 201: 213–221.
Rabea, E.I., Badawy, M.E., Stevens, C.V., Smagghe, G. and Steurbaut, W. (2003). Chitosan as antimicrobial agent: Aplications and mode of action. Biomacromolecules. 4(5): 1457-65.
Schaller, H., Grausem, B., Benveniste, P., Chye, M.L., Tan, C.T., Song, Y.H. and Chua, N.H. (1995). Expression of the Hevea brasiliensis (H.B.K.) Mull. Arg. 3-hydroxy-3-methylglutaryl-coenzyme A reductase 1 in tobacco results in sterol overproduction. Plant Physiology. 109: 761–770.
Silva, V., Singh, R.K., Gomes, N., Soares, B.G., Silva, A., Falco, V., Capita, R., Alonso-Calleja, C., Pereira, J.E., Amaral, J.S., Igrejas, G. and Poeta, P. (2020). Comparative insight upon chitosan solution and chitosan nanoparticles application on the phenolic content, antioxidant and antimicrobial activities of individual grape components of Sousão variety. Antioxidants. 9: 178.
Suwanmanee, P., Sirinupong, N. and Suvachittanont, W. (2013). Regulation of 3-hydroxy-3-methylglutaryl-CoA synthase and rubber biosynthesis of Hevea brasiliensis (B.H.K.) Mull. Arg. In: Bach TJ, Rohmer M, eds. Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. New York: Springer, 315–327.
Valdiani, A., Mihdzar, A.K., Tan, S.G., Talei, D., Puad, M.A. and Nikzad, S. (2012). Nain-e Havandi (Andrographis paniculata) present yesterday, absent today: A plenary review on underutilized herb of Iran’s pharmaceutical plants. Molecular Biology Reports. 39: 5409-5424.
Wang, H., Nagegowda, D.A., Rawat, R., Bouvier-Navé, P., Guo, D., Bach, T.J. and Chye, M.L. (2012). Overexpression of Brassica juncea wild-type and mutant HMG-CoA synthase 1 in Arabidopsis up-regulates genes in sterol biosynthesis and enhances sterol production and stress tolerance. Plant Biotechnology Journal. 10: 31–42
Xoca-Orozco, L.A.Â., Cuellar-Torres, E.A., GonzaÂlez-Morales, S., GutieÂrrez-MartõÂnez, P., LoÂpez-GarcõÂa, U., Herrera- Estrella, L., Vega-Arreguín, J. and Chacón-López, A. (2017). Transcriptomic analysis of avocado hass (Persea americana Mill) in the interaction system fruit-chitosan-Colletotrichum. Frontiers in Plant Science. 8: 956.
Zhao, J., Davis, L.C. and Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances. 23(4): 283–333
Zhishen, J., Mengcheng, T. and Jianming, W. (1999). The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chemistry. 64(4): 555-559
Zong, H., Liu, S., Xing, R., Chen, X. and Li, P. (2017). Protective effect of chitosan on photosynthesis and antioxidative defense system in edible rape (Brassica rapa L.) in the presence of cadmium. Ecotoxicology and Environmental Safety. 138: 271-278.
