Issue
Effect of drought stress on physiological traits and antioxidant activities in some olive cultivars
Corresponding Author(s) : Omid Sofalian
Cellular and Molecular Biology,
Vol. 65 No. 7: Issue 7
Abstract
Drought is important abiotic stress that negatively influences the growth and development of plants. Strong efforts are currently ongoing worldwide to improve olive production under adverse environmental conditions by extending genetic diversity to improve key agro-physiological and biochemical features through various breeding programs. This research was performed to evaluate the effect of drought stress on the changes of some physiological and biochemical traits in 20 commercial and promising olive genotypes under field conditions during 2015-2017. Fruit oil content as well as some of physiological traits and antioxidant activities under control and drought stress conditions were evaluated. The results of combined analysis of variance (ANOVA) for fruit yield and other measured traits showed that year, irrigation treatments, genotype main effects and their interactions were highly significant. In general, fruit yield, relative water content (RWC), oil content and total soluble proteins (TPs) showed a decreasing trend, whereas the electrolyte leakage, H2O2 content and activity of catalase (CAT), ascorbate peroxidase (APX) and peroxidase (POX) displayed an increasing trend in the tested olive genotypes during drought stress. A Principal component analysis (PCA)-based biplot demonstrated that stress tolerance index (STI) positively correlated with POX and TPs. Results also revealed a high level of genetic diversity in the tested olive genotypes, and among them, two commercial (Abou-satl) and promising genotypes (T2) responded better to drought by marinating a good balance for fruit yield and some of the antioxidant activities. These genotypes could be used in future programs to develop new olive cultivars with beneficial stress-adaptive traits.
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- Ben Ahmed CB, Rouina BB, Sensoy S, Boukhris M, Abdallah FB. Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exper Bot 2009; 67:345-352.
- Faostat. Food and Agriculture Organization, FAOSTAT Database 2017; Available at: http://www.fao.org/faostat/en/#data/QC, Access in:2017.
- Guerfel M, Boujnah D, Baccouri B, Zarrouk M. Evaluation of morphological and physiological traits for drought tolerance in 12 Tunisian olive varieties (Olea europaea L.). Int J Agron 2007; 6:356–361.
- Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM. Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 2006; 170:596–605.
- Fernandez J.E, Moreno F, Giron I.F, Blazquez O.M. Stomatal control of water use in olive tree leaves. Plant Soil 1997; 190:179–192.
- Chartzoulakis K, Patakas A, Bosabalidis AM. Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. Environ Exper Bot 1999; 42:113–120.
- Dichio B, Xiloyannis C, Sofo A, Montanaro G. Osmotic regulation in leaves and roots of olive trees during a water deficit and rewatering. Tree Physiol Victoria 2006; 26:179–185.
- Sofo A, Manfreda S, Dichio B, Fiorentino M, Xiloyannis C. The olive tree: a paradigm for drought tolerance in Mediterranean climates. Hydrol Earth Syst Sc Göttingen 2007; 4:2811–2835.
- Bosabalidis A.M, Kofidis G. Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci Amsterdam 2002; 163:375–379.
- Trentacoste ER, Zanessi O.C, Marshall VB, Puertas CM. Genotypic variation of physiological and morphological traits of seven olive cultivars under sustained and cyclic drought in Mendoza, Argentina. Agri Water Manag Amsterdam 2018; 196:48–56.
- Enamel M, Tounekti T, Vadel AM, Khemira H, Cochard H. Water relations and drought-induced embolism in olive (Olea europaea) varieties Meski and Chemlali during severe drought. Tree Physiol Victoria 2008; 28:971–976.
- Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique KHM. Wild relatives of wheat: Aegilops–Triticum accessions disclose differential antioxidative and physiological responses to water stress. Acta Physiol Plant 2018a; 40:90-101.
- Hossain MS, Elsayad AI, Moore M, Dietz KJ. Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet. J Exp Bot Oxford 2017; 68:1283–1298.
- Yadav SK. Cold stress tolerance mechanisms in plants. A review Agron Sustain Dev Berlin 2010; 30:515–527.
- Verma KK, Singh M, Gupta RK, Verma CL. Photosynthetic gas exchange, chlorophyll fluorescence, antioxidant enzymes, and growth responses of Jatropha curcas during soil flooding. Turkish JPN J BOT Ankara. 2014; 38:130–140.
- Petridis A, Therios L, Samouris G, Koundouras S, Giannakouls A. Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olives (Olea europaea L.) cultivars. Plant. Physiol Biochem. Amsterdam 2012; 60:1–11.
- Ben Abdallah M, Methenni K, Nouairi I, Youssef N.B. Drought priming improves subsequent more severe drought in a drought-sensitive cultivar of olive cv. Chétoui. Sci Hort Amsterdam 2017; 221:43–52.
- Gholami R, Sarikhani H, Arji I. Effects of Deficit Irrigation on some physiological and biochemical characteristics of six commercial olive cultivars in field conditions. Iranian J Hort Sci Technol 2016; 17:39-52.
- Smart RE, Bingham GE. Rapid estimates of relative water content. Plant Physiol Monona 1974; 53:258–260.
- Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem Amsterdam 1976; 72:248–254.
- Beauchamp C, Fridovich J. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem Amsterdam 1971; 44:276–287.
- Sergiev L, Alexieva E, Karanov E. Effect of spermine, atrazine and combination between them on some endogenous protective systems and markers in plants. Comptes rendus de l'Académie bulgare des Sciences, Sofia 1997; 51:121–124.
- Beers PF, Sizer IW. A spectrophotometric assay measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem Maryland 1952; 195:133–138.
- Chance B, Maehly SK. Assay of catalase and peroxidase. Methods in Enzymology, Amsterdam 1955; 2:764–775.
- Nakano Y, Asada K. Spinach chloroplasts scavenge hydrogen peroxide on illumination. Plant. Cell Physiol Oxford 1980; 21:1295–1307.
- I.O.O.C. Methodology for the secondary characterization (agronomic, phonological, pomological and oil quality) of olive varieties held in collection. Project on conservation, characterization, collection of Genetic Resources in olive 2002.
- Fernandez GCJ. Effective selection criteria for assessing plant stress tolerance. In: Kuo CG (ed) Adaptation of food crops to temperature and water stress. Shanhua, Taiwan 1993; 257–270.
- Pour"Aboughadareh A, Yousefian M, Moradkhani H, Moghaddam Vahed M, Poczai P, Siddique KHM. iPASTIC: An online toolkit to estimate plant abiotic stress indices. Appl Plant Sci 2019; 7:e11278.
- Pour-Aboughadareh A, Ahmadi J, Mehrabi A.A, Moghaddam M, Etminan A. Physiological responses to drought stress in wild relatives of wheat: implications for wheat improvement. Acta Physiol Plant Krakow 2017; 39:106.
- Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique, KHM. Screening wild progenitors of wheat for salinity stress at early stages of plant growth: Insight into potential sources of variability for salinity adaptation in wheat. Crop Pasture Sci 2018c; 69:649–458.
- Suneja Y, Gupta AK, Bains NS. Bread wheat progenitors: Aegilops tauschii (DD genome) and Triticum dicoccoides (AABB genome) reveal differential antioxidative response under water stress. Physiol Mol Biol Pla Berlin 2017; 23:99–114.
- Silva M, Jifon J, Silva JAG, Sharma V Use of physiological parameters as fast tools to screen for drought tolerance in sugarcane. Braz J Plant Physiol 2007; 19:193–201.
- Ahumada-Orellana LE, Ortega-Farías S, Searles PS, Retamales JB. Yield and water productivity responses to irrigation cut-off strategies after fruit set using stem water potential thresholds in a super-high density olive orchard. Front Plant Sci Lausanne 2017; 8:1280–1306.
- Moriana A, Pérez-López D, Prieto M.H, Ramírez-Santa-Pau M, Pérezrodriguez JM. Midday stem water potential as a useful tool for estimating irrigation requirements in olive trees. Agri Water Manag Amsterdam 2012; 112:43–54.
- Ghrab M, Gargouri K, Bentaher H, Chartzoulakis K, Ayadi M, Ben Mimoun M, Masmoudid MM, Mechlia NB, Psarras G. Water relations and yield of olive tree (cv. Chemlali) in response to partial root-zone drying (PRD) irrigation technique and salinity under arid climate. Agri Water Manag Amsterdam 2013; 123:1–11.
- Naghavi MR, Pour-Aboughadareh A, Khalili M. Evaluation of drought tolerance indices for screening some of corn (Zea mays L.) cultivars under environmental conditions. Notulae Scientia Biologicae, Cluj-Napoca 2013; 5:388-393.
- Khalili M, Pour-Aboughadareh AR, Naghavi MR, Mohammad Amini E. Evaluation of drought tolerance in safflower genotypes based on drought tolerance indices. Not Bot Horti Agrobo 2014; 42:214–218.
- Pour-Siahbidi MM, Pour-Aboughadareh A. Evaluation of grain yield and repeatability of drought tolerance indices for screening chickpea (Cicer aritinum L.) genotypes under rainfed conditions. Iranian J Gen Plant Breed 2015; 2:28-37.
- Khalili M, Pour-Aboughadareh A, Naghavi MR. Assessment of drought tolerance in barley: integrated selection criterion and drought tolerance indices. Environ Exp Bot, Latvia 2016; 14:33–41.
- Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique, KHM. Screening wheat germplasm for seedling root architectural traits under contrasting water regimes: potential sources of variability for drought adaptation. Arch Agron Soil Sci 2018; 64:1351–1365.
- Etminan A, Pour-Aboughadareh A, Mohammadi R, Shoshtari L, Yousefiazarkhanian M, Moradkhani H. Determining the best drought tolerance indices using artificial neural network (ANN): Insight into application of intelligent agriculture in agronomy and plant breeding. Cereal Res Commun 2019; 47:170–181.
- Breton C, Souyris I, Villemur P, Berville A. Oil accumulation kinetic along ripening in four olive cultivars varying for fruit size. Fundamental, Nakajima 2009; 16:58–64.
- Motilva M.J, Romero M, Alegre S, Girona J. Influence of regulated deficit irrigation strategies applied to olive trees (Arbequina cultivar) on oil yield and oil composition during the fruit ripening period. J Sci Food Agr. New Jersey 2008; 80:2037-43.
- Brescia MA, Pugliese T, Hardy E, Sacco A. Compositional and structural investigations of ripening of table olives, Bella della Daunia, by means of traditional and magnetic resonance imaging analyses. Food Chem Amsterdam 2007; 105:400-404.
- Seymour GB, Manning K, Poole M, King GJ. The genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol Amsterdam 2008; 11:58-63.
- Xu ZZ, Zhou G.S, Wang YL, Han G.X, Li YJ. Changes in chlorophyll fluorescence in maize plants with imposed rapid dehydration at different leaf ages. J Plant Growth Regul Berlin 2008; 27:83–92.
- Ahmadipour S, Arji I, Ebadi A, Abdossi V. Physiological and biochemical response of some olive cultivars (Olea europaea L.) to water stress. Cell Mol Biol 2018; 64:20-29.
- Yan W, Zhang XZ, Shi PL, Yang ZL, He YT, Xu LL. Carbon dioxide exchange and water use efficiency of alpine meadow ecosystems on the Tibetan Plateau. J Natural Resources 2006; 21:756-767.
- Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. Jpn J Bot London 2012; 217037:1–26.
- Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer C.H. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration. Ann Botany Oxford 2002; 89:841–850.
- Jiménez A, Gómez JM, Navarro E, Sevilla F. Changes in the antioxidative systems in mitochondria during ripening of pepper fruits. Plant Physiol Biochem Amsterdam 2002; 40:515–520.
- Cansev A, Gulen H, Eris A. The activities of catalase and ascorbate peroxidase in olive (Olea europaea L. cv. Gemlik) under low temperature stress. Hortic Environ Biote Jeollabuk-do 2011; 52:113-120.
- Hashempour A, Ghasemnezhad M, Ghazvini R, Sohani MM. Olive (Olea europaea L.) freezing tolerance related to antioxidant enzymes activity during cold acclimation and non-acclimation. Acta Physiol Plant 2014; 36:3231–3241.
References
Ben Ahmed CB, Rouina BB, Sensoy S, Boukhris M, Abdallah FB. Changes in gas exchange, proline accumulation and antioxidative enzyme activities in three olive cultivars under contrasting water availability regimes. Environ Exper Bot 2009; 67:345-352.
Faostat. Food and Agriculture Organization, FAOSTAT Database 2017; Available at: http://www.fao.org/faostat/en/#data/QC, Access in:2017.
Guerfel M, Boujnah D, Baccouri B, Zarrouk M. Evaluation of morphological and physiological traits for drought tolerance in 12 Tunisian olive varieties (Olea europaea L.). Int J Agron 2007; 6:356–361.
Bacelar EA, Santos DL, Moutinho-Pereira JM, Gonçalves BC, Ferreira HF, Correia CM. Immediate responses and adaptative strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci 2006; 170:596–605.
Fernandez J.E, Moreno F, Giron I.F, Blazquez O.M. Stomatal control of water use in olive tree leaves. Plant Soil 1997; 190:179–192.
Chartzoulakis K, Patakas A, Bosabalidis AM. Changes in water relations, photosynthesis and leaf anatomy induced by intermittent drought in two olive cultivars. Environ Exper Bot 1999; 42:113–120.
Dichio B, Xiloyannis C, Sofo A, Montanaro G. Osmotic regulation in leaves and roots of olive trees during a water deficit and rewatering. Tree Physiol Victoria 2006; 26:179–185.
Sofo A, Manfreda S, Dichio B, Fiorentino M, Xiloyannis C. The olive tree: a paradigm for drought tolerance in Mediterranean climates. Hydrol Earth Syst Sc Göttingen 2007; 4:2811–2835.
Bosabalidis A.M, Kofidis G. Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci Amsterdam 2002; 163:375–379.
Trentacoste ER, Zanessi O.C, Marshall VB, Puertas CM. Genotypic variation of physiological and morphological traits of seven olive cultivars under sustained and cyclic drought in Mendoza, Argentina. Agri Water Manag Amsterdam 2018; 196:48–56.
Enamel M, Tounekti T, Vadel AM, Khemira H, Cochard H. Water relations and drought-induced embolism in olive (Olea europaea) varieties Meski and Chemlali during severe drought. Tree Physiol Victoria 2008; 28:971–976.
Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique KHM. Wild relatives of wheat: Aegilops–Triticum accessions disclose differential antioxidative and physiological responses to water stress. Acta Physiol Plant 2018a; 40:90-101.
Hossain MS, Elsayad AI, Moore M, Dietz KJ. Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet. J Exp Bot Oxford 2017; 68:1283–1298.
Yadav SK. Cold stress tolerance mechanisms in plants. A review Agron Sustain Dev Berlin 2010; 30:515–527.
Verma KK, Singh M, Gupta RK, Verma CL. Photosynthetic gas exchange, chlorophyll fluorescence, antioxidant enzymes, and growth responses of Jatropha curcas during soil flooding. Turkish JPN J BOT Ankara. 2014; 38:130–140.
Petridis A, Therios L, Samouris G, Koundouras S, Giannakouls A. Effect of water deficit on leaf phenolic composition, gas exchange, oxidative damage and antioxidant activity of four Greek olives (Olea europaea L.) cultivars. Plant. Physiol Biochem. Amsterdam 2012; 60:1–11.
Ben Abdallah M, Methenni K, Nouairi I, Youssef N.B. Drought priming improves subsequent more severe drought in a drought-sensitive cultivar of olive cv. Chétoui. Sci Hort Amsterdam 2017; 221:43–52.
Gholami R, Sarikhani H, Arji I. Effects of Deficit Irrigation on some physiological and biochemical characteristics of six commercial olive cultivars in field conditions. Iranian J Hort Sci Technol 2016; 17:39-52.
Smart RE, Bingham GE. Rapid estimates of relative water content. Plant Physiol Monona 1974; 53:258–260.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem Amsterdam 1976; 72:248–254.
Beauchamp C, Fridovich J. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem Amsterdam 1971; 44:276–287.
Sergiev L, Alexieva E, Karanov E. Effect of spermine, atrazine and combination between them on some endogenous protective systems and markers in plants. Comptes rendus de l'Académie bulgare des Sciences, Sofia 1997; 51:121–124.
Beers PF, Sizer IW. A spectrophotometric assay measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem Maryland 1952; 195:133–138.
Chance B, Maehly SK. Assay of catalase and peroxidase. Methods in Enzymology, Amsterdam 1955; 2:764–775.
Nakano Y, Asada K. Spinach chloroplasts scavenge hydrogen peroxide on illumination. Plant. Cell Physiol Oxford 1980; 21:1295–1307.
I.O.O.C. Methodology for the secondary characterization (agronomic, phonological, pomological and oil quality) of olive varieties held in collection. Project on conservation, characterization, collection of Genetic Resources in olive 2002.
Fernandez GCJ. Effective selection criteria for assessing plant stress tolerance. In: Kuo CG (ed) Adaptation of food crops to temperature and water stress. Shanhua, Taiwan 1993; 257–270.
Pour"Aboughadareh A, Yousefian M, Moradkhani H, Moghaddam Vahed M, Poczai P, Siddique KHM. iPASTIC: An online toolkit to estimate plant abiotic stress indices. Appl Plant Sci 2019; 7:e11278.
Pour-Aboughadareh A, Ahmadi J, Mehrabi A.A, Moghaddam M, Etminan A. Physiological responses to drought stress in wild relatives of wheat: implications for wheat improvement. Acta Physiol Plant Krakow 2017; 39:106.
Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique, KHM. Screening wild progenitors of wheat for salinity stress at early stages of plant growth: Insight into potential sources of variability for salinity adaptation in wheat. Crop Pasture Sci 2018c; 69:649–458.
Suneja Y, Gupta AK, Bains NS. Bread wheat progenitors: Aegilops tauschii (DD genome) and Triticum dicoccoides (AABB genome) reveal differential antioxidative response under water stress. Physiol Mol Biol Pla Berlin 2017; 23:99–114.
Silva M, Jifon J, Silva JAG, Sharma V Use of physiological parameters as fast tools to screen for drought tolerance in sugarcane. Braz J Plant Physiol 2007; 19:193–201.
Ahumada-Orellana LE, Ortega-Farías S, Searles PS, Retamales JB. Yield and water productivity responses to irrigation cut-off strategies after fruit set using stem water potential thresholds in a super-high density olive orchard. Front Plant Sci Lausanne 2017; 8:1280–1306.
Moriana A, Pérez-López D, Prieto M.H, Ramírez-Santa-Pau M, Pérezrodriguez JM. Midday stem water potential as a useful tool for estimating irrigation requirements in olive trees. Agri Water Manag Amsterdam 2012; 112:43–54.
Ghrab M, Gargouri K, Bentaher H, Chartzoulakis K, Ayadi M, Ben Mimoun M, Masmoudid MM, Mechlia NB, Psarras G. Water relations and yield of olive tree (cv. Chemlali) in response to partial root-zone drying (PRD) irrigation technique and salinity under arid climate. Agri Water Manag Amsterdam 2013; 123:1–11.
Naghavi MR, Pour-Aboughadareh A, Khalili M. Evaluation of drought tolerance indices for screening some of corn (Zea mays L.) cultivars under environmental conditions. Notulae Scientia Biologicae, Cluj-Napoca 2013; 5:388-393.
Khalili M, Pour-Aboughadareh AR, Naghavi MR, Mohammad Amini E. Evaluation of drought tolerance in safflower genotypes based on drought tolerance indices. Not Bot Horti Agrobo 2014; 42:214–218.
Pour-Siahbidi MM, Pour-Aboughadareh A. Evaluation of grain yield and repeatability of drought tolerance indices for screening chickpea (Cicer aritinum L.) genotypes under rainfed conditions. Iranian J Gen Plant Breed 2015; 2:28-37.
Khalili M, Pour-Aboughadareh A, Naghavi MR. Assessment of drought tolerance in barley: integrated selection criterion and drought tolerance indices. Environ Exp Bot, Latvia 2016; 14:33–41.
Ahmadi J, Pour-Aboughadareh A, Ourang SF, Mehrabi AA, Siddique, KHM. Screening wheat germplasm for seedling root architectural traits under contrasting water regimes: potential sources of variability for drought adaptation. Arch Agron Soil Sci 2018; 64:1351–1365.
Etminan A, Pour-Aboughadareh A, Mohammadi R, Shoshtari L, Yousefiazarkhanian M, Moradkhani H. Determining the best drought tolerance indices using artificial neural network (ANN): Insight into application of intelligent agriculture in agronomy and plant breeding. Cereal Res Commun 2019; 47:170–181.
Breton C, Souyris I, Villemur P, Berville A. Oil accumulation kinetic along ripening in four olive cultivars varying for fruit size. Fundamental, Nakajima 2009; 16:58–64.
Motilva M.J, Romero M, Alegre S, Girona J. Influence of regulated deficit irrigation strategies applied to olive trees (Arbequina cultivar) on oil yield and oil composition during the fruit ripening period. J Sci Food Agr. New Jersey 2008; 80:2037-43.
Brescia MA, Pugliese T, Hardy E, Sacco A. Compositional and structural investigations of ripening of table olives, Bella della Daunia, by means of traditional and magnetic resonance imaging analyses. Food Chem Amsterdam 2007; 105:400-404.
Seymour GB, Manning K, Poole M, King GJ. The genetics and epigenetics of fruit development and ripening. Curr Opin Plant Biol Amsterdam 2008; 11:58-63.
Xu ZZ, Zhou G.S, Wang YL, Han G.X, Li YJ. Changes in chlorophyll fluorescence in maize plants with imposed rapid dehydration at different leaf ages. J Plant Growth Regul Berlin 2008; 27:83–92.
Ahmadipour S, Arji I, Ebadi A, Abdossi V. Physiological and biochemical response of some olive cultivars (Olea europaea L.) to water stress. Cell Mol Biol 2018; 64:20-29.
Yan W, Zhang XZ, Shi PL, Yang ZL, He YT, Xu LL. Carbon dioxide exchange and water use efficiency of alpine meadow ecosystems on the Tibetan Plateau. J Natural Resources 2006; 21:756-767.
Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage and antioxidative defense mechanism in plants under stressful conditions. Jpn J Bot London 2012; 217037:1–26.
Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer C.H. Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration. Ann Botany Oxford 2002; 89:841–850.
Jiménez A, Gómez JM, Navarro E, Sevilla F. Changes in the antioxidative systems in mitochondria during ripening of pepper fruits. Plant Physiol Biochem Amsterdam 2002; 40:515–520.
Cansev A, Gulen H, Eris A. The activities of catalase and ascorbate peroxidase in olive (Olea europaea L. cv. Gemlik) under low temperature stress. Hortic Environ Biote Jeollabuk-do 2011; 52:113-120.
Hashempour A, Ghasemnezhad M, Ghazvini R, Sohani MM. Olive (Olea europaea L.) freezing tolerance related to antioxidant enzymes activity during cold acclimation and non-acclimation. Acta Physiol Plant 2014; 36:3231–3241.