Alleviation of allelochemical stress-induced growth inhibition and oxidative damage in lettuce under closed hydroponics through electro-degradation M.R., Asaduzzaman M., Ueno M., Tanaka H., Asao T. (2020): Alleviation of allelochemical stress-induced growth inhibition and oxidative damage in lettuce under closed hydroponics through electro-degradation. Hort. Sci. (Prague), 47: 53-68.
download PDF

Successive lettuce cultivation in closed hydroponics using the same nutrient solution causes the excess production and accumulation of allelochemicals. The accumulated allelochemicals induce oxidative damage and lipid peroxidation in plants leading to growth inhibition. In this study, we investigated the allelochemicals that induced oxidative damage and lipid peroxidation in lettuce grown in a once used non-renewed nutrient solution (1NR) and a twice used non-renewed nutrient solution (2NR) obtained from the successive cultivation and the alleviation of these damages through electro-degradation (ED). The 1NR solution was used for six weeks for a one-time lettuce cultivation while the 2NR solution was used for twelve weeks for a two-times lettuce cultivation. The results showed that the allelochemical stress caused growth inhibition in the lettuce in both the 1NR and 2NR solutions. It was observed that there was a higher generation of H2O2 and O2.– as well as a lower activity of the antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase (POD), and ascorbate peroxidase (APX) in the roots of the plants grown in both the 1NR and 2NR solutions compared to plants grown in the new nutrient solution. The higher level of lipid peroxidation due to the higher MDA (malondialdehyde) content and higher soluble protein content were also observed in the roots of those plants. It was evident that lettuce root damage occurred due to accumulation of the allelochemicals in the 1NR and 2NR solutions. These damaged roots could not function normally nor uptake water and minerals from the culture solution. As a result, retarded lettuce growth was observed in the 1NR and 2NR solutions. The oxidative damage, soluble protein content, lipid peroxidation and ultimately growth retardation were more pronounced in the plants grown in the 2NR solution compared to the plants grown in the 1NR solution. The application of ED to the 1NR and 2NR solutions maintained the plant growth through less oxidative damage, soluble protein production and lipid peroxidation as was observed in the plants grown with the new nutrient solution. Therefore, the ED of a non-renewed culture solution would alleviate the allelochemical stress in lettuce under recycled hydroponics.

Abenavoli M.R., Cacco G., Sorgona A., Marabottini R., Paolacci A.R., Ciaffi M., Badiani M. (2006): The inhibitory effects of coumarin on the germination of durum wheat (Triticum turgidum ssp. durum, cv. Simeto) seeds. Journal of Chemical Ecology, 32: 489–506.
Ahmed I.M., Cao F., Zhang M., Chen X., Zhang G., Wu F. (2013): Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLOS ONE, 8: e77869.
Apel K., Hirt H. (2004): Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55: 373–399.
Asaduzzaman M., Kobayashi Y., Isogami K., Tokura M., Tokumasa K., Asao T. (2012): Growth and yield recovery in strawberry plants under autotoxicity through electro-degradation. European Journal of Horticultural Science, 77: 58–67.
Asao T., Kitazawa H., Ban T., Pramanik M.H.R. (2004b): Search of autotoxic substances in some leaf vegetables. Journal of the Japanese Society for Horticultural Science, 73: 247–249.
Asao T., Kitazawa H., Ban T., Pramanik M.H.R. (2008): Electro-degradation of root exudates to mitigate autotoxicity in hydroponically grown strawberry (Fragaria × ananassa Duch.) plants. HortScience, 43: 2034–2038.
Asao T., Kitazawa H., Tomita K., Suyama K., Yamamoto H., Hosoki T., Pramanik M.H.R. (2004a): Mitigation of cucumber autotoxicity in hydroponic culture using microbial strain. Scientia Horticulturae, 99: 207–214.
Asao T., Kitazawa H., Ushio K., Sueda Y., Ban T., Pramanik M.H.R. (2007): Autotoxicity in some ornamentals with means to overcome it. HortScience, 42: 1346–1350.
Asao T., Umeyama M., Ohta K., Hosoki T., Ito T., Ueda H. (1998): Decrease of yield of cucumber by non-renewal of the nutrient hydroponic solution and its reversal by supplementation of activated charcoal. Journal of the Japanese Society for Horticultural Science, 67: 99–105. (in Japanese with English summary).
Ashraf M., Harris P. (2004): Potential biochemical indicators of salinity tolerance in plants. Plant Science, 166: 3–16.
Bais H.P., Vepachedu R., Gilroy S., Callaway R.M., Vivanco J.M. (2003): Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science, 301: 1377–1380.
Barkosky R.R., Einhellig F.A. (1993): Effects of salicylic acid on plant-water relationships. Journal of Chemical Ecology, 19: 237–247.
Batish D.R., Singh H.P., Setia N., Kaur S., Kohli R.K. (2006): 2-Benzoxazolinone (BOA) induced oxidative stress, lipid peroxidation and changes in some antioxidant enzyme activities in mung bean (Phaseolus aureus). Plant Physiology and Biochemistry, 44: 819–827.
Baziramakenga R., Leroux G.D., Simard R.R. (1995): Effects of benzoic and cinnamic acids on membrane permeability of soybean roots. Journal of Chemical Ecology, 21: 1271–1285.
Baziramakenga R., Simard R.R., Leroux G.D. (1994): Effects of benzoic and cinnamic acids on growth, mineral composition and chlorophyll content of soybean roots. Journal of Chemical Ecology, 20: 2821–2833.
Bertin C., Yang X.H., Weston L.A. (2003): The role of root exudates and allelochemicals in the rhizosphere. Plant and Soil, 256: 67–83.
Bertoldi F.C., Sant’Anna E., Barcelos-Oliveira J.L. (2009): Chlorella vulgaris cultivated in hydroponic wastewater. In: Rodriguez-Delfin A., Martinez P.F. (eds): Proceedings of IS on Soilless Culture and Hydroponics. Acta Horticuturae (ISHS), 843: 373–380.
Blum U. (2005): Relationships between phenolic acid concentrations, transpiration, water utilization, leaf area expansion, and uptake of phenolic acids: nutrient culture studies. Journal of Chemical Ecology, 31: 1907–1932.
Blum U., Shafer R., Lehmen M.E. (1999): Evidence for inhibitory allelopathic interactions including phenolic acids in field soils: Concept vs. an experimental model. Critical Reviews in Plant Sciences, 18: 673–693.
Böhm P.A.F., Zanado F.M.L., Ferrarese M.L.L., Ferrarese-Filho O. (2006): Peroxidase activity and lignification in soybean root growth-inhibition by juglone. Biologia Plantarum, 50: 315–317.
Bradford M.M. (1976): A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248–254.
Chi W.C., Fu S.F., Huang T.L., Chen Y.A., Chen C.C., Huang H.J. (2011): Identification of transcriptome profiles and signaling pathways for the allelochemical juglone in rice roots. Plant Molecular Biology, 77: 591–607.
Cruz-Ortega R., Ayala-Cordero G., Anaya A.L. (2002): Allelochemical stress produced by the aqueous leachate of Callicarpa acuminata: Effects on roots of bean, maize, and tomato. Physiologia Plantarum, 116: 20–27.
Cruz-Ortega R., Lara-Núñez A., Anaya A.L. (2007): Allelochemical stress can trigger oxidative damage in receptor plants. Plant Signaling & Behavior, 2: 269–270.
Ding J., Sun Y., Xiao C.L., Shi K., Zhou Y.H., Yu J.Q. (2007): Physiological basis of different allelopathic reactions of cucumber and fig leaf gourd plants to cinnamic acid. Journal of Experimental Botany, 58: 3765–3773.
Doblinski P.M.F., Ferrarese M.L.L., Huber D.A., Scapim C.A., Braccini A.L., Ferrarese F.O. (2003): Peroxidase and lipid peroxidation of soybean roots in response to p-coumaric and p-hydroxybenzoic acids. Brazilian Archives of Biology and Technology, 46: 193–198.
Dorning M., Cipollini D. (2006): Leaf and root extracts of the invasive shrub Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecology, 184: 287–296.
Foreman J., Demidchik V., Bothwell J.H., Mylona P., Miedema H., Torres M.A., Linstead P., Costa S., Brownlee C., Jones J.D., Davies J.M., Dolan L. (2003): Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422: 442–446.
Foyer C., Fletcher J. (2001): Plant antioxidants: colour me healthy. Biologist (London), 48: 115–120.
Gniazdowska A., Bogatek R. (2005): Allelopathic interaction between plants. Multi-site action of allelochemicals. Acta Physiologiae Plantarum, 27: 395–408.
Gossett D.R., Millhollon E.P., Lucas M.(1994): Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Science, 34: 706–714.
Halliwell B. (2006): Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology, 141: 312–322.
Holappa L.D., Blum U. (1991): Effects of exogenously applied ferulic acid, a potential allelopathic compound, on leaf growth, water utilization, and endogenous abscisic acid levels of tomato, cucumber, and beans. Journal of Chemical Ecology, 17: 865–886.
Hong Y., Hu H.Y., Xie X., Li F.M. (2008): Responses of enzymatic antioxidants and non-enzymatic antioxidants in the cyanobacterium Microcystis aeruginosa to the allelochemical ethyl 2-methyl acetoacetate (EMA) isolated from reed (Phragmites communis). Journal of Plant Physiology, 165: 1264–1273.
Hori Y. (1966): Gravel culture of vegetables and ornamentals. 3. Nutrient solution. Yokendo, Tokyo, Japan: 69–80. (in Japanese).
Inderjit (1996): Plant phenolics in allelopathy. The Botanical Review, 62: 186–202.
Inderjit, Duke S.O. (2003): Ecophysiological aspect of allelopathy. Planta, 217: 529–539.
Inderjit, Weston L.A. (2003): Root exudates: an overview. In: de Kroon H., Visser E.J.W. (eds): Root ecology. Ecological Studies (Analysis and Synthesis), Vol. 168, Springer, Verlag Berlin, Heidelberg, New York: 235–255.
Jiang M., Zhang J. (2002): Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. Journal of Experimental Botany, 53: 2401–2410.
Kitazawa H., Asao T., Ban T., Pramanik M.H.R., Hosoki T. (2005): Autotoxicity of root exudates from strawberry in hydroponic culture. The Journal of Horticultural Science and Biotechnology, 80: 677–680.
Lara-Núñez A., Romero-Romero T., Ventura J.L., Blancas V., Anaya A.L., Cruz-Ortega R. (2006): Allelochemical stress causes inhibition of growth and oxidative damage in Lycopersicon esculentum Mill. Plant, Cell & Environment, 29: 2009–2016.
Lee J.G., Lee B.Y., Lee H.J. (2006): Accumulation of phytotoxic organic acids in reused nutrient solution during hydroponic cultivation of lettuce (Lactuca sativa L.). Scientia Horticulturae, 110: 119–128.
Li F.M., Hu H.Y. (2005): Isolation and characterization of a novel anti algal allelochemical from Phragmites communis. Applied and Environmental Microbiology, 71: 6545–6553.
Lin W.X., Kim K.U., Sgub D.G. (2000): Rice allelopathic potential and its modes of action on barnyardgrass (Echinochloa crusgalli). Allelopathy Journal, 7: 215–224.
Lyu S.W., Blum U. (1990): Effects of ferulic acid, an allelopathic compound, on net P, K, and water uptake by cucumber seedlings in a split-root system. Journal of Chemical Ecology, 16: 2429–2439.
Mersie W., Singh M. (1993): Phenolic acids affect photosynthesis and protein synthesis by isolated leaf cells of velvet leaf. Journal of Chemical Ecology, 19: 1293–1301.
Mittler R. (2002): Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7: 405–410.
Mondal F.M., Asaduzzaman M., Kobayashi Y., Ban T., Asao T. (2013): Recovery from autotoxicity in strawberry by supplementation of amino acids. Scientia Horticulturae, 164: 137–144.
Mylona P.V., Polidoros A.N., Scandalios J.G. (2007): Antioxidant gene responses to ROS-generating xenobiotics in developing and germinated scutella of maize. Journal of Experimental Botany, 58: 1301–1312.
Nakano Y., Asada K. (1981): Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology, 22: 867–880.
Oracz K., Bailly C., Gniazdowska A., Come D., Corbineau F., Bogatek R. (2007): Induction of oxidative stress by sunflower phytotoxins in germinating mustard seeds. Jounal of Chemical Ecology, 33: 251–264.
Ozkur O., Ozdemir F., Bor M., Turkan I. (2009): Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovata Desf. to drought. Environmental and Experimental Botany, 66: 487–492.
Penuelas J., Ribas-Carbo M., Giles L. (1996): Effects of allelochemicals on plant respiration and oxygen isotope fractionation by the alternative oxyldase. Journal of Chemical Ecology, 22: 801–805.
Politycka B. (1996): Peroxidase activity and lipid peroxidation in roots of cucumber seedlings influenced by derivatives of cinnamic and benzoic acids. Acta Physiologiae Plantarum, 18: 365–370.
Qian H., Xu X., Chen W., Jiang H., Jin Y., Liu W., Fu Z. (2009): Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Clorella vulgaris. Chemosphere, 75: 368–375.
Rhoads D.M., Umbach A.L., Subbaiah C.C., Siedow J.N. (2006): Mitochondrial reactive oxygen species: contribution to oxidative stress and inter organellar signaling. Plant Physiology, 141: 357–366.
Rohn S., Rawel H.M., Kroll J. (2002): Inhibitory effects of plant phenols on the activity of selected enzymes. Journal of Agricultural and Food Chemistry, 50: 3566–3571.
Romero-Romero T., Sánchez-Nieto S., San Juan-Badillo A., Anaya A.L. (2005): Comparative effects of allelochemical and water stress in roots of Lycopersicon esculentum Mill. (Solanaceae). Plant Science, 168: 1059–1066.
Russel D.F. (1986): M-STAT Director. Crop and Soil Science Department, Michigan, State University, U.S.A.
Sánchez-Moreiras A.M., Reigosa M.J. (2005): Whole plant response of lettuce after root exposure to BOA (2(3H)-Benzoxazolinone). Journal of Chemical Ecology, 31: 2689–2703.
Scandalios J. (2005): Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research, 38: 995–1014.
Singh H.P., Batish D.R., Kaur S., Arora K., Kohli R.K. (2006): α-Pinene inhibits growth and induces oxidative stress in roots. Annals of Botany, 98: 1261–1269.
Singh H.P., Batish D.R., Kohli R.K. (1999): Autotoxicity: concept, organisms and ecological significance. Critical Reviews in Plant Sciences, 18: 757–772.
Singh N.K., Bracker C.A., Hasegawa P.M., Handa A.K., Buckel S., Hermodson M.A. (1987): Characterization of osmotin: a thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiology, 85: 529–536.
Talukder M.R., Asaduzzaman M., Tanaka H., Asao T. (2018): Light-emitting diodes and exogenous amino acids application improve growth and yield of strawberry plants cultivated in recycled hydroponics. Scientia Horticulturae, 239: 93–103.
Talukder M.R., Asaduzzaman M., Tanaka H., Asao T. (2019a): Electro-degradation of culture solution improves growth, yield and quality of strawberry plants grown in closed hydroponics. Scientia Horticulturae, 243: 243–251.
Talukder M.R., Asaduzzaman M., Tanaka H., Asao T. (2019b): Application of alternating current electro-degradation improves retarded growth and quality in lettuce under autotoxicity in successive cultivation. Scientia Horticulturae, 252: 324–331.
Tang C.S., Young C.C. (1982): Collection and identification of allelopathic compounds from the undisturbed root system of bitaltalimpograss (Helmarthria altissima). Plant Physiology, 69: 155–160.
Weir T.L., Park S.W., Vivanco J.M. (2004): Biochemical and physiological mechanisms mediated by allelochemicals. Current Opinion in Plant Biology, 7: 472–479.
Willekens H., Chamnongpol S., Davey M., Schraudner M., Langebartels C., Van Montagu M., Inze D., Van Camp W. (1997): Catalase is a sink for H2O2 and is indispensable for stress defense in C3 plants. The EMBO Journal, 16: 4806–4816.
Willekens H., Inzé D., Van Montagu M., Van Camp W. (1995): Catalases in plants. Molecular Breeding, 1: 207–228.
Wu F.B., Zhang G.P., Dominy P. (2003): Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity. Environmental and Experimental Botany, 50: 67–78.
Yamamoto Y., Kobayashi Y., Devi S.R., Rikiishi S., Matsumono H. (2003): Oxidative stress triggered by aluminum in plant roots. Plant and Soil, 255: 239–243.
Yan X., You-Gen W., Ying C., Jun-Feng Z., Xi-Qiang S., Guo-Peng Z., Xin-Wen H. (2015): Autotoxicity in Pogostemon cablin and their allelochemicals. Revista Brasileira de Farmacognosia, 25: 117–123.
Yang F., Xu X., Xiao X., Li C. (2009): Responses to drought stress in two poplar species originating from different altitudes. Biologia Plantarum, 53: 511–516.
Ye S.F., Yu J.Q., Peng Y.H., Zheng J.H., Zou L.Y. (2004): Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant and Soil, 263: 143–150.
Ye S.F., Zhou Y.H., Sun Y., Zou L.Y., Yu J.Q. (2006): Cinnamic acid causes oxidative stress in cucumber roots and promotes incidence of Fusarium wilt. Environmental and Experimental Botany, 56: 255–262.
Yu J.Q., Matsui Y. (1993): Extraction and identification of phytotoxic substances accumulated in nutrient solution for the hydroponic culture of tomato. Soil Science and Plant Nutrition, 39: 691–700.
Yu J.Q., Matsui Y. (1994): Phytotoxic substances in root exudates of cucumber (Cucumis sativus L). Journal of Chemical Ecology, 20: 21–31.
Yu J.Q., Ye S.F., Zhang M.F., Hu W.H. (2003): Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochemical Systematics and Ecology, 31: 129–139.
Zeng F., Wu X., Qiu B., Wu F., Jiang L., Zhang G. (2014): Physiological and proteomic alterations in rice (Oryza sativa L.) seedlings under hexavalent chromium stress. Planta, 240: 291–308.
Zeng R.S., Luo S.M., Shi Y.H., Shi M.B., Tu C.Y. (2001): Physiological and biochemical mechanism of allelopathy of secalonic acid F on higher plants. Agronomy Journal, 93: 72–79.
Zhang S., Zhang B., Dai W., Zhang X. (2011): Oxidative damage and antioxidant responses in Microcystis aeruginosa exposed to the allelochemical berberine isolated from golden thread. Journal of Plant Physiology, 168: 639–643.
Zhang X.Z. (1992): The measurement and mechanism of lipid peroxidation and SOD, POD and CAT activities in biological system. In: Zhang, X.Z. (ed.), Research methodology of crop physiology. Agriculture Press, Beijing: 208–211.
download PDF

© 2020 Czech Academy of Agricultural Sciences