Celastrol, produced by Tripterygium wilfordii Hook F. enhances defense response in cucumber seedlings against diverse environmental stresses

Journal of Plant Biology - Tập 60 - Trang 82-92 - 2017
Li-jun Zhu1,2, Xing-guang Deng1, Li-juan Zou1,2, Peng-xu Li1, Jun-qiang Wu1, Da-wei Zhang1, Honghui Lin1
1Ministry of Education Key Laboratory for Bio-Resource and Eco-Environment, College of Life Science, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, China
2Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang Sichuan, China

Tóm tắt

Celastrol is an active triterpenoid compound isolated from Tripterygium wilfordii Hook F.. Many reports have highlighted that celastrol is an effective, safe and desirable approach to the treatment of cancers. However, their biological function during environmental stresses in plants is rarely reported. In the present study, the effects of celastrol on the tolerance against high light (HL), polyethylene glycol (PEG) and cold stress in cucumber (Cucumis sativus L.) were investigated. Celastrol pretreatment could enhance cucumber seedlings stress tolerance at a concentration of 1 μg ml–1. The results showed that pretreatment with 1 μg ml–1 celastrol clearly induced the activities of antioxidative enzymes, which subsequently alleviated stress-induced oxidative damage in plant cells. We also provided evidence that celastrol upregulated ABA biosynthetic gene NCED2 expression and ABA accumulation in cucumber seedlings, which resulted to the enhanced tolerance in response to environmental stresses. Furthermore, the celastrol-pretreated seedlings showed less photosystem damaged caused by the stress conditions, when compared with the control. Therefore, our findings provide a novel role of celastrol in plant against environmental stresses and indicate that the celastrol-induced activities of antioxidative enzymes and ABA content might contribute to the stress tolerance.

Tài liệu tham khảo

Allison AC, Cacabelos R, Lombardi VRM, Alvarez XA, Vigo C (2001) Celastrol, a potent antioxidant and anti-inflammatory drug, as a possible treatment for Alzheimer’s disease. Prog Neuro-Psychoph 25:1341–1357 Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399 Cao Y, Zhang ZW, Xue LW, Du JB, Shang J, Xu F, Yuan S, Lin HH (2008) Lack of salicylic acid in Arabidopsis protects plants against moderate salt stress. Z Naturforsch C 64:231–238 Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357 Dong CJ, Li L, Shang QM, Liu XY, Zhang ZG (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240:687–700 Du JB, Yuan S, Chen YE, Sun X, Zhang ZW, Xu F, Yuan M, Shang J, Lin HH (2011) Comparative expression analysis of dehydrins between two barley varieties, wild barley and Tibetan hulless barley associated with different stress resistance. Acta Physiol Plant 33:567–574 Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905 Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442 Galvez-Valdivieso G, Fryer MJ, Lawson T, Slattery K, Truman W, Smirnoff N, Asami T, Davies WJ, Jones AM, Baker NR (2009) The high light response in Arabidopsis involves ABA signaling between vascular and bundle sheath cells. Plant Cell 21:2143–2162 Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. BBA-Gen Subj 990:87–92 Gilbert N (2012) Drought devastates US crops. Nature: 11065. doi:10.1038/nature.2012.11065 Hsieh EJ, Cheng MC, Lin TP (2013) Functional characterization of an abiotic stress-inducible transcription factor AtERF53 in Arabidopsis thaliana. Plant Mol Biol 82:223–237 Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68 Hu XL, Liu RX, Li YH, Wang W, Tai FJ, Xue RL, Li CH (2010) Heat shock protein 70 regulates the abscisic acid-induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul 60:225–235 Huang Y, Zhou Y, Fan Y, Zhou D (2008) Celastrol inhibits the growth of human glioma xenografts in nude mice through suppressing VEGFR expression. Cancer Lett 264:101–106 Julliard J, Maldiney R, Sotta B, Miginiac E, Kerhoas L, Einhorn J (1994) HPLC-ELISA and MS as complementary techniques to study plant hormone metabolites. Analusis 22:483–489 Kannaiyan R, Manu KA, Chen LX, Li F, Rajendran P, Subramaniam A (2011) Celastrol inhibits tumor cell proliferation and promotes apoptosis through the activation of c-Jun N-terminal kinase and suppression of PI3 K/Akt signaling pathways. Apoptosis 16:1028–1041 Kim DY, Park JW, Jeoung D, Ro JY (2009) Celastrol suppresses allergen-induced airway inflammation in a mouse allergic asthma model. Eur J Pharmacol 612:98–105 Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897 Larkindale J, Knight MR (2002) Protection against heat stressinduced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128: 682–695 Law M, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleracea) chloroplasts.The effect of hydrogen peroxide and of Paraquat. Biochem J 210:899–903 Lee JH, Won YS, Park KH, Lee MK, Tachibana H, Yamada K, Seo K (2012) Celastrol inhibits growth and induces apoptotic cell death in melanoma cells via the activation ROS-dependent mitochondrial pathway and the suppression of PI3K/AKT signaling. Apoptosis 17:1275–1286 Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60 Lei T, Feng H, Sun X, Dai QL, Zhang F, Liang HG, Lin HH (2010) The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul 60:35–42 Li HY, Zhang J, Sun LL, Li BH, Gao HL, Xie T, Zhang N, Ye ZM (2015) Celastrol induces apoptosis and autophagy via the ROS/ JNK signaling pathway in human osteosarcoma cells: an in vitro and in vivo study. Cell Death Dis 6:e1604 Li H, Zhang YY, Huang XY, Sun YN, Jia YF, Li D (2005) Beneficial effect of tripterine on systemic lupus erythematosus induced by active chromatin in BALB/c mice. Eur J Pharmacol 512:231–237 Lu S, SuW, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermuda grass and involves H2O2- and NOinduced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138 Møller IM, Bérczi A, Plas LH, Lambers H (1988) Measurement of the activity and capacity of the alternative pathway in intact plant tissues: identification of problems and possible solutions. Physiol Plantarum 72:642–649 Møller IM, Sweetlove LJ (2010) ROS signalling–specificity is required. Trends Plant Sci 15:370–374 Peng B, Xu LM, Cao FF, Wei TX, Yang CX, Uzan G, Zhang DH (2010) HSP90 inhibitor, celastrol, arrests human leukemia cell U937 at G0/G1 in thiol-containing agents reversible way. Mol Cancer 9:79 Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell 6:65–74 Qiu D, Kao PN (2003) Immunosuppressive and anti-inflammatory mechanisms of triptolide, the principal active diterpenoid from the Chinese medicinal herb Tripterygium wilfordii Hook. F. Drugs R D 4:1–18 Sethi G, Ahn KS, Pandey MK, Aggarwal BB (2007) Celastrol, a novel triterpene, potentiates TNF-induced apoptosis and suppresses invasion of tumor cells by inhibiting NF-kappaB regulated gene products and TAK1-mediated NF-kappaB activation. Blood 109:2727–2735 Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248 Tao X, Younger J, Fan FZ, Wang B, Lipsky PE (2002) Benefit of an extract of Tripterygium Wilfordii Hook F. in patients with rheumatoid arthritis: A double-blind, placebo-controlled study. Arthritis Rheum 46:1735–1743 Tao XL, Cush JJ, Garret M, Lipsky PE (2001) A phase I study of ethyl acetate extract of the Chinese antirheumatic herb Tripterygium wilfordii Hook F. in rheumatoid arthritis. J Rheumatol 28:2160–2167 Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403 Varshney RK, Ribaut JM, Buckler ES, Tuberosa R, Rafalski JA, Langridge P (2012) Can genomics boost productivity of orphan crops? Nat Biotechnol 30:1172–1176 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 Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291 Wang CY, Shi CF, Yang XP, Yang M, Sun HL, Wang CH (2014) Celastrol suppresses obesity process via increasing antioxidant capacity and improving lipid metabolism. Eur J Pharmacol 744:52–58 Wang SD, Zhu F, Yuan S, Yang H, Xu F, Shang J, Xu MY, Jia SD, Zhang ZW, Wang JH, Xi DH, Lin HH (2011) The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234:171–181 Wang SY, Jiao HJ, Faust M (1991) Changes in ascorbate, glutathione, and related enzyme activities during thidiazuron induced bud break of apple. Physiol Plantarum 82:231–236 Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525 Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami TD, Chen ZX, Yu JQ (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814 Xu F, Zhang DW, Zhu F, Tang H, Lv X, Cheng J, Xie H.F., Lin HH (2012) A novel role for cyanide in the control of cucumber (Cucumis sativus L.) seedlings response to environmental stress. Plant Cell Environ 35:1983–1997 Zhang KM, Yu HJ, Shi K, Zhou YH, Yu JQ, Xia XJ (2010) Photoprotective roles of anthocyanins in Begonia semperflorens. Plant Sci 179:202–208 Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448 Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:23