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Plant function and evolutionary biology
RESEARCH ARTICLE

Penconazole and calcium ameliorate drought stress in canola by upregulating the antioxidative enzymes

Maryam Rezayian https://orcid.org/0000-0003-1135-9118 A , Vahid Niknam A B and Hassan Ebrahimzadeh A
+ Author Affiliations
- Author Affiliations

A Department of Plant Biology, and Centre of Excellence in Phylogeny of Living Organisms in Iran, School of Biology, College of Science, University of Tehran, Tehran 14155, Iran.

B Corresponding author. Email: vniknam@khayam.ut.ac.ir

Functional Plant Biology 47(9) 825-839 https://doi.org/10.1071/FP19341
Submitted: 30 November 2019  Accepted: 3 April 2020   Published: 25 June 2020

Abstract

The aim of this research was to gauge the alternations in the lipid peroxidation and antioxidative enzyme activity in two cultivars (cv. RGS003 and cv. Sarigol) of canola under drought stress and drought tolerance amelioration by penconazole (PEN) and calcium (Ca). Plants were treated with different polyethylene glycol (PEG) concentrations (0, 5, 10 and 15%) without or with PEN (15 mg L–1) and Ca (15 mM). The Ca treatment prevented the negative effects of drought on fresh weight (FW) in RGS003 and Sarigol at 5 and 15% PEG respectively. Ca and PEN/Ca treatments caused significant induction in the proline content in Sarigol at 15% PEG; the latter treatment was accompanied by higher glycine betaine (GB), lower malondialdehyde (MDA) and growth recovery. Hydrogen peroxide (HO2) content in Sarigol was proportional to the severity of drought stress and all PEN, Ca and PEN/Ca treatments significantly reduced the H2O2 content. PEN and PEN/Ca caused alleviation of the drought-induced oxidative stress in RGS003. RGS003 cultivar exhibited significantly higher antioxidative enzymes activity at most levels of drought, which could lead to its drought tolerance and lower MDA content. In contrast to that of Sarigol, the activity of catalase and superoxide dismutase (SOD) increased with Ca and PEN/Ca treatments in RGS003 under low stress. The application of PEN and Ca induced significantly P5CS and SOD expression in RGS003 under drought stress after 24 h. Overall, these data demonstrated that PEN and Ca have the ability to enhance the tolerance against the drought stress in canola plants.

Additional keywords: antioxidant enzymes, canola.


References

Abeles FB, Biles CL (1991) Characterization of peroxidases in lignifying peach fruit endocarp. Plant Physiology 95, 269–273.
Characterization of peroxidases in lignifying peach fruit endocarp.Crossref | GoogleScholarGoogle Scholar | 16667963PubMed |

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

Alam R, Iqbal A, Khan L, Ali L, Munir L, Javed A, Rehman L, Swati ZA (2011) Enhanced antioxidant defense after exogenous application of Ca2+ and K+ in Brassica napus seedlings under water deficit stress. African Journal of Biotechnology 10, 14052–14060.
Enhanced antioxidant defense after exogenous application of Ca2+ and K+ in Brassica napus seedlings under water deficit stress.Crossref | GoogleScholarGoogle Scholar |

Asada K (1994) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In ‘Photoinhibition of photosynthesis. From molecular mechanisms to the field’. (Eds NR Baker, JR Bowyer) pp. 129–142. (Bios Scientific Publishers: Oxford, UK)

Ashraf M, Foolad MR (2007) Roles of glycinebetaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 59, 206–216.
Roles of glycinebetaine and proline in improving plant abiotic stress resistance.Crossref | GoogleScholarGoogle Scholar |

Ashraf M, Iram A (2005) Drought-induced changes in some organic substances in nodules and other plant parts of two legumes differing in salt tolerance. Flora 200, 535–546.
Drought-induced changes in some organic substances in nodules and other plant parts of two legumes differing in salt tolerance.Crossref | GoogleScholarGoogle Scholar |

Barker AV, Pilbeam DJ (2007) ‘Handbook of plant nutrition.’ (Taylor & Francis Group: Boca Raton, FL, USA)

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Journal of Plant Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar |

Ben Amor NB, Megdiche W, Abdelly C (2010) The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress. Acta Physiologiae Plantarum 32, 453–461.
The effect of calcium on the antioxidant systems in the halophyte Cakile maritima under salt stress.Crossref | GoogleScholarGoogle Scholar |

Boyer JS (1982) Plant productivity and environment. Science 218, 443–448.
Plant productivity and environment.Crossref | GoogleScholarGoogle Scholar | 17808529PubMed |

Demiral T, Turkan I (2004) Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? Journal of Plant Physiology 161, 1089–1100.
Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment?Crossref | GoogleScholarGoogle Scholar | 15535118PubMed |

Din J, Khan SU, Ali L, Gurmani AR (2011) Physiological and agronomic response of canola varieties to drought stress. Journal of Animal and Plant Sciences 21, 78–82.

Farooq MA, Gill RA, Islam F, Ali B, Liu H, Xu J, He S, Zhou W (2016) Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Frontiers in Plant Science 7, 468–484.
Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L.Crossref | GoogleScholarGoogle Scholar | 27148299PubMed |

Fazeli F, Ghorbanali M, Niknam V (2007) Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two Sesame cultivars. Biologia Plantarum 51, 98–103.
Effect of drought on biomass, protein content, lipid peroxidation and antioxidant enzymes in two Sesame cultivars.Crossref | GoogleScholarGoogle Scholar |

Fletcher RA, Hofstra G (1990) Improvement of uniconazole induced protection in wheat seedlings. Journal of Plant Growth Regulation 9, 207–212.
Improvement of uniconazole induced protection in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |

Fletcher RA, Gill A, Davis TD, Sankhla N (2000) Triazoles as plant growth regulator and stress protectants. Review Horticulture 24, 55–138.
Triazoles as plant growth regulator and stress protectants.Crossref | GoogleScholarGoogle Scholar |

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

Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology 155, 93–100.
Understanding oxidative stress and antioxidant functions to enhance photosynthesis.Crossref | GoogleScholarGoogle Scholar | 21045124PubMed |

Gao XY, Yang GP, Xu ZQ, Xu FC (1999) Effect of calcium on anti-oxidant enzymes of lipid peroxidation of soybean leaves under water stress. Journal of South China Agricultural University 2, 58–62.

Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosystems 143, 81–96.
ROS generation in plants: boon or bane?Crossref | GoogleScholarGoogle Scholar |

Giannopolitis CN, Ries SK (1977) Superoxide dismutases: II. Purification and quantitative relationship with water soluble protein in seedlings. Plant Physiology 59, 315–318.
Superoxide dismutases: II. Purification and quantitative relationship with water soluble protein in seedlings.Crossref | GoogleScholarGoogle Scholar | 16659840PubMed |

Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil 70, 303–307.
Rapid assay for determination of water soluble quaternary ammonium compounds.Crossref | GoogleScholarGoogle Scholar |

Grossmann K (1990) Plant growth retardants as tools in physiological research. Physiologia Plantarum 78, 640–648.
Plant growth retardants as tools in physiological research.Crossref | GoogleScholarGoogle Scholar |

Hassanpour H, Khavari-Nejad RA, Niknam V, Najafi F, Razavi Kh (2012) Effects of penconazole and water deficit stress on physiological and antioxidative responses in pennyroyal (Mentha pulegium L.). Acta Physiologiae Plantarum 34, 1537–1549.
Effects of penconazole and water deficit stress on physiological and antioxidative responses in pennyroyal (Mentha pulegium L.).Crossref | GoogleScholarGoogle Scholar |

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

Hong-Bo S, Li-Ye C, Ming-An S (2008) Calcium as a versatile plant signal transducer under soil water stress. BioEssays 30, 634–641.
Calcium as a versatile plant signal transducer under soil water stress.Crossref | GoogleScholarGoogle Scholar | 18536032PubMed |

Hussain M, Malik MA, Farooq M, Ashraf MY, Cheema MA (2008) Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. Journal Agronomy & Crop Science 194, 193–199.
Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower.Crossref | GoogleScholarGoogle Scholar |

Jaleel CA, Gopi R, Alagu Lakshmanan GM, Panneerselvam R (2006) Triadimefon induced changes in the antioxidant metabolism and ajmalicine production in Catharanthus roseus (L.) G. Don. Plant Science 171, 271–276.
Triadimefon induced changes in the antioxidant metabolism and ajmalicine production in Catharanthus roseus (L.) G. Don.Crossref | GoogleScholarGoogle Scholar |

Jebara S, Jebara M, Limam F, Elarbi Aouani M (2005) Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress. Journal of Plant Physiology 162, 929–936.
Changes in ascorbate peroxidase, catalase, guaiacol peroxidase and superoxide dismutase activities in common bean (Phaseolus vulgaris) nodules under salt stress.Crossref | GoogleScholarGoogle Scholar | 16146319PubMed |

Jensen CR, Mogensen VO, Mortensen G, Fieldsend JK, Milford GFJ, Anderson MN, Thage JH (1996) Seed glucosinolate, oil and protein content of field-grown rape (Brassica napus L.) affected by soil drying and evaporative demand. Field Crops Research 47, 93–105.
Seed glucosinolate, oil and protein content of field-grown rape (Brassica napus L.) affected by soil drying and evaporative demand.Crossref | GoogleScholarGoogle Scholar |

Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signaling & Behavior 5, 233–238.
Cytosolic calcium and pH signaling in plants under salinity stress.Crossref | GoogleScholarGoogle Scholar |

Kader MA, Lindberg S, Seidel T, Golldack D, Yemelyanov V (2007) Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt tolerant and – sensitive rice (Oryza sativa) cultivars. Physiologia Plantarum 130, 99–111.
Sodium sensing induces different changes in free cytosolic calcium concentration and pH in salt tolerant and – sensitive rice (Oryza sativa) cultivars.Crossref | GoogleScholarGoogle Scholar |

Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20, 915–921.
Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid.Crossref | GoogleScholarGoogle Scholar |

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 5432063PubMed |

Leul M, Zhou WJ (1999) Alleviation of waterlogging damage in winter rape by uniconazole application: effects on enzyme activity, lipid peroxidation, and membrane integrity. Journal of Plant Growth Regulation 18, 9–14.
Alleviation of waterlogging damage in winter rape by uniconazole application: effects on enzyme activity, lipid peroxidation, and membrane integrity.Crossref | GoogleScholarGoogle Scholar | 10467014PubMed |

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 |

Ma R, Zhang M, Li B, Du G, Wang J, Chen J (2005) The effects of exogenous Ca on endogenous polyamine levels and drought-resistant traits of spring wheat grown under arid conditions. Journal of Arid Environments 63, 177–190.
The effects of exogenous Ca on endogenous polyamine levels and drought-resistant traits of spring wheat grown under arid conditions.Crossref | GoogleScholarGoogle Scholar |

Mascher R, Nagy E, Lippmann B, Hornlein S, Fischer S, Scheiding W, Neagoe A, Bergmann H (2005) Improvement of tolerance to paraquat and drought in barley (Hordeum vulgare L.) by exogenous 2-aminoethanol: effects on superoxide dismutase activity and chloroplast ultrastructure. Plant Science 168, 691–698.
Improvement of tolerance to paraquat and drought in barley (Hordeum vulgare L.) by exogenous 2-aminoethanol: effects on superoxide dismutase activity and chloroplast ultrastructure.Crossref | GoogleScholarGoogle Scholar |

Merati MJ, Hassanpour H, Niknam V, Mirmasoumi M (2014) Exogenous application of penconazole regulates plant growth and antioxidative responses in salt stressed Mentha pulegium L. Journal of Plant Interactions 9, 791–801.
Exogenous application of penconazole regulates plant growth and antioxidative responses in salt stressed Mentha pulegium L.Crossref | GoogleScholarGoogle Scholar |

Munne-Bosch S, Alegre L (2000) The xanthophyll cycle is induced by light irrespective of water status in field-grown lavender (Lavandula stoechas). Physiologia Plantarum 108, 147–151.
The xanthophyll cycle is induced by light irrespective of water status in field-grown lavender (Lavandula stoechas).Crossref | GoogleScholarGoogle Scholar |

Munns R, Rebetzke GJ, Husain S, James RA, Hare RA (2003) Genetic control of sodium extrusion in durum wheat. Australian Journal of Agricultural Research 54, 627–635.
Genetic control of sodium extrusion in durum wheat.Crossref | GoogleScholarGoogle Scholar |

Nazemi G, Alhani A (2014) The effects of water deficit stress on seed yield and quantitative traits of canola cultivars. International Journal Farming & Alli Science 3, 819–822.

Noctor G (2006) Metabolic signalling in defence and stress: the control roles of soluble redox couples. Plant, Cell & Environment 29, 409–425.
Metabolic signalling in defence and stress: the control roles of soluble redox couples.Crossref | GoogleScholarGoogle Scholar |

Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 15012235PubMed |

Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. Journal of Experimental Botany 49, 623–647.
Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants.Crossref | GoogleScholarGoogle Scholar |

Raymond J, Rakariyatham N, Azanza J (1993) Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochemistry 34, 927–931.
Purification and some properties of polyphenoloxidase from sunflower seeds.Crossref | GoogleScholarGoogle Scholar |

Shao HB, Song WY, Chu LY (2008a) Advances of calcium signals involved in plant anti-drought. Comptes Rendus Biologies 331, 587–596.
Advances of calcium signals involved in plant anti-drought.Crossref | GoogleScholarGoogle Scholar | 18606388PubMed |

Shao HB, Chu LY, Shao MA (2008b) Calcium as a versatile plant signal transducer under soil water stress. BioEssays 30, 634–641.
Calcium as a versatile plant signal transducer under soil water stress.Crossref | GoogleScholarGoogle Scholar |

Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221–227.
Gene networks involved in drought stress response and tolerance.Crossref | GoogleScholarGoogle Scholar | 17075077PubMed |

Shu MY, Fan MQ (2000) Effect of osmotic stress and calcium on membrane-lipid peroxidation and the activity of defense enzymes in fir seedling. Forest Research 4, 391–396.

Sofo A, Dichio B, Xiloyannis C, Masia A (2005) Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Functional Plant Biology 32, 45–53.
Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes.Crossref | GoogleScholarGoogle Scholar |

Somasundaram R, Jaleel CA, Abraham SS, Azooz MM, Panneerselvam R (2009) Role of paclobutrazol and ABA in drought stress amelioration in Sesamum indicum L. Global Journal of Molecular Science 4, 56–62.

Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 20036181PubMed |

Turan M, Esringu A (2007) Phytoremediation based on canola (Brassica napus L.) and Indian mustard (Brassica juncea L.) planted on spiked soil by aliquot amount of Cd, Cu, Pb, and Zn. Plant, Soil and Environment 53, 7–15.
Phytoremediation based on canola (Brassica napus L.) and Indian mustard (Brassica juncea L.) planted on spiked soil by aliquot amount of Cd, Cu, Pb, and Zn.Crossref | GoogleScholarGoogle Scholar |

Tuteja N (2009) Integrated calcium signaling in plants. In ‘Signaling and communication in plants’. (Eds F Baluška, S Mancuso) pp. 29–49. (Springer-Verlag, Berlin: Germany)

Upadhyaya H, Panda SK, Dutta BK (2011) CaCl2 improves post-drought recovery potential in Camellia sinensis (L) O. Plant Cell Reports 30, 495–503.
CaCl2 improves post-drought recovery potential in Camellia sinensis (L) O.Crossref | GoogleScholarGoogle Scholar | 21153899PubMed |

van Loon LC (1971) Tobacco polyphenol oxidase. A specific staining method indicating non-identify with peroxidase. Phytochemistry 10, 503–507.
Tobacco polyphenol oxidase. A specific staining method indicating non-identify with peroxidase.Crossref | GoogleScholarGoogle Scholar |

van Rensburg LV, Kruger GHJ (1994) Evaluation of components of oxidative stress metabolism for use in selection of drought tolerant cultivars of Nicotiana tabacum L. Journal of Plant Physiology 143, 730–737.
Evaluation of components of oxidative stress metabolism for use in selection of drought tolerant cultivars of Nicotiana tabacum L.Crossref | GoogleScholarGoogle Scholar |

Vaseva I, Akiscan Y, Simova-Stoilova L, Kostadinova A, Nenkova R, Anders I, Feller U, Demirevska K (2012) Antioxidant response to drought in red and white clover. Acta Physiologiae Plantarum 34, 1689–1699.
Antioxidant response to drought in red and white clover.Crossref | GoogleScholarGoogle Scholar |

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science 151, 59–66.
Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |

Wan G, Najeeb U, Jilani G, Naeem MS, Zhou W (2011) Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. Environmental Science and Pollution Research International 18, 1478–1486.
Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system.Crossref | GoogleScholarGoogle Scholar | 21533918PubMed |

Wendel JF, Weeden NF (1989) Visualization and interpretation of plant isozymes. In ‘Isozyme in plant biology’. (Eds DE Soltis, PS Soltis) pp. 5–45. (Chapman and Hall: London, UK)

Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Analytical Biochemistry 44, 301–305.
An improved procedure using ferricyanide for detecting catalase isozymes.Crossref | GoogleScholarGoogle Scholar | 4109029PubMed |

Xiang J, Chen Z, Wang P, Yu L, Li M (2008) Effect of CaCl2 treatment on the changing of drought related physiological and biochemical indexes of Brassica napus. Frontiers of Agriculture in China 2, 423–427.
Effect of CaCl2 treatment on the changing of drought related physiological and biochemical indexes of Brassica napus.Crossref | GoogleScholarGoogle Scholar |

Xu L, Islam F, Ali B, Pei Z, Li J, Awais Ghani M, Zhou W (2017) Silicon and water-deficit stress differentially modulate physiology and ultrastructure in wheat (Triticum aestivum L.). 3 Biotech 7, 273–286.
Silicon and water-deficit stress differentially modulate physiology and ultrastructure in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 28794928PubMed |

Zhou B, Guo Z (2009) Calcium is involved in the abscisic acid-induced ascorbate peroxidase, superoxide dismutase and chilling resistance in Stylosanthes guianensis. Biologia Plantarum 53, 63–68.
Calcium is involved in the abscisic acid-induced ascorbate peroxidase, superoxide dismutase and chilling resistance in Stylosanthes guianensis.Crossref | GoogleScholarGoogle Scholar |

Zhou W, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regulation 26, 41–47.
Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape.Crossref | GoogleScholarGoogle Scholar |

Zhou W, Leul M (1999) Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation. Plant Growth Regulation 27, 99–104.
Uniconazole-induced tolerance of rape plants to heat stress in relation to changes in hormonal levels, enzyme activities and lipid peroxidation.Crossref | GoogleScholarGoogle Scholar |