Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Biochemical and molecular approach of oxidative damage triggered by water stress and rewatering in sunflower seedlings of two inbred lines with different ability to tolerate water stress

Federico Ramírez A , Maximiliano Escalante A , Ana Vigliocco B , M. Verónica Pérez-Chaca C , Mariana Reginato B , Alicia Molina C , Julio A. Di Rienzo D , Andrea Andrade B and Sergio Alemano https://orcid.org/0000-0003-2701-1052 B E
+ Author Affiliations
- Author Affiliations

A Laboratorio de Fisiología Vegetal, Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto (UNRC), 5800-Río Cuarto, Córdoba, Argentina.

B Laboratorio de Fisiología Vegetal, Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, UNRC, Instituto de Investigaciones Agrobiotecnológicas-Consejo Nacional de Investigaciones Científicas y Técnicas (INIAB-CONICET), 5800-Río Cuarto, Córdoba, Argentina.

C Departamento de Bioquímica y Ciencias Biológicas, Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis, 5700-San Luis, Argentina.

D Facultad de Ciencias Agropecuarias, Universidad Nacional de Córdoba, 5000-Córdoba, Argentina.

E Corresponding author. Email: salemano@exa.unrc.edu.ar

Functional Plant Biology 47(8) 727-743 https://doi.org/10.1071/FP19264
Submitted: 10 September 2019  Accepted: 10 March 2020   Published: 1 June 2020

Abstract

Water stress accelerates the generation of reactive oxygen species, which trigger a cascade of antioxidative defence mechanisms comprising enzymatic and nonenzymatic antioxidants. The aim of this study was to investigate the oxidative damage and the antioxidative defence systems in seedlings of the water stress-tolerant (B71) and the sensitive (B59) inbred lines of sunflower (Helianthus annuus L.) in response to water stress and rewatering. In addition, we characterised the transcriptomic profile associated with enzymatic antioxidative defence. An elevated electrolyte leakage in B59 indicated increased plasmatic membrane permeability, which correlated with greater sensitivity to water stress. In response to water stress, both lines showed an increase in malondialdehyde and H2O2 content but these increases were more noticeable in the sensitive line. In both lines, an increase in enzymatic activity (e.g. peroxidase and ascorbate peroxidase) was not sufficient to overcome the H2O2 accumulation triggered by water stress. Upon water stress, the overall expression level of genes associated with the enzymatic antioxidant system increased in B71 and decreased in B59, which showed downregulated levels of most genes in the shoots. The general profile of phenolic compounds was clearly different between organs and between inbred lines. The B59 line activated nonenzymatic antioxidant responses to counteract the oxidative stress caused by water stress. The tolerance of B71 to water stress could be associated with compensatory antioxidant mechanisms based on the expression of genes encoding enzyme components of the ascorbate–glutathione and redoxin cycles, which contributed to explaining, at least partly, the response of this line.

Additional keywords: antioxidative response, gene expression, Helianthus annuus L., phenolic compounds, reactive oxygen species.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |

Andrade A, Vigliocco A, Alemano S, Alvarez D, Abdala G (2009) Differential accumulation of abscisic acid and its catabolites in drought-sensitive and drought-tolerant sunflower seeds. Seed Science Research 19, 201–211.
Differential accumulation of abscisic acid and its catabolites in drought-sensitive and drought-tolerant sunflower seeds.Crossref | GoogleScholarGoogle Scholar |

Andrade A, Vigliocco A, Alemano S, Llanes A, Abdala G (2013) Comparative morpho-biochemical responses of sunflower lines sensitive and tolerant to water stress. American Journal of Plant Sciences 4, 156–167.
Comparative morpho-biochemical responses of sunflower lines sensitive and tolerant to water stress.Crossref | GoogleScholarGoogle Scholar |

Andrade A, Escalante M, Vigliocco A, Tordable MC, Alemano S (2017) Involvement of jasmonates in responses of sunflower (Helianthus annuus) seedlings to moderate water stress. Plant Growth Regulation 83, 501–511.
Involvement of jasmonates in responses of sunflower (Helianthus annuus) seedlings to moderate water stress.Crossref | GoogleScholarGoogle Scholar |

Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidant system in plants. Current Science 82, 1227–1238.

Bajji M, Kinet JM, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regulation 36, 61–70.
The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat.Crossref | GoogleScholarGoogle Scholar |

Baloğlu MC, Kavas M, Aydin G, Öktem HA, Yücel AM (2012) Antioxidative and physiological responses of two sunflower (Helianthus annuus) cultivars under PEG-mediated drought stress. Turkish Journal of Botany 36, 707–714.

Basu S, Ramegowda HV, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Research 5, 1554
Plant adaptation to drought stress.Crossref | GoogleScholarGoogle Scholar |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.Crossref | GoogleScholarGoogle Scholar | 4943714PubMed |

Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae 120, 264–270.
Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery.Crossref | GoogleScholarGoogle Scholar |

Bradford MM (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.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. International Journal of Molecular Sciences 14, 3540–3555.
Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans.Crossref | GoogleScholarGoogle Scholar | 23434657PubMed |

Buer CS, Muday GK, Djorjevic MA (2008) Implications of long-distance flavonoid movement in Arabidopsis thaliana. Plant Signaling & Behavior 3, 415–417.
Implications of long-distance flavonoid movement in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 18662937PubMed |

Cona A, Rea G, Botta M, Corelli F, Federico R, Angelini R (2006) Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. Journal of Experimental Botany 57, 2277–2289.
Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L.Crossref | GoogleScholarGoogle Scholar | 16831849PubMed |

Contour-Ansel D, Torres-Franklin ML, Cruz de Carvalho MH, D’Arcy-Lameta A, Zuily-Fodil Y (2006) Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment. Annals of Botany 98, 1279–1287.
Glutathione reductase in leaves of cowpea: cloning of two cDNAs, expression and enzymatic activity under progressive drought stress, desiccation and abscisic acid treatment.Crossref | GoogleScholarGoogle Scholar | 17008354PubMed |

del Río LA, Gómez M, López-Gorgé J (1977) Catalase and peroxidase activities, chlorophyll and proteins during storage of pea plants at chilling temperatures. Revista Espanola de Fisiologia 33, 143–148.

Dhanda SS, Sethi SS, Behl RK (2004) Indices of drought tolerance in wheat genotypes at stages of plant growth. Journal Agronomy & Crop Science 190, 6–12.
Indices of drought tolerance in wheat genotypes at stages of plant growth.Crossref | GoogleScholarGoogle Scholar |

Di Rienzo JA, Guzmán AW, Casanoves F (2002) A multiple-comparisons method based on the distribution of the root node distance of a binary tree. Journal of Agricultural Biological & Environmental Statistics 7, 129–142.
A multiple-comparisons method based on the distribution of the root node distance of a binary tree.Crossref | GoogleScholarGoogle Scholar |

Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2018) ‘InfoStat versión 2018’. (Centro de Transferencia InfoStat, Facultad de Ciencias Agrarias FCA, Universidad Nacional de Córdoba: Córdoba, Argentina). Available at: http://www.infostat.com.ar [Verified 18 May 2020]

Dudziak K, Zapalska M, Borner A, Szczerba H, Kowalczyk K, Nowak M (2019) Analysis of wheat gene expression related to the oxidative stress response and signal transduction under short-term osmotic stress. Nature 9, 2743.

Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cellular and Molecular Life Sciences 72, 673–689.
General mechanisms of drought response and their application in drought resistance improvement in plants.Crossref | GoogleScholarGoogle Scholar | 25336153PubMed |

Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell & Environment 28, 1056–1071.
Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context.Crossref | GoogleScholarGoogle Scholar |

Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112, 15–21.
Roles of cell wall peroxidases in plant development.Crossref | GoogleScholarGoogle Scholar | 25109234PubMed |

Gaber A, Yoshimura K, Yamamoto T, Yabuta Y, Takeda T, Miyasaka H, Nakano Y, Shigeoka S (2006) Glutathione peroxidase-like protein of Synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis. Physiologia Plantarum 128, 251–262.
Glutathione peroxidase-like protein of Synechocystis PCC 6803 confers tolerance to oxidative and environmental stresses in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Geetha A, Sivasankar A, Saidaiah P, Prayaga L (2017) Antioxidant enzyme response in water stress sunflower genotypes. International Journal of Current Microbiology and Applied Sciences 6, 138–146.
Antioxidant enzyme response in water stress sunflower genotypes.Crossref | GoogleScholarGoogle Scholar |

Ghobadi M, Taherabadi S, Ghobadi ME, Mohammadi GR, Jalali-Honarmand S (2013) Antioxidant capacity, photosynthetic characteristics and water relations of sunflower (Helianthus annuus L.) cultivars in response to drought stress. Industrial Crops and Products 50, 29–38.
Antioxidant capacity, photosynthetic characteristics and water relations of sunflower (Helianthus annuus L.) cultivars in response to drought stress.Crossref | GoogleScholarGoogle Scholar |

Griesser M, Weingart G, Schoedl-Hummel K, Neumann N, Becker M, Varmuza K, Liebner F, Schuhmacher R, Forneck A (2015) Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir). Plant Physiology and Biochemistry 88, 17–26.
Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir).Crossref | GoogleScholarGoogle Scholar | 25602440PubMed |

Guan LM, Scandalios JG (2000) Hydrogen peroxide-mediated catalase gene expression in response to wounding. Free Radical Biology & Medicine 28, 1182–1190.
Hydrogen peroxide-mediated catalase gene expression in response to wounding.Crossref | GoogleScholarGoogle Scholar |

Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. Journal of Proteome Research 6, 1451–1460.
Proteomics uncovers a role for redox in drought tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 17343403PubMed |

Halime R, Mahlagh G, Peyvandi M (2013) Effect of drought interactions with ascorbate on some biochemical parameters and antioxidant enzymes activities in Dracocephalum moldavica L. World Applied Sciences Journal 27, 872–882.
Effect of drought interactions with ascorbate on some biochemical parameters and antioxidant enzymes activities in Dracocephalum moldavica L.Crossref | GoogleScholarGoogle Scholar |

Hamid Badawi GH, Yamauchi Y, Shimada E, Sasaki R, Kawano N, Tanaka K, Tanaka K (2004) Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts. Plant Science 166, 919–928.
Enhanced tolerance to salt stress and water deficit by overexpressing superoxide dismutase in tobacco (Nicotiana tabacum) chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Hasanuzzaman M, Nahar K, Anee TI, Fujita M (2017) Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance. Physiology and Molecular Biology of Plants 23, 249–268.
Glutathione in plants: biosynthesis and physiological role in environmental stress tolerance.Crossref | GoogleScholarGoogle Scholar | 28461715PubMed |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stechiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts: I. Kinetics and stechiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |

Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiology 133, 170–181.
Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower.Crossref | GoogleScholarGoogle Scholar | 12970484PubMed |

Jiang Y, Watkins E, Liu S, Yu X, Luo N (2010) Antioxidative responses and candidate gene expression in prairie junegrass under drought stress. Journal of the American Society for Horticultural Science 135, 303–309.
Antioxidative responses and candidate gene expression in prairie junegrass under drought stress.Crossref | GoogleScholarGoogle Scholar |

Jiménez A, Hernández JA, del Rio LA, Sevilla F (1997) Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiology 114, 275–284.
Evidence for the presence of the ascorbate–glutathione cycle in mitochondria and peroxisomes of pea leaves.Crossref | GoogleScholarGoogle Scholar | 12223704PubMed |

Kasote DM, Katyare SS, Hedge MV, Bae H (2015) Significance of antioxidant potential of plants and its relevance to therapeutic applications. International Journal of Biological Sciences 11, 982–991.
Significance of antioxidant potential of plants and its relevance to therapeutic applications.Crossref | GoogleScholarGoogle Scholar | 26157352PubMed |

Kim D, Chun OK, Kim YJ, Moon H-Y, Lee CY (2003) Quantification of phenolics and their antioxidant capacity in fresh plums. Journal of Agricultural and Food Chemistry 51, 6509–6515.
Quantification of phenolics and their antioxidant capacity in fresh plums.Crossref | GoogleScholarGoogle Scholar | 14558771PubMed |

Laxa M, Liebthal M, Telman W, Chibani K, Dietz KJ (2019) The role of the plant antioxidant system in drought tolerance. Antioxidants 8, 94
The role of the plant antioxidant system in drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Lehtimäki N, Lintala M, Allahverdiyeva Y, Aro E-M, Mulo P (2010) Drought stress-induced upregulation of components involved inferredoxin-dependent cyclic electron transfer. Journal of Plant Physiology 167, 1018–1022.
Drought stress-induced upregulation of components involved inferredoxin-dependent cyclic electron transfer.Crossref | GoogleScholarGoogle Scholar | 20392519PubMed |

Liu Y, He C (2016) Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD. Plant Cell Reports 35, 995–1007.
Regulation of plant reactive oxygen species (ROS) in stress responses: learning from AtRBOHD.Crossref | GoogleScholarGoogle Scholar | 26883222PubMed |

Long T, Okegawa Y, Shikanai T, Schmidt G, Covert S (2008) Conserved role of PROTON GRADIENT REGULATION 5 in the regulation of PSI cyclic electron transport. Planta 228, 907–918.
Conserved role of PROTON GRADIENT REGULATION 5 in the regulation of PSI cyclic electron transport.Crossref | GoogleScholarGoogle Scholar | 18663471PubMed |

Lou L, Li X, Chen J, Li Y, Tang Y, Lv J (2018) Photosynthetic and ascorbate-glutathione metabolism in the flag leaves as compared to spikes under drought stress of winter wheat (Triticum aestivum L.) PLoS One 13, e0194625
Photosynthetic and ascorbate-glutathione metabolism in the flag leaves as compared to spikes under drought stress of winter wheat (Triticum aestivum L.)Crossref | GoogleScholarGoogle Scholar | 29566049PubMed |

Luo LJ (2010) Breeding for water-saving and drought-resistance rice (WDR) in China. Journal of Experimental Botany 61, 3509–3517.
Breeding for water-saving and drought-resistance rice (WDR) in China.Crossref | GoogleScholarGoogle Scholar | 20603281PubMed |

Marok MA, Tarrago L, Ksas B, Henri P, Abrous-Belbachir O, Havaux M, Rey P (2013) A drought-sensitive barley variety displays oxidative stress and strongly increased contents in low-molecular weight antioxidant compounds during water deficit compared to a tolerant variety. Journal of Plant Physiology 170, 633–645.
A drought-sensitive barley variety displays oxidative stress and strongly increased contents in low-molecular weight antioxidant compounds during water deficit compared to a tolerant variety.Crossref | GoogleScholarGoogle Scholar | 23541087PubMed |

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 12234732PubMed |

Most P, Jutta P (2015) Possible roles of plant sulfurtransferases in detoxification of cyanide, reactive oxygen species, selected heavy metals and arsenate. Molecules (Basel, Switzerland) 20, 1410–1423.
Possible roles of plant sulfurtransferases in detoxification of cyanide, reactive oxygen species, selected heavy metals and arsenate.Crossref | GoogleScholarGoogle Scholar |

Nair NC, Sheela D (2016) Quantification of secondary metabolites and antioxidant potential of selected members of the tribe Heliantheae. Journal of Pharmacognosy and Phytochemistry 5, 163–166.

Nigel CW, Glories Y (1991) Use of a modified dimethylaminocinnamaldehyde reagent for analysis of flavanols. American Journal of Enology and Viticulture 42, 364–366.

Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Frontiers in Plant Science 7, 230
Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium.Crossref | GoogleScholarGoogle Scholar | 26973673PubMed |

Nxele X, Klein A, Ndimba BK (2017) Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. South African Journal of Botany 108, 261–266.
Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants.Crossref | GoogleScholarGoogle Scholar |

Pérez-Chaca MV, Rodríguez-Serrano M, Molina AS, Pedranzani HE, Zirulnik F, Sandalio LM, Romero-Puertas MC (2014) Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots. Plant, Cell & Environment 37, 1672–1687.
Cadmium induces two waves of reactive oxygen species in Glycine max (L.) roots.Crossref | GoogleScholarGoogle Scholar |

Pérez-López U, Robredo A, Lacuesta M, Sgherri C, Muñoz-Rueda A, Navari-Izzoc F, Mena-Petite A (2009) The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2. Physiologia Plantarum 135, 29–42.
The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2.Crossref | GoogleScholarGoogle Scholar | 19121097PubMed |

Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018). ‘nlme: linear and nonlinear mixed effects models. R package version 3.1–137.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at: https://CRAN.R-project.org/package=nlme [Verified 18 May 2020]

Popović BM, Štajner D, Ždero-Pavlović R, Tumbas-Šaponjac V, Čanadanović-Brunet J, Orlović S (2016) Water stress induces changes in polyphenol profile and antioxidant capacity in poplar plants (Populus spp.). Plant Physiology and Biochemistry 105, 242–250.
Water stress induces changes in polyphenol profile and antioxidant capacity in poplar plants (Populus spp.).Crossref | GoogleScholarGoogle Scholar | 27116372PubMed |

Prashanth SR, Sadhasivam V, Parida A (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Research 17, 281–291.
Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia marina in indica rice var Pusa Basmati-1 confers abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 17541718PubMed |

Quartacci MF, Navari-Izzo F (1992) Water stress and free radical mediated changes in sunflower seedlings. Journal of Plant Physiology 139, 621–625.
Water stress and free radical mediated changes in sunflower seedlings.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2018). ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria). Available at: https://www.R-project.org/ [Verified 18 May 2020]

Ramachandra Reddy A, Chaitanya KV, Jutur PP, Sumithra K (2004) Differential anti-oxidative responses to water stress among five mulberry (Morus alba L.) cultivars. Environmental and Experimental Botany 52, 33–42.
Differential anti-oxidative responses to water stress among five mulberry (Morus alba L.) cultivars.Crossref | GoogleScholarGoogle Scholar |

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology & Medicine 26, 1231–1237.
Antioxidant activity applying an improved ABTS radical cation decolorization assay.Crossref | GoogleScholarGoogle Scholar |

Reddy AR, Chaitanyaa KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology 161, 1189–1202.
Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants.Crossref | GoogleScholarGoogle Scholar |

Romani A, Mancini P, Tatti S, Vincieri F (1996) Polyphenols and polysaccharides in Tuscan grapes and wines. Italian Journal of Food Science 8, 13–24.

Rossel JB, Walter PB, Hendrickson L, Chow WS, Poole A, Mullineaux PM, Pogson BJ (2006) A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance. Plant, Cell & Environment 29, 269–281.
A mutation affecting ASCORBATE PEROXIDASE 2 gene expression reveals a link between responses to high light and drought tolerance.Crossref | GoogleScholarGoogle Scholar |

Safronov O, Kreuzwieser J, Haberer G, Alyousif MS, Schulze W, Al-Harbi N, Arab L, Ache P, Stempfl T, Kruse J, Mayer KX, Hedrich R, Rennenberg H, Salojärvi J, Kangasjärvi J (2017) Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm). PLoS One 12, e0177883
Detecting early signs of heat and drought stress in Phoenix dactylifera (date palm).Crossref | GoogleScholarGoogle Scholar | 28570677PubMed |

Sairam RK, Srivastava GC (2001) Water stress tolerance of wheat (Triticum aestivum L.): variations in hydrogen peroxide accumulation and antioxidant activity in tolerant and susceptible genotypes. Journal Agronomy & Crop Science 186, 63–70.
Water stress tolerance of wheat (Triticum aestivum L.): variations in hydrogen peroxide accumulation and antioxidant activity in tolerant and susceptible genotypes.Crossref | GoogleScholarGoogle Scholar |

Sarvari M, Darvishzadeh R, Najafzadeh R, Maleki H (2017) Physio-biochemical and enzymatic responses of sunflower to drought stress. Journal of Plant Physiology and Breeding 7, 105–119.

Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Dokladi na Bulgarskata Akademiâ na Naukite 51, 121–124.

Shojaie B, Mostajeran A, Ghannadian M (2015) Flavonoid dynamic responses to different drought conditions: amount, type, and localization of flavonols in roots and shoots of Arabidopsis thaliana L. Turkish Journal of Biology 40, 612–622.
Flavonoid dynamic responses to different drought conditions: amount, type, and localization of flavonols in roots and shoots of Arabidopsis thaliana L.Crossref | GoogleScholarGoogle Scholar |

Sosa Alderete LG, Talano MA, Ibañez SG, Purro S, Agostini E, Milrad SR, Medina MI (2009) Establishment of transgenic tobacco hairy roots expressing basic peroxidases and its application for phenol removal. Journal of Biotechnology 139, 273–279.
Establishment of transgenic tobacco hairy roots expressing basic peroxidases and its application for phenol removal.Crossref | GoogleScholarGoogle Scholar | 19124050PubMed |

Teixeira FK, Menezes-Benavente L, Galvão VC, Margis R, Margis-Pinheiro M (2006) Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta 224, 300–314.
Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments.Crossref | GoogleScholarGoogle Scholar | 16397796PubMed |

Torres-Franklin ML, Contour-Ansel D, Zuily-Fodil Y, Pham-Thi AT (2008) Molecular cloning of glutathione reductase cDNAs and analysis of GR gene expression in cowpea and common bean leaves during recovery from moderate drought stress. Journal of Plant Physiology 165, 514–521.
Molecular cloning of glutathione reductase cDNAs and analysis of GR gene expression in cowpea and common bean leaves during recovery from moderate drought stress.Crossref | GoogleScholarGoogle Scholar | 17707549PubMed |

Vanková R, Dobrá J, Storchová H (2012) Recovery from drought stress in tobacco: an active process associated with the reversal of senescence in some plant parts and the sacrifice of others. Plant Signaling & Behavior 7, 19–21.
Recovery from drought stress in tobacco: an active process associated with the reversal of senescence in some plant parts and the sacrifice of others.Crossref | GoogleScholarGoogle Scholar |

Varela MC, Arslan I, Reginato MA, Cenzano AM, Luna MV (2016) Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina). Plant Physiology and Biochemistry 104, 81–91.
Phenolic compounds as indicators of drought resistance in shrubs from Patagonian shrublands (Argentina).Crossref | GoogleScholarGoogle Scholar | 27017434PubMed |

Vassilevska-Ivanova R, Shtereva L, Krapchtev B, Karceva T (2014) Response of sunflower (Helianthus annuus L.) genotypes to PEG-mediated water stress. Central European Journal of Biology 9, 1206–1214.

Vighi IL, Benítez LC, Amaral MN, Moraes GP, Auler PA, Rodrigues GS, Deuner S, Maia LC, Braga EJB (2017) Functional characterization of the antioxidant enzymes in rice plants exposed to salinity stress. Biologia Plantarum 61, 540–550.
Functional characterization of the antioxidant enzymes in rice plants exposed to salinity stress.Crossref | GoogleScholarGoogle Scholar |

Xu L, Han L, Huang B (2011) Antioxidant enzyme activities and gene expression patterns in leaves of Kentucky bluegrass in response to drought and post-drought recovery. Journal of the American Society for Horticultural Science 136, 247–255.
Antioxidant enzyme activities and gene expression patterns in leaves of Kentucky bluegrass in response to drought and post-drought recovery.Crossref | GoogleScholarGoogle Scholar |

Yamane K, Mitsuya S, Taniguchi M, Miyake H (2010) Transcription profiles of genes encoding catalase and ascorbate peroxidase in rice leaf tissues under salinity. Plant Production Science 13, 164–168.
Transcription profiles of genes encoding catalase and ascorbate peroxidase in rice leaf tissues under salinity.Crossref | GoogleScholarGoogle Scholar |

Yang Z, Wu Y, Li Y, Ling HQ, Chu C (2009) OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice. Plant Molecular Biology 70, 219–229.
OsMT1a, a type 1 metallothionein, plays the pivotal role in zinc homeostasis and drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 19229638PubMed |

Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytologist 132, 361–373.
Antioxidant responses to drought in sunflower and sorghum seedlings.Crossref | GoogleScholarGoogle Scholar | 26763632PubMed |

Zhang LX, Li SX, Zhang H, Liang ZS (2007) Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes. Journal Agronomy & Crop Science 193, 387–397.
Nitrogen rates and water stress effects on production, lipid peroxidation and antioxidative enzyme activities in two maize (Zea mays L.) genotypes.Crossref | GoogleScholarGoogle Scholar |

Zhang Z, Zhang Q, Wu J, Zheng X, Zheng S, Sun X, Qui Q, Lu T (2013) Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses. PLoS One 8, e57472
Gene knockout study reveals that cytosolic ascorbate peroxidase 2 (OsAPX2) plays a critical role in growth and reproduction in rice under drought, salt and cold stresses.Crossref | GoogleScholarGoogle Scholar | 24392024PubMed |