Abstract
In this study, poplar tissue culture (hybrid black poplar, M1 genotype) was subjected to water stress influenced by polyethyleneglycol 6000 (100 and 200 mOsm PEG 6000). The aim of the research was to investigate the biochemical response of poplar tissue culture on water deficit regime. Antioxidant status was analyzed including antioxidant enzymes, superoxide-dismutase (SOD), catalase (CAT), guiacol-peroxidase (GPx), glutathione-peroxidase (GSH-Px), glutathione-reductase, reduced glutathione, total phenol content, Ferric reducing antioxidant power and DPPH radical antioxidant power. Polyphenol oxidase and phenylalanine-ammonium-lyase were determined as enzymatic markers of polyphenol metabolism. Among oxidative stress parameters lipid peroxidation, carbonyl-proteins, hydrogen-peroxide, reactive oxygen species, nitric-oxide and peroxynitrite were determined. Proline, proline-dehydrogenase and glycinebetaine were measured also as parameters of water stress. Cell viability is finally determined as a biological indicator of osmotic stress. It was found that water stress induced reactive oxygen and nitrogen species and lipid peroxidation in leaves of hybrid black poplar and reduced cell viability. Antioxidant enzymes including SOD, GPx, CAT and GSH-Px were induced but total phenol content and antioxidant capacity were reduced by PEG 6000 mediated osmotic stress. The highest biochemical response and adaptive reaction was the increase of proline and GB especially by 200 mOsm PEG. While long term molecular analysis will be necessary to fully address the poplar potentials for water stress adaptation, our results on hybrid black poplar suggest that glycine-betaine, proline and PDH enzyme might be the most important markers of poplar on water stress and that future efforts should be focused on these markers and strategies to enhance their concentration in poplar.
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References
Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126
Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877
Ancillotti C, Bogani P, Biricolti S, Calistri E, Checchini L, Ciofi L, Gonnelli C, Del Bubba M (2015) Changes in polyphenol and sugar concentrations in wild type and genetically modified Nicotiana langsdorffii Weinmann in response to water and heat stress. Plant Physiol Biochem 97:52–61
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
Badiani M, De Biasi MG, Colognola M, Artemi F (1990) Catalase, peroxidase and superoxide dismutase activities in seedlings submitted to increasing water deficit. Agrochimica 34:90–102
Barchet GL, Dauwe R, Guy RD, Schroeder WR, Soolanayakanahally RY, Campbell MM, Mansfield SD (2014) Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling. Tree Physiol 34:1203–1219
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant soil 39:205–207
Benzie, I.F.F., Strain JJ (1999) Ferric reducing antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 299:15–27
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chiu DT, Stults FH, Tappel AL (1976) Purification and properties of rat lung soluble glutathione peroxidase. Biochim Biophys Acta (BBA) Enzymol 445:558–566
Chmielowska-Bąk J, Izbiańska K, Deckert J (2015) Products of lipid, protein and RNA oxidation as signals and regulators of gene expression in plants. Front Plant Sci 6:405
Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2094
Csiszár J, Szabó M, Erdei L, Márton L, Horváth F, Tari I (2004) Auxin autotrophic tobacco callus tissues resist oxidative stress: the importance of glutathione S-transferase and glutathione peroxidase activities in auxin heterotrophic and autotrophic calli. J Plant Physiol 161:691–699
Devappa RK, Rakshit SK, Dekker RF (2015) Forest biorefinery: potential of poplar phytochemicals as value-added co-products. Biotechnol Adv 33:681–716
Egert M, Tevini M (2002) Influence of drought on some physiological parameters symptomatic for oxidative stress in leaves of chives (Allium schoenoprasum). Environ Exp Bot 48:43–49
Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11
Gamble PE, Burke JJ (1984) Effect of water stress on the chloroplast antioxidant system I. Alterations in glutathione reductase activity. Plant Physiol 76:615–621
Gebre GM, Kuhns MR, Brandle JR (1994) Organic solute accumulation and dehydration tolerance in three water-stressed Populus deltoides clones. Tree Physiol 14:575–587
Gerasimova NG, Pridvorova SM, Ozeretskovskaya OL (2005) Role of L-phenylalanine ammonia Lyase in the induced resistance and susceptibility of potato plants. Appl Biochem Microbiol 41:103–105
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6:1746–1751
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307
Gu RS, Jiang XN, Guo ZC (1999) Organogenesis and plantlet regeneration in vitro of Populus euphratica. Acta Bot Sin 41:29–33
Halliwell B (1989) Free radicals, reactive oxygen species and human disease: a critical evaluation with special reference to atherosclerosis. Br J Exp Pathol 70:737
Halliwell B, Foyer CH (1978) Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. Planta 139:9–17
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756
Iqbal S, Bano A (2009) Water stress induced changes in antioxidant enzymes, membrane stability and seed protein profile of different wheat accessions. Afr J Biotechnol 8:6576–6587
Ke Q, Wang Z, Ji CY, Jeong JC, Lee HS, Li H, Xu B, Deng X, Kwak SS (2015) Transgenic poplar expressing Arabidopsis YUCCA6 exhibits auxin-overproduction phenotypes and increased tolerance to abiotic stress. Plant Physiol Biochem 94:19–27
Kolbert Z, Pető A, Lehotai N, Feigl G, Erdei L (2012) Long-term copper (Cu2+) exposure impacts on auxin, nitric oxide (NO) metabolism and morphology of Arabidopsis thaliana L. Plant Growth Regul 68:151–159
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608
Łabanowska M, Filek M, Kurdziel M, Bidzińska E, Miszalski Z, Hartikainen H (2013) EPR spectroscopy as a tool for investigation of differences in radical status in wheat plants of various tolerances to osmotic stress induced by NaCl and PEG-treatment. J Plant Physiol 170:136–145
Lehotai N, Pető A, Bajkán S, Erdei L, Tari I, Kolbert Z (2011) In vivo and in situ visualization of early physiological events induced by heavy metals in pea root meristem. Acta Physiol Plant 33:2199–2207
Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Ahn BW, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478
Macedo AF, 2012. Abiotic stress responses in plants: metabolism to productivity. In abiotic stress responses in plants (pp 41–61). Springer New York
Manivannan P, Jaleel CA, Sankar B, Kishorekumar A, Somasundaram R, Lakshmanan GA, Panneerselvam R (2007) Growth, biochemical modifications and proline metabolism in Helianthus annuus L. as induced by drought stress. Colloids Surf B 59:141–149
Manoj K, Uday D (2007) In vitro screening of tomato genotypes for drought resistance using polyethylene glycol. Afr J Biotechnol 6:691–696
Marcińska I, Czyczyło-Mysza I, Skrzypek E, Filek M, Grzesiak S, Grzesiak MT, Janowiak F, Hura T, Dziurka M, Dziurka K, Nowakowska A (2013) Impact of osmotic stress on physiological and biochemical characteristics in drought-susceptible and drought-resistant wheat genotypes. Acta Physiol Plant 35:451–461
Matsumoto T, Nishida K, Noguchi M, Tamaki E (1973) Some factors affecting the anthocyanin formation by Populus cells in suspension culture. Agric Biol Chem 37:561–567
McClendon JH, Blinks LR (1952) Use of high molecular weight solutes in the study of isolated intracellular structures. Nature 170:577–578
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497
Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. CMLS Cell Mol Life Sci 69:3225–3243
Orlović S, Pilipović A, Pajnik LP (2004) Conservation of black poplar (Populus nigra L.) and other poplars in Serbia and Montenegro, in Populus nigra network, Report of the 7–8 th meetings in Osijek and Germany, Koskela, Vries, Gajaba and Wuhlisch, pp 65–66
Osman HS (2015) Enhancing antioxidant–yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann Agric Sci 60:389–402
Pető A, Lehotai N, Feigl G, Tugyi N, Ördög A, Gémes K, Tari I, Erdei L, Kolbert Z (2013) Nitric oxide contributes to copper tolerance by influencing ROS metabolism in Arabidopsis. Plant Cell Rep 32:1913–1923
Plaut Z, Federman E (1985) A simple procedure to overcome polyethelene glycol toxicity on whole plants. Plant Physiol 79:559–561
Polle A, Otter T, Seifert F (1994) Apoplastic peroxidases and lignification in needles of Norway spruce (Picea abies L.). Plant Physiol 106:53–60
Popović BM, Štajner D, Slavko K, Sandra B (2012) Antioxidant capacity of cornelian cherry (Cornus mas L.)–Comparison between permanganate reducing antioxidant capacity and other antioxidant methods. Food Chem 134:734–741
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 Physiol Biochem 105:242–250
Qi-lin D, Chen C, Bin F, Ting-ting L, Xia T, Yuan-ya G, Ying-kun S, Jin W, Shi-zhang D (2009) Effects of NaCl treatment on the antioxidant enzymes of oilseed rape (Brassica napus L.) seedlings. Afr J Biotechnol 8:5400–5405
Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207
Sánchez-Moreno C, Larrauri JA, Saura-Calixto F (1998) A procedure to measure the antiradical efficiency of polyphenols. J Sci Food Agric 76:270–276
Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060
Sorkheh K, Shiran B, Khodambashi M, Rouhi V, Mosavei S, Sofo A (2012) Exogenous proline alleviates the effects of H2O2-induced oxidative stress in wild almond species. Russ J Plant Physiol 59:788–798
Štajner D, Orlović S, Popović BM, Kebert M, Stojnić S, Klašnja B (2012) Chemical parameters of oxidative stress adaptability in beech. J Chem 2013:1–8
Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
Türkan I, Bor M, Özdemir F, Koca H (2005) Differential responses of lipid peroxidation and antioxidants in the leaves of drought-tolerant P. acutifolius Gray and drought-sensitive P. vulgaris L. subjected to polyethylene glycol mediated water stress. Plant Sci 168:223–231
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376
Wang M, Li Q, Fu S, Xiao D, Dong B (2005) Effects of exogenous nitric oxide on drought-resistance of poplar. J Appl Ecol 16:805–810
Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue Organ Cult 63:199–206
Woff SF (1994) Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydrogen peroxides. Methods Enzymol 233:182–189
Yang F, Xiao X, Zhang S, Korpelainen H, Li C (2009) Salt stress responses in Populus cathayana Rehder. Plant Sci 176:669–677
Acknowledgements
This research is part of Project No. III43002 which is financially supported by the Ministry of Science, Technologies and Development of the Republic of Serbia and IPA Planttrain project (ID: HUSBR/1203/221/173).
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Popović, B.M., Štajner, D., Ždero-Pavlović, R. et al. Biochemical response of hybrid black poplar tissue culture (Populus × canadensis) on water stress. J Plant Res 130, 559–570 (2017). https://doi.org/10.1007/s10265-017-0918-4
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DOI: https://doi.org/10.1007/s10265-017-0918-4