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Investigating the effect of methyl jasmonate and melatonin on resistance of Malus crabapple ‘Hong Jiu’ to ozone stress

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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.’

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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

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts, polyphénoloxidase in Beta vulgaris. Plant Physiol 24:1–13

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287

    Article  CAS  Google Scholar 

  • Besada A (1987) A facile and sensitive spectrophotometric determination of ascorbic acid. Talanta 34(8):731–732

    Article  CAS  Google Scholar 

  • Cheong JJ, Choi YD (2003) Methyl jasmonate as a vital substance in plants. Trends Genet 19(7):409–413

    Article  CAS  Google Scholar 

  • Ding F, Liu B, Zhang S (2017) Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci Hortic 219:264–271

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Fishman J (1991) The global consequences of increasing tropospheric ozone concentrations. Chemosphere 22(7):685–695

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Gong B, Shi QH (2017) Review of melatonin in horticultural crops. Sci Agric Sin 50(12):2326–2337

    Google Scholar 

  • 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

    Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: i. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125(1):189–198

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ji YY, Hamayun M, Lee SK, Lee IJ (2009) Methyl jasmonate alleviated salinity stress in soybean. J Crop Sci Biotechnol 12(2):63–68

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Krishnaveni M (2013) Air pollution tolerance index and antioxidant activity of Parthenium hysterophorus. J Pharm Res 7(4):296–298

    CAS  Google Scholar 

  • Kruger NJ (1994) The Bradford method for protein quantitation. Methods Mol Biol 32(32):9

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lie GW, Guo SH, Xue L (2014a) Effects of ozone stress on plant growth. Ecol Sci 33(3):607–612

    Google Scholar 

  • Lie GW, Ye LH, Xue L (2014b) Effects of ozone stress on major plant physiological functions. Acta Ecol Sin 34(2):294–306

    CAS  Google Scholar 

  • Liu RK, Shen YW, Liu XJ (1983) A study on physiological responses of plant to SO2. Plant Physiol Commun 4:25–28

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Putter J (1978) Peroxydase. In: Bergmayer HU (ed) methods of enzymatic analysis, vol 2. Academic, Cambridge, pp 685–690

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Reiter RJ, Tan DX, Zhou Z, Cruz MH, Fuentesbroto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20:7396–7437

    Article  CAS  Google Scholar 

  • Secretariat O (2011) Environmental effects of ozone depletion and its interactions with climate change: 2002 assessment. Photochem Photobiol Sci 10(2):178–181

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Book  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wang SY (1999) Methyl jasmonate reduces water stress in strawberry. J Plant Growth Regul 18(3):127–134

    Article  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhao Q, Dai S (2012) Salt-responsive mechanisms in the plant root revealed by proteomic analyses. Acta Ecol Sin 32(1):274–283

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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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).

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Correspondence to Yanling Wang.

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Yanfen Qiu and Kai An are co-first authors.

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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

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