Abstract
Jasmonic acid (JA), which is an important phytohormone, plays a key role in plant growth, development and stress responses. Here, Malus baccata Borkh. seedlings were used to study the mechanism by which JA alleviates the oxidative damage induced by low root-zone temperature (5 °C) through regulating the ascorbate–glutathione (AsA–GSH) cycle. The roots of M. baccata Borkh. were subjected to three treatments [5 °C, 5 °C + JA, and 5 °C + ibuprofen (IBU)] for 0, 12, 24, and 48 h. The results showed that treatment with low root-zone temperature could modulate the non-enzymatic and enzymatic components of the AsA–GSH cycle, significantly inducing the accumulation of MDA and H2O2. Additionally, the endogenous JA content changed dramatically, and the expression levels of the related genes [lipoxygenase (LOX), allene oxide synthase (AOS), and allene oxide cyclase (AOC)] showed different trends. In plants pretreated with JA, the endogenous JA content increased at 24 h, and the gene expression levels of LOX, AOS, and AOC were upregulated. We also found a marked increase in the activities of antioxidant enzymes [ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), and glutathione reductase (GR)], a decrease in oxidized glutathione (GSSG) and an increased GSH/GSSG ratio, which resulted in lower MDA and H2O2 contents. Thus, the oxidative stress was alleviated. Plants pretreated with IBU experienced an opposite effect on the function of the AsA–GSH cycle and the gene expression in the JA synthesis route relative to those subjected to exogenous JA treatment, indicating that endogenous JA can alleviate oxidative damage by regulating the function of the AsA–GSH cycle under low root-zone temperature.
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References
Agrawal GK, Jwa N-S, Agrawal SK, Tamogami S, Iwahashi H, Rakwal R (2003) Cloning of novel rice allene oxide cyclase (OsAOC): mRNA expression and comparative analysis with allene oxide synthase (OsAOS) gene provides insight into the transcriptional regulation of octadecanoid pathway biosynthetic genes in rice. Plant Sci 164:979–992. doi:10.1016/S0168-9452(03)00082-7
Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, LA Del RÍO, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295. doi:10.1111/j.1365-3040.2011.02310.x
Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, Li Z, Kinoshita T, Ecker JR, Schroeder JI (2016) An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci Rep 6:28941. doi:10.1038/srep28941
Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350. doi:10.1016/j.jplph.2010.05.012
Bankaji I, Sleimi N, López-Climent MF, Perez-Clemente RM, Gomez-Cadenas A (2014) Effects of combined abiotic stresses on growth, trace element accumulation, and phytohormone regulation in two halophytic species. J Plant Growth Regul 33:632–643. doi:10.1007/s00344-014-9413-5
Cai Y, Cao S, Yang Z, Zheng Y (2011) MeJA regulates enzymes involved in ascorbic acid and glutathione metabolism and improves chilling tolerance in loquat fruit. Postharvest Biol Technol 59:324–326. doi:10.1016/j.postharvbio.2010.08.020
Cao S, Zheng Y, Wang K, Jin P, Rui H (2009) Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem 115:1458–1463. doi:10.1016/j.foodchem.2009.01.082
Chen L, Han Y, Jiang H, Korpelainen H, Li C (2011) Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot 62(14):5037–5050. doi:10.1093/jxb/err203
Chen J, Yan Z, Li X (2014a) Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf 104:349–356. doi:10.1016/j.ecoenv.2014.01.022
Chen LJX, Xiang HZ, Miao Y, Zhang L, Guo ZF, Zhao XH, Lin JW, Li TL (2014b) An overview of cold resistance in plants. J Agron Crop Sci 200:237–245. doi:10.1111/jac.12082
Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate–glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877. doi:10.1074/jbc.M307525200
Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. doi:10.1146/annurev.arplant.48.1.355
De Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147(3):296–306. doi:10.1111/j.1399-3054.2012.01659.x
Du H, Liu H, Xiong L (2013) Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Front Plant Sci 4:397. doi:10.3389/fpls.2013.00397
Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography–electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442. doi:10.1021/jf050884b
Edwards EA, Rawsthorne S, Mullineaux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284. doi:10.1007/bf00194008
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. doi:10.1104/pp.110.167569
Gambino G, Perrone I, Gribaudo I (2008) A Rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19:520–525. doi:10.1002/pca.1078
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016
Hanaka A, Wójcik M, Dresler S, Mroczek-Zdyrska M, Maksymiec W (2016) Does methyl jasmonate modify the oxidative stress response in Phaseolus coccineus treated with Cu? Ecotoxicol Environ Saf 124:480–488. doi:10.1016/j.ecoenv.2015.11.024
He J, Qin J, Long L, Ma Y, Li H, Li K, Jiang X, Liu T, Polle A, Liang Z, Luo Z-B (2011) Net cadmium flux and accumulation reveal tissue-specific oxidative stress and detoxification in Populus × canescens. Physiol Plant 143:50–63. doi:10.1111/j.1399-3054.2011.01487.x
He Y, Yang J, Zhu B, Zhu Z-J (2014) Low root zone temperature exacerbates the ion imbalance and photosynthesis inhibition and induces antioxidant responses in tomato plants under salinity. J Integr Agric 13:89–99. doi:10.1016/S2095-3119(13)60586-9
Hu FX, Zhong JJ (2008) Jasmonic acid mediates gene transcription of ginsenoside biosynthesis in cell cultures of Panax notoginseng treated with chemically synthesized 2-hydroxyethyl jasmonate. Process Biochem 43:113–118. doi:10.1016/j.procbio.2007.10.010
Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression–c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924. doi:10.1105/tpc.113.112631
Jiang M, Xu F, Peng M, Huang F, Meng F (2016) Methyl jasmonate regulated diploid and tetraploid black locust (Robinia pseudoacacia L.) tolerance to salt stress. Acta Physiol Plant 38:106. doi:10.1007/s11738-016-2120-z
Jin P, Duan Y, Wang L, Wang J, Zheng Y (2014) Reducing chilling injury of loquat fruit by combined treatment with hot air and methyl jasmonate. Food Bioprocess Technol 7:2259–2266. doi:10.1007/s11947-013-1232-3
Kamal AHM, Komatsu S (2016) Jasmonic acid induced protein response to biophoton emissions and flooding stress in soybean. J Proteom 133:33–47. doi:10.1016/j.jprot.2015.12.004
Kaya A, Doganlar ZB (2016) Exogenous jasmonic acid induces stress tolerance in tobacco (Nicotiana tabacum) exposed to imazapic. Ecotoxicol Environ Saf 124:470–479. doi:10.1016/j.ecoenv.2015.11.026
Kim JK, Bamba T, Harada K, Fukusaki E, Kobayashi A (2007) Time-course metabolic profiling in Arabidopsis thaliana cell cultures after salt stress treatment. J Exp Bot 58:415–424. doi:10.1093/jxb/erl216
Kuk YI, Shin JS, Burgos NR, Hwang TE, Han O, Cho BH, Jung S, Guh JO (2003) Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci 43:2109–2117. doi:10.2135/cropsci2003.2109
Landhäusser SM, DesRochers A, Lieffers VJ (2001) A comparison of growth and physiology in Picea glauca and Populus tremuloides at different soil temperatures. Can J For Res 31:1922–1929. doi:10.1139/x01-129
Lee SH, Ahn SJ, Im YJ, Cho K, Chung G-C, Cho B-H, Han O (2005) Differential impact of low temperature on fatty acid unsaturation and lipoxygenase activity in figleaf gourd and cucumber roots. Biochem Biophys Res Commun 330:1194–1198. doi:10.1016/j.bbrc.2005.03.098
Li Y, Liu Y, Zhang J (2010) Advances in the research on the AsA–GSH cycle in horticultural crops. Front Agric China 4:84–90. doi:10.1007/s11703-009-0089-8
Li ZG, Yuan LX, Wang QL, Ding ZL, Dong CY (2013) Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol Plant 35:2127–2136. doi:10.1007/s11738-013-1249-2
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Lyr H (1996) Effect of the root temperature on growth parameters of various European tree species. Ann For Sci 53:317–323. doi:10.1051/forest:19960214
Mustafa MA, Ali A, Seymour G, Tucker G (2016) Enhancing the antioxidant content of carambola (Averrhoa carambola) during cold storage and methyl jasmonate treatments. Postharvest Biol Technol 118:79–86. doi:10.1016/j.postharvbio.2016.03.021
Nemchenko A, Kunze S, Feussner I, Kolomiets M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. J Exp Bot 57:3767–3779. doi:10.1093/jxb/erl137
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279. doi:10.1146/annurev.arplant.49.1.249
Peng YY, Dang Q-L (2003) Effects of soil temperature on biomass production and allocation in seedlings of four boreal tree species. For Ecol Manag 180:1–9. doi:10.1016/S0378-1127(02)00486-3
Polle A, Chakrabarti K, Schürmann W, Renneberg H (1990) Composition and properties of hydrogen peroxide decomposing systems in extracellular and total extracts from needles of Norway Spruce (Picea abies L., Karst.). Plant Physiol 94:312–319. doi:10.1104/pp.94.1.312
Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208. doi:10.1016/j.ecoenv.2014.03.014
Rezai S, Orojloo M, Bidabadi SS, Soleimanzadeh M (2013) Possible role of methyl jasmonate in protection to NaCl-induced salt stress in pepper cv. “Green Hashemi”. Int J Agric Crop Sci 6:1235
Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V (2013) Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. Plant Cell Rep 32:1085–1098. doi:10.1007/s00299-013-1441-2
Shan C, Liang Z (2010) Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci 178:130–139. doi:10.1016/j.plantsci.2009.11.002
Sharma M, Laxmi A (2015) Jasmonates: emerging players in controlling temperature stress tolerance. Front Plant Sci 6:1129. doi:10.3389/fpls.2015.01129
Stevens R, Page D, Gouble B, Garchery C, Zamir D, Causse M (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31:1086–1096. doi:10.1111/j.1365-3040.2008.01824.x
Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105. doi:10.1007/s00425-012-1641-y
Tittarelli A, Santiago M, Morales A, Meisel LA, Silva H (2009) Isolation and functional characterization of cold-regulated promoters, by digitally identifying peach fruit cold-induced genes from a large EST dataset. BMC Plant Biol 9:121. doi:10.1186/1471-2229-9-121
Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164. doi:10.1105/tpc.000679
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 Sci 151:59–66. doi:10.1016/S0168-9452(99)00197-1
Wang CY, Buta JG (1994) Methyl jasmonate reduces chilling injury in Cucurbita pepo through its regulation of abscisic acid and polyamine levels. Environ Exp Bot 34:427–432. doi:10.1016/0098-8472(94)90025-6
Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697. doi:10.1093/aob/mcm079
Yang X-Y, Jiang W-J, Yu H-J (2012) The expression profiling of the Lipoxygenase (LOX) family genes during fruit development, abiotic stress and hormonal treatments in Cucumber (Cucumis sativus L.). Int J Mol Sci 13:2481–2500. doi:10.3390/ijms13022481
Yang SL, Lan SS, Deng FF, Gong M (2016) Effects of calcium and calmodulin antagonists on chilling stress-induced proline accumulation in Jatropha curcas L. J Plant Growth Regul 35(3):815–826. doi:10.1007/s00344-016-9584-3
Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2013) Induction of jasmonate signalling regulators MaMYC2 s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51. doi:10.1111/j.1365-3040.2012.02551.x
Ziegler J, Keinänen M, Baldwin IT (2001) Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry 58:729–738. doi:10.1016/S0031-9422(01)00284-9
Acknowledgements
This work was funded by the China Agriculture Research System (Grant Number CARS-28), Institutions of Higher Learning Fruit Tree Cultivation and Physio-Ecology Innovation Team of Liaoning Province (Grant Number LT2014014), Science and Technology Research Projects for Apple of Liaoning Province (Grant Number 2014204004), the National Science and Technology Plan “twelfth five-year “ in rural areas (2014BAD10B02-1).
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Communicated by L. A. Kleczkowski.
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Li, L., Lu, X., Ma, H. et al. Jasmonic acid regulates the ascorbate–glutathione cycle in Malus baccata Borkh. roots under low root-zone temperature. Acta Physiol Plant 39, 174 (2017). https://doi.org/10.1007/s11738-017-2469-7
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DOI: https://doi.org/10.1007/s11738-017-2469-7