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Plant function and evolutionary biology
RESEARCH ARTICLE

The effect of vanadium(IV) complexes on development of Arabidopsis thaliana subjected to H2O2-induced stress

Joanna Rojek https://orcid.org/0000-0002-2257-7201 A D , Małgorzata Kozieradzka-Kiszkurno A , Małgorzata Kapusta A , Anna Aksmann B , Dagmara Jacewicz C , Joanna Drzeżdżon C , Aleksandra Tesmar C , Krzysztof Żamojć C , Dariusz Wyrzykowski C and Lech Chmurzyński C
+ Author Affiliations
- Author Affiliations

A Department of Plant Cytology and Embryology, Faculty of Biology, University of Gdańsk, Wita Stwosza 59, 80-308 Gdańsk, Poland.

B Department of Plant Physiology and Biotechnology, Faculty of Biology, University of Gdańsk, Wita Stwosza 59, 80-308 Gdańsk, Poland.

C Department of General and Inorganic Chemistry, Faculty of Chemistry, University of Gdańsk, Wita Stwosza 63, 80-308 Gdańsk, Poland.

D Corresponding author. Email: joanna.rojek@ug.edu.pl

Functional Plant Biology 46(10) 942-961 https://doi.org/10.1071/FP18262
Submitted: 10 October 2018  Accepted: 17 May 2019   Published: 17 June 2019

Abstract

The impact of oxydiacetate oxidovanadium(IV) complexes on plants is currently unknown. This report demonstrates the influence of these complexes on Arabidopsis thaliana (L.) Heynh. In the presence of 10−6 M vanadium(IV) complexes, plants proceeded through their entire life cycle, with the occurrence of proper morphological and cytological organisation of leaf and root tissues. The addition of 10−1 M H2O2 caused root damage, leaf necrosis, and plant death at around the seventh day, due to the destruction of the root system. Pretreatment of the plants with 10−6 M of vanadium(IV) compounds: VOSO4 and VO(oda), alleviated the effects of H2O2 to some extent. Plants pretreated with 10−6 M vanadium(IV) complexes survived longer despite the presence of H2O2. Considering the higher rate of plant survival in the presence of VOSO4, and the relatively high photosynthetic parameters and anthocyanin contents in the cells, we conclude that this vanadium(IV) compound can have positive effects on plants that are grown under stress conditions.

Additional keywords: hydroponic culture, H2O2, leaf and root ultrastructure, reactive oxygen species, vanadium(IV) complexes.


References

Appenroth KJ, Krech K, Keresztes A, Fischer W, Koloczek H (2010) Effects of nickel on the chloroplasts of the duckweeds Spirodela polyrhiza and Lemna minor and their possible use in biomonitoring and phytoremediation. Chemosphere 78, 216–223.
Effects of nickel on the chloroplasts of the duckweeds Spirodela polyrhiza and Lemna minor and their possible use in biomonitoring and phytoremediation.Crossref | GoogleScholarGoogle Scholar | 19945735PubMed |

Aroca R, Amodeo G, Fernández-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiology 137, 341–353.
The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots.Crossref | GoogleScholarGoogle Scholar | 15591439PubMed |

Benabdellah K, Ruiz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Molecular Biology 70, 647
Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar | 19437122PubMed |

Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. The Plant Cell 9, 209–221.
Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola.Crossref | GoogleScholarGoogle Scholar | 9061952PubMed |

Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. The Plant Cell 13, 1499–1510.
Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants.Crossref | GoogleScholarGoogle Scholar | 11449047PubMed |

Chen LS, Cheng L (2009) Photosystem 2 is more tolerant to high temperature in apple (Malus domestica Borkh.) leaves than in fruit peel. Photosynthetica 47, 112–120.
Photosystem 2 is more tolerant to high temperature in apple (Malus domestica Borkh.) leaves than in fruit peel.Crossref | GoogleScholarGoogle Scholar |

Claeys H, Van Landeghem S, Dubois M, Maleux K, Inzé D (2014) What is stress? Dose-response effects in commonly used in vitro stress assays. Plant Physiology 165, 519–527.
What is stress? Dose-response effects in commonly used in vitro stress assays.Crossref | GoogleScholarGoogle Scholar | 24710067PubMed |

Cuesta S, Francés D, García GB (2011) ROS formation and antioxidant status in brain areas of rats exposed to sodium metavanadate. Neurotoxicology and Teratology 33, 297–302.
ROS formation and antioxidant status in brain areas of rats exposed to sodium metavanadate.Crossref | GoogleScholarGoogle Scholar | 21056100PubMed |

D’Cruz OJ, Uckun FM (2002) Metvan: a novel oxovanadium(IV) complex with broad spectrum anticancer activity. Expert Opinion on Investigational Drugs 11, 1829–1836.
Metvan: a novel oxovanadium(IV) complex with broad spectrum anticancer activity.Crossref | GoogleScholarGoogle Scholar | 12457442PubMed |

Drzeżdżon J, Jacewicz D, Wyrzykowski D, Inkielewicz-Stępniak I, Sikorski A, Tesmar A, Chmurzyński A (2017) Structures, physicochemical and cytoprotective properties of new oxidovanadium(IV) complexes -(VO(mIDA)(dmbpy))·1.5H2O and (VO(IDA)(dmbpy))·2H2O. Journal of Molecular Structure 1143, 515–525.
Structures, physicochemical and cytoprotective properties of new oxidovanadium(IV) complexes -(VO(mIDA)(dmbpy))·1.5H2O and (VO(IDA)(dmbpy))·2H2O.Crossref | GoogleScholarGoogle Scholar |

Dzagli MM, Sossoe KK, Gadedjisso-Tossou KS, Mohou MA, Boca S, Astilean S, Zoueu J (2001) Spectroscopic studies on extracts of Moringa oleifera leaves for biosensing: adsorption of gold nanospheres on chloroplasts. ISESCO Journal of Science and Technology 12, 33–37.

Edelenbos M, Christensen LP, Grevsen K (2001) HPLC determination of chlorophyll and carotenoid pigments in processed green pea cultivars (Pisum sativum L.). Journal of Agricultural and Food Chemistry 49, 4768–4774.
HPLC determination of chlorophyll and carotenoid pigments in processed green pea cultivars (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar | 11600019PubMed |

Elektorowicz M, Keropian Z (2015) Lithium, vanadium and chromium uptake ability of Brassica juncea from lithium mine tailings. International Journal of Phytoremediation 17, 521–528.
Lithium, vanadium and chromium uptake ability of Brassica juncea from lithium mine tailings.Crossref | GoogleScholarGoogle Scholar | 25747238PubMed |

Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. Journal of Experimental Botany 53, 1249–1254.

Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiology 141, 341–345.
Control of plant development by reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 16760485PubMed |

García-Jiménez A, Trejo-Téllez LI, Guillén-Sánchez D, Gómez-Merino FC (2018) Vanadium stimulates pepper plant growth and flowering, increases concentrations of amino acids, sugars and chlorophylls, and modifies nutrient concentrations. PLoS One 13, e0201908
Vanadium stimulates pepper plant growth and flowering, increases concentrations of amino acids, sugars and chlorophylls, and modifies nutrient concentrations.Crossref | GoogleScholarGoogle Scholar | 30092079PubMed |

Gómez-Arroyo S, Barba-García A, Arenas-Huertero F, Cortés-Eslava J, de la Mora MG, García-Martínez R (2018) Indicators of environmental contamination by heavy metals in leaves of Taraxacum officinale in two zones of the metropolitan area of Mexico City. Environmental Science and Pollution Research International 25, 4739–4749.
Indicators of environmental contamination by heavy metals in leaves of Taraxacum officinale in two zones of the metropolitan area of Mexico City.Crossref | GoogleScholarGoogle Scholar | 29197063PubMed |

Gómez-Merino FC, Trejo-Téllez LI (2018) The role of beneficial elements in triggering adaptive responses to environmental stressors and improving plant performance. In ‘Biotic and abiotic stress tolerance in plants’. pp. 137–172. (Springer: Singapore)

Gould KS (2004) Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves. Journal of Biomedicine & Biotechnology 2004, 314–320.
Nature’s Swiss army knife: the diverse protective roles of anthocyanins in leaves.Crossref | GoogleScholarGoogle Scholar |

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, 1–32.

Imtiaz M, Rizwan MS, Xiong S, Li H, Ashraf M, Shahzad SM, Shahzad M, Rizwan M, Tu S (2015a) Vanadium, recent advancements and research prospects: a review. Environment International 80, 79–88.
Vanadium, recent advancements and research prospects: a review.Crossref | GoogleScholarGoogle Scholar | 25898154PubMed |

Imtiaz M, Tu S, Xie Z, Han D, Ashraf M, Rizwan MS (2015b) Growth, V uptake, and antioxidant enzymes responses of chickpea (Cicer arietinum L.) genotypes under vanadium stress. Plant and Soil 390, 17–27.
Growth, V uptake, and antioxidant enzymes responses of chickpea (Cicer arietinum L.) genotypes under vanadium stress.Crossref | GoogleScholarGoogle Scholar |

Imtiaz M, Mushtaq MA, Rizwan MS, Arif MS, Yousaf B, Ashraf M, Shuanglian X, Rizwan M, Mehmood S, Tu S (2016) Comparison of antioxidant enzyme activities and DNA damage in chickpea (Cicer arietinum L.) genotypes exposed to vanadium. Environmental Science and Pollution Research International 23, 19787–19796.
Comparison of antioxidant enzyme activities and DNA damage in chickpea (Cicer arietinum L.) genotypes exposed to vanadium.Crossref | GoogleScholarGoogle Scholar | 27411539PubMed |

Imtiaz M, Rizwan MS, Mushtaq MA, Yousaf B, Ashraf M, Ali M, Yousuf A, Rizwan M, Din M, Dai Z, Xiong S, Mehmood S, Tu S (2017) Interactive effects of vanadium and phosphorus on their uptake, growth and heat shock proteins in chickpea genotypes under hydroponic conditions. Environmental and Experimental Botany 134, 72–81.
Interactive effects of vanadium and phosphorus on their uptake, growth and heat shock proteins in chickpea genotypes under hydroponic conditions.Crossref | GoogleScholarGoogle Scholar |

Iseki K, Homma K, Shiraiwa T, Jongdee B, Mekwatanakarn P (2014) The effects of cross-tolerance to oxidative stress and drought stress on rice dry matter production under aerobic conditions. Field Crops Research 163, 18–23.
The effects of cross-tolerance to oxidative stress and drought stress on rice dry matter production under aerobic conditions.Crossref | GoogleScholarGoogle Scholar |

Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiology 145, 1460–1470.
Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17932308PubMed |

Jiang Z, Zhu S, Ye R, Xue Y, Chen A, An L, Pei ZM (2013) Relationship between NaCl- and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis. PLoS One 8, e76130
Relationship between NaCl- and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24391760PubMed |

Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. The Plant Journal 61, 909–921.
The development of Arabidopsis as a model plant.Crossref | GoogleScholarGoogle Scholar | 20409266PubMed |

Kovinich N, Kayanja G, Chanoca A, Riedl K, Otegui MS, Grotewold E (2014) Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis. Planta 240, 931–940.
Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24903357PubMed |

Kozieradzka-Kiszkurno M, Płachno BJ, Bohdanowicz J (2011) Are unusual plasmodesmata in the embryo-suspensor restricted to species from the genus Sedum among Crassulaceae? Flora 206, 684–690.
Are unusual plasmodesmata in the embryo-suspensor restricted to species from the genus Sedum among Crassulaceae?Crossref | GoogleScholarGoogle Scholar |

Krüger GH, Tsimilli‐Michael M, Strasser RJ (1997) Light stress provokes plastic and elastic modifications in structure and function of photosystem II in camellia leaves. Physiologia Plantarum 101, 265–277.
Light stress provokes plastic and elastic modifications in structure and function of photosystem II in camellia leaves.Crossref | GoogleScholarGoogle Scholar |

Libik-Konieczny M, Kozieradzka-Kiszkurno M, Desel C, Michalec-Warzecha Ż, Miszalski Z, Konieczny R (2015) The localization of NADPH oxidase and reactive oxygen species in in vitro-cultured Mesembryanthemum crystallinum L. hypocotyls discloses their differing roles in rhizogenesis. Protoplasma 252, 477–487.
The localization of NADPH oxidase and reactive oxygen species in in vitro-cultured Mesembryanthemum crystallinum L. hypocotyls discloses their differing roles in rhizogenesis.Crossref | GoogleScholarGoogle Scholar | 25172434PubMed |

Lin CW, Lin CY, Chang CC, Lee RH, Tsai TM, Chen PY, Chi WC, Huan HJ (2009) Early signalling pathways in rice roots under vanadate stress. Plant Physiology and Biochemistry 47, 369–376.
Early signalling pathways in rice roots under vanadate stress.Crossref | GoogleScholarGoogle Scholar | 19250836PubMed |

Lin CY, Huang LY, Chi WC, Huang TL, Kakimoto T, Tsai CR, Huang HJ (2015) Pathways involved in vanadate‐induced root hair formation in Arabidopsis. Physiologia Plantarum 153, 137–148.
Pathways involved in vanadate‐induced root hair formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24833217PubMed |

Liu L, Jiang Z, Zhang S, Zhao H, Yang W, Siedow JN, Pei Z-M (2018) Both NaCl and H2O2 long-term stresses affect basal cytosolic Ca2+ levels but only NaCl alters cytosolic Ca2+ signatures in Arabidopsis. Frontiers in Plant Science 9, 1390
Both NaCl and H2O2 long-term stresses affect basal cytosolic Ca2+ levels but only NaCl alters cytosolic Ca2+ signatures in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30405646PubMed |

Malan C, Greyling M, Gressel J (1990) Correlation between CuZn superoxide dismutase and glutathione reductase, and environmental and xenobiotic stress tolerance in maize inbreds. Plant Science 69, 157–166.
Correlation between CuZn superoxide dismutase and glutathione reductase, and environmental and xenobiotic stress tolerance in maize inbreds.Crossref | GoogleScholarGoogle Scholar |

Mandal C, Ghosh N, Adak MK, Dey N (2013) Interaction of polyamine on oxidative stress induced by exogenously applied hydrogen peroxide in Salvinia natans Linn. Theoretical and Experimental Plant Physiology 25, 203–212.
Interaction of polyamine on oxidative stress induced by exogenously applied hydrogen peroxide in Salvinia natans Linn.Crossref | GoogleScholarGoogle Scholar |

Marzban L, McNeill JH (2003) Insulin‐like actions of vanadium: potential as a therapeutic agent. Journal of Trace Elements in Experimental Medicine 16, 253–267.
Insulin‐like actions of vanadium: potential as a therapeutic agent.Crossref | GoogleScholarGoogle Scholar |

Mendoza-Soto AB, Sánchez F, Hernández G (2012) MicroRNAs as regulators in plant metal toxicity response. Frontiers in Plant Science 3, 105
MicroRNAs as regulators in plant metal toxicity response.Crossref | GoogleScholarGoogle Scholar | 22661980PubMed |

Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends in Plant Science 16, 300–309.
ROS signaling: the new wave?Crossref | GoogleScholarGoogle Scholar | 21482172PubMed |

Mukherjee B, Patra B, Mahapatra S, Banerjee P, Tiwari A, Chatterjee M (2004) Vanadium – an element of atypical biological significance. Toxicology Letters 150, 135–143.
Vanadium – an element of atypical biological significance.Crossref | GoogleScholarGoogle Scholar | 15093669PubMed |

Nawaz MA, Jiao Y, Chen C, Shireen F, Zheng Z, Imtiaz M, Bie Z, Huang Y (2018) Melatonin pretreatment improves vanadium stress tolerance of watermelon seedlings by reducing vanadium concentration in the leaves and regulating melatonin biosynthesis and antioxidant-related gene expression. Journal of Plant Physiology 220, 115–127.
Melatonin pretreatment improves vanadium stress tolerance of watermelon seedlings by reducing vanadium concentration in the leaves and regulating melatonin biosynthesis and antioxidant-related gene expression.Crossref | GoogleScholarGoogle Scholar | 29172132PubMed |

Orozco-Cárdenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of the National Academy of Sciences of the United States of America 96, 6553–6557.
Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway.Crossref | GoogleScholarGoogle Scholar | 10339626PubMed |

Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Reports 24, 255–265.
Peroxidases have more functions than a Swiss army knife.Crossref | GoogleScholarGoogle Scholar | 15856234PubMed |

Perez IB, Brown PJ (2014) The role of ROS signaling in cross-tolerance: from model to crop. Frontiers in Plant Science 5, 754
The role of ROS signaling in cross-tolerance: from model to crop.Crossref | GoogleScholarGoogle Scholar | 25566313PubMed |

Pessoa JC, Etcheverry S, Gambino D (2015) Vanadium compounds in medicine. Coordination Chemistry Reviews 301–302, 24–48.
Vanadium compounds in medicine.Crossref | GoogleScholarGoogle Scholar |

Pokora W, Aksmann A, Baścik-Remisiewicz A, Dettlaff-Pokora A, Rykaczewski M, Gappa M, Tukaj Z (2017) Changes in nitric oxide/hydrogen peroxide content and cell cycle progression: study with synchronized cultures of green alga Chlamydomonas reinhardtii. Journal of Plant Physiology 208, 84–93.
Changes in nitric oxide/hydrogen peroxide content and cell cycle progression: study with synchronized cultures of green alga Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 27894022PubMed |

Pranczk J, Jacewicz D, Wyrzykowski D, Chmurzyński L (2014) Analytical methods for determination of reactive oxygen species. Current Pharmaceutical Analysis 10, 293–304.
Analytical methods for determination of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |

Puckette MC, Weng H, Mahalingam R (2007) Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula. Plant Physiology and Biochemistry 45, 70–79.
Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 17270456PubMed |

Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrative Plant Biology 50, 2–18.
Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network.Crossref | GoogleScholarGoogle Scholar | 18666947PubMed |

Raju NGJ, Sarita P, Chandra Sekhara Rao J, Rao KCB, Bhuloka Reddy S (2013) Correlation of trace elemental content in selected anticancer medicinal plants with their curative ability using particle induced x-ray emission (PIXE). Journal of Medicinal Plants Research 7, 1081–1086.

Rehder D (1991) Biologische Chemie des Vanadiums: Biomimetische Vanadium-verbindungen als Katalysatoren und Antidiabetika. Angewandte Chemie 30, 148–167.
Biologische Chemie des Vanadiums: Biomimetische Vanadium-verbindungen als Katalysatoren und Antidiabetika.Crossref | GoogleScholarGoogle Scholar |

Reiter RJ, Tan DX, Zhou Z, Cruz MHC, Fuentes-Broto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20, 7396–7437.
Phytomelatonin: assisting plants to survive and thrive.Crossref | GoogleScholarGoogle Scholar | 25911967PubMed |

Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiology 141, 357–366.
Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling.Crossref | GoogleScholarGoogle Scholar | 16760488PubMed |

Roy PR, Tahjib-Ul-Arif MM, Akter T, Rani Ray S, Abu Sayed M (2016) Exogenous ascorbic acid and hydrogen peroxide alleviates salt-induced oxidative stress in rice (Oryza sativa L.) by enhancing antioxidant enzyme activities and proline content. Advances in Environmental Biology 10, 148–154.

Saco D, Martín S, San José P (2013) Vanadium distribution in roots and leaves of Phaseolus vulgaris: morphological and ultrastructural effects. Biologia Plantarum 57, 128–132.
Vanadium distribution in roots and leaves of Phaseolus vulgaris: morphological and ultrastructural effects.Crossref | GoogleScholarGoogle Scholar |

Singh BB (1971) Effect of vanadium on the growth, yield and chemical composition of maize (Zea mays L.) Plant and Soil 34, 209–213.
Effect of vanadium on the growth, yield and chemical composition of maize (Zea mays L.)Crossref | GoogleScholarGoogle Scholar |

Smirnoff N, Arnaud D (2019) Hydrogen peroxide metabolism and functions in plants. New Phytologist 221, 1197–1214.
Hydrogen peroxide metabolism and functions in plants.Crossref | GoogleScholarGoogle Scholar | 30222198PubMed |

Srivastava AK, Mehdi MZ (2005) Insulino‐mimetic and anti‐diabetic effects of vanadium compounds. Diabetic Medicine 22, 2–13.
Insulino‐mimetic and anti‐diabetic effects of vanadium compounds.Crossref | GoogleScholarGoogle Scholar | 15606684PubMed |

Stewart AJ, Chapman W, Jenkins GI, Graham I, Martin T, Crozier A (2001) The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant, Cell & Environment 24, 1189–1197.
The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues.Crossref | GoogleScholarGoogle Scholar |

Strasser RJ, Srivastava A, Govindjee (1995) Polyphasis chlorophyll a fluorescence transient in plant and cyanobacteria. Photochemistry and Photobiology 61, 32–42.
Polyphasis chlorophyll a fluorescence transient in plant and cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as tool to characterize and screen photosynthetics samples. In ‘Probing photosynthesis: mechanism, regulation and adaptation’. (Eds M Yunus, U Pathre, P Mohanty) pp. 445–483. (Taylor & Francis: Bristol, UK)

Sun Y, Wang H, Liu S, Peng X (2016) Exogenous application of hydrogen peroxide alleviates drought stress in cucumber seedlings. South African Journal of Botany 106, 23–28.
Exogenous application of hydrogen peroxide alleviates drought stress in cucumber seedlings.Crossref | GoogleScholarGoogle Scholar |

Surówka E, Dziurka M, Kocurek M, Goraj S, Rapacz M, Miszalski Z (2016) Effects of exogenously applied hydrogen peroxide on antioxidant and osmoprotectant profiles and the C3-CAM shift in the halophyte Mesembryanthemum crystallinum L. Journal of Plant Physiology 200, 102–110.
Effects of exogenously applied hydrogen peroxide on antioxidant and osmoprotectant profiles and the C3-CAM shift in the halophyte Mesembryanthemum crystallinum L.Crossref | GoogleScholarGoogle Scholar | 27368070PubMed |

Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell & Environment 35, 259–270.
ROS and redox signalling in the response of plants to abiotic stress.Crossref | GoogleScholarGoogle Scholar |

Swanson S, Gilroy S (2010) ROS in plant development. Physiologia Plantarum 138, 384–392.
ROS in plant development.Crossref | GoogleScholarGoogle Scholar | 19947976PubMed |

Terzi R, Kadioglu A, Kalaycioglu E, Saglam A (2014) Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves. Journal of Plant Interactions 9, 559–565.
Hydrogen peroxide pretreatment induces osmotic stress tolerance by influencing osmolyte and abscisic acid levels in maize leaves.Crossref | GoogleScholarGoogle Scholar |

Tesmar A, Wyrzykowski D, Kazimierczuk K, Kłak J, Kowalski S, Inkielewicz-Stępniak I, Drzeżdżon J, Jacewicz D, Chmurzyński L (2017a) Structure, physicochemical and biological properties of an aqua (2,2′,2″-nitrilotriacetato)-oxidovanadium(IV) salt with 4-methylpyridinium cation. Zeitschrift fur Anorganische und Allgemeine Chemie 643, 501–510.
Structure, physicochemical and biological properties of an aqua (2,2′,2″-nitrilotriacetato)-oxidovanadium(IV) salt with 4-methylpyridinium cation.Crossref | GoogleScholarGoogle Scholar |

Tesmar A, Wyrzykowski D, Kruszyński R, Niska K, Inkielewicz-Stępniak I, Drzeżdżon J, Jacewicz D, Chmurzyński L (2017b) Characterization and cytotoxic effect of aqua-(2,2′,2′’-nitrilotriacetato)-oxo-vanadium salts on human osteosarcoma cells. Biometals 30, 261–275.
Characterization and cytotoxic effect of aqua-(2,2′,2′’-nitrilotriacetato)-oxo-vanadium salts on human osteosarcoma cells.Crossref | GoogleScholarGoogle Scholar | 28204978PubMed |

Thompson KH, Lichter J, LeBel C, Scaife MC, McNeill JH, Orvig C (2009) Vanadium treatment of type 2 diabetes: a view to the future. Journal of Inorganic Biochemistry 103, 554–558.
Vanadium treatment of type 2 diabetes: a view to the future.Crossref | GoogleScholarGoogle Scholar | 19162329PubMed |

Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal 11, 1187–1194.
Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction.Crossref | GoogleScholarGoogle Scholar |

Tian M, Gu Q, Zhu M (2003) The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus. Plant Science 165, 701–707.
The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus.Crossref | GoogleScholarGoogle Scholar |

Tocquin P, Corbesier L, Havelange A, Pieltain A, Kurtem E, Bernier G, Périlleux C (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biology 3, 2
A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12556248PubMed |

Tsiani E, Fantus IG (1997) Vanadium compounds: biological actions and potential as pharmacological agents. Trends in Endocrinology and Metabolism 8, 51–58.
Vanadium compounds: biological actions and potential as pharmacological agents.Crossref | GoogleScholarGoogle Scholar | 18406786PubMed |

Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163, 515–523.
Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar |

Vaccarino C, Cimino G, Tripodo MM, Laganà G, Lo Giudice L, Matarese R (1983) Leaf and fruit necroses associated with vanadium-rich ash emitted from a power plant burning fossil fuel. Agriculture, Ecosystems & Environment 10, 275–283.
Leaf and fruit necroses associated with vanadium-rich ash emitted from a power plant burning fossil fuel.Crossref | GoogleScholarGoogle Scholar |

Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Current Medicinal Chemistry 12, 1161–1208.
Metals, toxicity and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 15892631PubMed |

Wang Y, Li J, Wang J, Li Z (2010) Exogenous H2O2 improves the chilling tolerance of manilagrass and mascarenegrass by activating the antioxidative system. Plant Growth Regulation 61, 195–204.
Exogenous H2O2 improves the chilling tolerance of manilagrass and mascarenegrass by activating the antioxidative system.Crossref | GoogleScholarGoogle Scholar |

Wyrzykowski D, Inkielewicz‐Stępniak I, Czupryniak J, Jacewicz D, Ossowski T, Woźniak M, Chmurzyński L (2013) Electrochemical and biological studies on reactivity of (VO(oda)(H2O)2), (Co(oda)(H2O)2)·H2O, and (Ni(oda)(H2O)3)·1.5H2O towards superoxide free radicals. Zeitschrift fur Anorganische und Allgemeine Chemie 639, 1795–1799.
Electrochemical and biological studies on reactivity of (VO(oda)(H2O)2), (Co(oda)(H2O)2)·H2O, and (Ni(oda)(H2O)3)·1.5H2O towards superoxide free radicals.Crossref | GoogleScholarGoogle Scholar |

Wyrzykowski D, Inkielewicz-Stępniak I, Pranczk J, Żamojć K, Zięba P, Tesmar A, Jacewicz D, Ossowski T, Chmurzyński L (2015a) Physicochemical properties of ternary oxovanadium(IV) complexes with oxydiacetate and 1,10-phenanthroline or 2,2′-bpyridine. Cytoprotective activity in hippocampal neuronal HT22 cells. Biometals 28, 307–320.
Physicochemical properties of ternary oxovanadium(IV) complexes with oxydiacetate and 1,10-phenanthroline or 2,2′-bpyridine. Cytoprotective activity in hippocampal neuronal HT22 cells.Crossref | GoogleScholarGoogle Scholar | 25656562PubMed |

Wyrzykowski D, Kloska A, Pranczk J, Szczepańska A, Tesmar A, Jacewicz D, Pilarski B, Chmurzyński L (2015b) Physicochemical and biological properties of oxovanadium(IV), cobalt(II) and nickel(II) complexes with oxydiacetate anions. Biological Trace Element Research 164, 139–149.
Physicochemical and biological properties of oxovanadium(IV), cobalt(II) and nickel(II) complexes with oxydiacetate anions.Crossref | GoogleScholarGoogle Scholar | 25488702PubMed |

Xu FJ, Jin CW, Liu WJ, Zhang YS, Lin XY (2011) Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings. Journal of Integrative Plant Biology 53, 44–53.
Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 21205173PubMed |

Zhang JZ, Creelman RA, Zhu JK (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops. Plant Physiology 135, 615–621.
From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops.Crossref | GoogleScholarGoogle Scholar | 15173567PubMed |

Zheng X, Tan DX, Allan AC, Zuo B, Zhao Y, Reiter RJ, Wang L, Wang Z, Guo Y, Zhou J, Shan D, Li Q, Han Z, Kong J (2017) Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Scientific Reports 7, 41236
Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress.Crossref | GoogleScholarGoogle Scholar | 28145449PubMed |