Abstract
Ozone (O3) is an adverse environmental factor posing damage to ornamental plants. Thus, it is important to seek an effective way of enhancing plant tolerance to O3-induced damage. Methyl jasmonate (MJ) and melatonin (MT) are plant growth regulators (PGRs) involved in plant abiotic stress responses. In this study, compared with the control group of plants without ozone, the influence of exogenous MJ (0, 10, 50, 100, and 150 μM) and MT (0, 0.1, 0.5, 2.5, and 12.5 μM) on the resistance of Malus crabapple ‘Hong Jiu’ was evaluated under O3 stress (100 ± 10 nL/L for 3 h). Our data revealed that levels of MDA were significantly enhanced following O3 treatment compared with plants without O3. O3 induced the activities of antioxidant enzymes and the accumulation of non-enzymatic antioxidants. While lower malondialdehyde (MDA) content, greater activities of antioxidant enzymes, and higher levels of soluble protein and non-enzymatic antioxidants were observed in PGRs-pretreated plants than in non-PGRs-pretreated plants under O3 stress. Based on the above results and air pollution tolerance index (APTI), an exogenous supply of MJ and MT to Malus crabapple ‘Hong Jiu’ seedlings was protective for O3-induced toxicity. The present study provides new insights into the mechanisms of MJ and MT amelioration of O3-induced oxidative stress damages in Malus crabapple ‘Hong Jiu.’
Similar content being viewed by others
Abbreviations
- ANOVA:
-
Analysis of variance
- APTI:
-
Air pollution tolerance index
- AsA:
-
Ascorbic acid
- CAT:
-
Catalase
- GSH:
-
Glutathione
- H2O2 :
-
Hydrogen peroxide
- MDA:
-
Malondialdehyde
- MJ:
-
Methyl jasmonate
- MT:
-
Melatonin
- NBT:
-
Nitroblue tetrazolium
- O2 :
-
Oxygen
- O2 − :
-
Superoxide anion
- O3 :
-
Ozone
- OTC:
-
Open-top chamber
- PGRs:
-
Plant growth regulators
- POD:
-
Peroxidase
- ROS:
-
Reactive oxygen species
- RWC:
-
Relative water content
- SD:
-
Standard deviation
- SDAU:
-
Shandong Agricultural University
- SE:
-
Standard error
- SOD:
-
Superoxide dismutase
- TBA:
-
2-Thiobarbituric acid
- TCH:
-
Total chlorophyll
References
Aeobi H (1974) In: Bergmayer (ed) Catalase: H.U methods of enzymeatic analysis, vol 2. Academic, Cambridge, pp 673–684
Ali MB, Yu KW, Hahn EJ, Paek KY (2006) Methyl jasmonate and salicylic acid elicitation induces ginsenosides accumulation, enzymatic and non-enzymatic antioxidant in suspension culture panax ginseng, roots in bioreactors. Plant Cell Rep 25:613–620
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (sods) in controlling oxidative stress in plants. J Exp Bot 53(372):1331–1341
Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphénoloxidase in Beta vulgaris. Plant Physiol 24:1–13
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287
Besada A (1987) A facile and sensitive spectrophotometric determination of ascorbic acid. Talanta 34(8):731–732
Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19(7):409–413
Ding F, Liu B, Zhang S (2017) Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci Hortic 219:264–271
Fan J, Hu Z, Xie Y, Chan Z, Chen K, Amombo E et al (2015) Alleviation of cold damage to photosystem ii and metabolisms by melatonin in bermudagrass. Front Plant Sci 6:925
Feng Z, Sun J, Wan W, Hu E, Calatayud V (2014) Evidence of widespread ozone-induced visible injury on plants in Beijing, China. Environ Pollut 193(1):296–301
Fishman J (1991) The global consequences of increasing tropospheric ozone concentrations. Chemosphere 22(7):685–695
Galano A, Tan DX, Reiter RJ (2011) Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 51(1):1–16
Gao F, Li P, Feng ZZ (2017a) Interactive effects of ozone and drought stress on plants: a review. Chin J Plant Ecol 41(2):252–268
Gao F, Xia H, Yuan X, Huang S, Liu J, Liang D (2017b) Effects of exogenous melatonin on phenolic substance content and antioxidant ability of kiwifruit seedlings under salt stress. Acta Agric Zhejiangensis 29(7):1144–1150
Gaucher C, Costanzo N, Widden P, Renaud JP, Dizengremel P, Mauffette Y, Chevrier N (2006) Response to an ozone gradient of growth and enzymes implicated in tolerance to oxidative stress in Acer saccharum (Marsh.) seedlings. Ann For Sci 63(4):387–397
Gonçalves JF, Becker AG, Cargnelutti D, Tabaldi LA, Pereira LB, Battisti V et al (2007) Cadmium toxicity causes oxidative stress and induces response of the antioxidant system in cucumber seedlings toxicidade de cádmio causa estresse oxidativo e induz resposta do sistema antioxidante em plântulas de pepino. Braz J Plant Physiol 19(3):119–123
Gong B, Shi QH (2017) Review of melatonin in horticultural crops. Sci Agric Sin 50(12):2326–2337
Gong X, Chen X, Feng S, Sun J, Qiu Y, Ma L (2017) Effects of ozone stress on physiological and biochemical characteristics dwarfing rootstock M9T337. Agric Sci Technol 18(4):579–582
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212
Heagle AS, Body DE, Heck WW (1973) An open-top field chamber to assess the impact of air pollution on plants. J Environ Qual 2(3):365–368
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: i. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198
Hou S, Zou T, Wang J, Sun X, Xu N (2017) Effects of methyl jasmonate and salicylic acid on the growth and resistance of Pyropia haitanensis. Mar Sci 41(1):104–112
Hu Z, Fan J, Xie Y, Amombo E, Liu A, Gitau MM, Khaldun ABM, Chen L, Fu J (2016) Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermuda grass by exogenous melatonin. Plant Physiol Biochem Ppb 100:94–104
Ji YY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12(2):63–68
Jia Y (2016) Effects of ozone stress on grain yield, quality and plant lodging resistance of different wheat varieties. (Doctoral dissertation, Yangzhou University)
Jiang C, Cui Q, Feng K, Xu D, Li C, Zheng Q (2016) Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings. Acta Physiol Plant 38(4):1–9
Krishnaveni M (2013) Air pollution tolerance index and antioxidant activity of Parthenium hysterophorus. J Pharm Res 7(4):296–298
Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol 32(32):9
Krupa S, Mcgrath MT, Andersen CP, Booker FL, Burkey KO, Chappelka AH et al (2007) Ambient ozone and plant health. Plant Dis 85(1):4–12
Lie GW, Guo SH, Xue L (2014a) Effects of ozone stress on plant growth. Ecol Sci 33(3):607–612
Lie GW, Ye LH, Xue L (2014b) Effects of ozone stress on major plant physiological functions. Acta Ecol Sin 34(2):294–306
Liu RK, Shen YW, Liu XJ (1983) A study on physiological responses of plant to SO2. Plant Physiol Commun 4:25–28
Liu SX, Huang YZ, Luo ZJ, Huang YC, Bao QL, Wang PP et al (2016) Effects of exogenous melatonin on germination of rice seeds under cd stresses. J Agro Environ Sci 35(6):1034–1041
Mahalingam R, Jambunathan N, Gunjan SK, Faustin E, Weng H, Ayoubi P (2006) Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana. Plant Cell Environ 29(7):1357–1371
Meng X, Jin H, Wang Q, Tian S (2009) Changes in physiology and quality of peach fruits treated by methyl jasmonate under low temperature stress. Food Chem 114(3):1028–1035
Meng X, Zhang Y, Xue Y, Liu Y et al (2016) Analysis of the soluble substances, grouting rate and yield factors of different wheat varieties (strains) in coastal saline-alkali soil. Crops 1:135–139
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410
Morgan PB, Mies TA, Bollero GA, Nelson RL, Long SP (2006) Season-long elevation of ozone concentration to projected 2050 levels under fully open-air conditions substantially decreases the growth and production of soybean. New Phytol 170(2):333–343
Nagalakshmi N, Prasad MN (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160(2):291–299
Ogunkunle CO, Suleiman LB, Oyedeji S, Awotoye OO, Fatoba PO (2015) Assessing the air pollution tolerance index and anticipated performance index of some tree species for biomonitoring environmental health. Agrofor Syst 89(3):447–454
Pandey AK, Pandey M, Tripathi BD (2015a) Air pollution tolerance index of climber plant species to develop vertical greenery systems in a polluted tropical city. Landsc Urban Plan 144:119–127
Pandey AK, Pandey M, Mishra A, Tiwary SM, Tripathi BD (2015b) Air pollution tolerance index and anticipated performance index of some plant species for development of urban forest. Urban For Urban Green 14(4):866–871
Pandey AK, Pandey M, Tripathi BD (2016) Assessment of air pollution tolerance index of some plants to develop vertical gardens near street canyons of a polluted tropical city. Ecotoxicol Environ Saf 134(Pt 2):358–364
Pathak V, Tripathi BD, Mishra VK (2011) Evaluation of anticipated performance index of some tree species for green belt development to mitigate traffic generated noise. Urban For Urban Green 10(1):61–66
Putter J (1978) Peroxydase. In: Bergmayer HU (ed) methods of enzymatic analysis, vol 2. Academic, Cambridge, pp 685–690
Rai PK, Panda LLS (2014) Dust capturing potential and air pollution tolerance index (APTI) of some road side tree vegetation in Aizawl, Mizoram, India: an indo-Burma hot spot region. Air Qual Atmos Health 7(1):93–101
Ramakrishna B, Rao SSR (2012) 24-epibrassinolide alleviated zinc-induced oxidative stress in radish ( Raphanus sativus, L.) seedlings by enhancing antioxidative system. Plant Growth Regul 68(2):249–259
Reiter RJ, Tan DX, Osuna C, Gitto E (2000) Actions of melatonin in the reduction of oxidative stress. J Biomed Sci 7(6):444–458
Reiter RJ, Tan DX, Zhou Z, Cruz MH, Fuentesbroto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20:7396–7437
Secretariat O (2011) Environmental effects of ozone depletion and its interactions with climate change: 2002 assessment. Photochem Photobiol Sci 10(2):178–181
Sen DN, Bhandari MC (1978) Ecological and water relation to two Citrullus spp. In: Althawadi AM (ed) Environmental physiology and ecology of plants. Indian arid zone, pp 203–228
Singh SK, Rao DN (1983) Evaluation of plants for their tolerance to air pollution. In: Control IAfAP (ed) Proceedings symposium on air pollution control. New Delhi, India, pp 218–224
Singh SN, Verma A (2007) Phytoremediation of air pollutants: a review. Environmental Bioremediation Technologies. Springer, Berlin p 409-443
Singh SK, Rao DN, Agrawal M, Pandey J, Naryan D (1991) Air pollution tolerance index of plants. J Environ Manag 32(1):45–55
Smith GC, Morin RS, McCaskill GL (2012) Ozone injury to forests across the northeast and north central United States, 1994–2010. Gen. Tech. Rep. NRS-103. U.S. Department of Agriculture, Forest Service, Northern Research Station, Newtown Square 46 p
Suganthi. P, Ganeshkumar RS, Govindaraju M, Selvaraj M, Kumar P (2013) Estimation of biochemical characters of plants in response to vechicular air pollution stress in Tiruchirappalli city corporation, Tamil Nadu, India. J Exp Biol 203(8):3425–3434
Sun J, Wang Y, Chen X, Gong X, Wang N, Ma L, Qiu Y, Wang Y, Feng S (2017) Effects of methyl jasmonate and abscisic acid on anthocyanin biosynthesis in callus cultures of red-fleshed apple ( Malus sieversii, f. niedzwetzkyana ). Plant Cell Tissue Organ Cult 130(2):227–237
Wan W, Manning WJ, Wang X, Zhang H, Sun X, Zhang Q (2014) Ozone and ozone injury on plants in and around Beijing, China. Environ Pollut 191(1):215–222
Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. J Plant Growth Regul 18(3):127–134
Wang XL, & Chen QC (1985). Study on monitoring ozone indicator plant of Chaenomeles speciosa. Environmental Research and Monitoring (S1), 44-46
Wang J, Wang Y, Zhao T, Cao Y, Liu Y, Duan M (2011) Effects of ozone on asa-gsh cycle in soybean leaves. Acta Ecol Sin 31(8):2068–2075
Wang J, Geng Q, Xing H, Sun Y, Wang Y, Zhai H et al (2016a) Effects of shading on photosynthesis and reactive oxygen metabolism in Vitis vinifera ‘cabernet sauvignon’ leaves under ozone stress. J Fruit Sci 33(7):823–831
Wang W, Zhang R, Sun Y, Liu J (2016b) Effect of exogenous melatonin on the antioxidant system of cucumber seedlings under nitrate stress. Acta Hortic Sin 43(4):695–703
Wu Y, Jia S (2017) Alleviation effects of melatonin and Ca2+ on melon seedlings under salt stress. Chin J Appl Ecol 28(6):1925–1931
Wu FF, Zheng YF, Wu RJ, Wang JQ (2011) Concentration of O3 at the atmospheric surface affects the changes characters of antioxidant enzyme activities in Triticum aestivum. Acta Ecol Sin 31(14):4019–4026
Xie JQ, Wang XK, Li GX, Zheng QW, Feng ZZ (2009) Effects of ozone on growth of rice and prevention of exogenous ascorbic acid. J Agro Environ Sci 28(6):1235–1239
Yang H, Yan S, Chen H, Yang C, Yang F, Liu Z (2011) Effect of exogenous methyl jasmonate, calcium and salicylic acid on the heat tolerance in phalaenopsis seedlings under high temperature stress. Chin Agric Sci Bull 27(28):150–157
Yang Y, Chang D, Wang Y, Xueyan Z, Fuguang LI, Zhang F (2015) Effects of ja and meja pretreatment on seed germination and seedling physiological characteristics of Gossypium hirsutum under drought stress. Acta Botan Boreali-Occiden Sin 35(2):302–308
Yang XL, Xu H, Li T, Wang R (2017) Effects of exogenous melatonin on photosynthesis of tomato leaves under drought stress. Sci Agric Sin 50(16):3186–3195
Ye X (2015) Effect of methyl jasmonate on the peroxidation and related antioxidant enzymes of kiwi seedlings under high temperature stress. Jiangsu Agric Sci 43(5):173–175
Zhang WW, Niu JF, Wang XK, Tian Y, Yao FF, Feng ZZ (2011) Effects of elevated ozone concentration on slash pine (Pinus elliottii) seedlings. Environ Sci 32(6):1710–1716
Zhang PQ, Liu YJ, Xing C, Zheng Y, Zhu MH, Li YP (2016) Pollution resistance assessment of existing landscape plants on Beijing streets based on air pollution tolerance index method. Ecotoxicol Environ Saf 132:212–223
Zhao Q, Dai S (2012) Salt-responsive mechanisms in the plant root revealed by proteomic analyses. Acta Ecol Sin 32(1):274–283
Zheng QW, Wang XK, Feng ZZ, Song WZ, Feng ZW (2005) Ozone effects on chlorophyll content and lipid peroxidation in the in situ leaves of winter wheat. Acta Botan Boreali-Occiden Sin 25(11):2240–2244
Zheng QW, Wang XK, Xie JQ, Feng ZZ, Feng ZW, Ni XW et al (2006) Effects of exogenous ascorbate acid on membrane protective system of in situ rice leaves under o3 stress. Acta Ecol Sin 26(4):1131–1137
Zhou Y, Wen Z, Zhang J, Chen X, Cui J, Xu W, Liu HY (2017) Exogenous glutathione alleviates salt-induced oxidative stress in tomato seedlings by regulating glutathione metabolism, redox status, and the antioxidant system. Sci Hortic 220:90–101
Zhu Y, Meng X, Gai W, Liu Y, Shi C, Zhang Y et al (2017) Effects of salt stress on antioxidant enzymes and osmotic adjustment substances of winter wheat. Chin Agric Sci Bull 33(19):1–6
Zou QC, Zhu KY, Liu HC, Zhou JH (2011) Effect of exogenous methyl jasmonate on chlorophyll fluorescence and antioxidant characteristics in the leaves of Phalaenopsis amabilis under abiotic stress. Plant Physiol J 47(9):913–917
Funding
The work was supported by grants from the National Natural Science Foundation of China (CN) (31730080) and the National Key Research and Development Project (2016YFC0501505).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Yanfen Qiu and Kai An are co-first authors.
Electronic supplementary material
ESM 1
(DOC 435 kb)
Rights and permissions
About this article
Cite this article
Qiu, Y., An, K., Sun, J. et al. Investigating the effect of methyl jasmonate and melatonin on resistance of Malus crabapple ‘Hong Jiu’ to ozone stress. Environ Sci Pollut Res 26, 27761–27768 (2019). https://doi.org/10.1007/s11356-019-05946-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05946-w