Melatonin plays a pivotal role in conferring tolerance against endoplasmic reticulum stress via mitogen-activated protein kinases and bZIP60 in Arabidopsis thaliana
Melatonin confers ER stress tolerance
Keywords:
ER chaperones, melatonin, mitogen-activated protein kinase, protein folding capacity, unfolded protein response
Abstract
Melatonin has diverse roles as a signaling molecule that activates a number of downstream defense systems against various biotic and abiotic stresses in plants. However, there have been no reports regarding a direct protective role of melatonin against endoplasmic reticulum (ER) stress. Here, we report that exogenous melatonin treatment attenuated ER stress damage by preserving ER structure and enhancing secretory protein folding capacity in response to tunicamycin treatment. Further transgenic experiments indicated that melatonin-deficient snat1 mutant was hypersensitive to ER stress, whereas melatonin-proficient SNAT1 overexpression (OE) was tolerant to ER stress, as evidenced by reduced ion leakage and higher transcript levels of ER chaperones, including luminal binding protein (BIP) 2, BIP3, and CNX1, compared to wild-type controls. Moreover, this melatonin-mediated ER stress tolerance was dependent on the bZIP60 transcription factor and mitogen-activated protein kinase. Our data suggest that melatonin is actively involved in maintaining homeostasis of the ER during normal plant growth, and also has a protective effect against many environmental stressors that induce ER stress.
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2. Byeon Y, Lee K, Park YI, Park S, Back K (2013) Molecular cloning and functional analysis of serotonin N-acetyltransferase from the cyanobacterium Synechocystis sp. PCC 6803. J. Pineal Res. 55: 371-376.
3. Kobylińska A, Reiter RJ, Posmyk MM (2017) Melatonin protects cultured tobacco cells against lead-induced cell death via inhibition of cytochrome C translocation. Front. Plant Sci. 8: 1560.
4. Lee K, Back K (2017) Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield. J. Pineal Res. 62: e12392.
5. Hwang OJ, Back K (2018) Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in plants. J. Pineal Res. 65: e12495.
6. Lee HY, Byeon Y, Tan DX, Reiter RJ, Back K (2015) Arabidopsis serotonin N-acetyltransferase knockout plants exhibit decreased melatonin and salicylic acid levels resulting in susceptibility to an avirulent pathogen. J. Pineal Res. 58: 291-299.
7. Wang Y, Reiter RJ, Chan Z (2018) Phytomelatonin: a universal abiotic stress regulator. J. Exp. Bot. 69: 963-974.
8. Zhang S, Liu S, Zhang J, Reiter RJ, Wang Y, Qiu D, Luo X, Khalid AR, Wang H, Feng L, Lin Z, Ren M (2018) Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease. J. Pineal Re.s 65: e12492.
9. Zheng X, Tan DX, Allan AC, Zuo B, Zhao Y, Reiter RJ, Wang L, Wang Z, Guo Y, Zhou J, Shan D, Li Q, Han Z, Kong J (2017) Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Sci. Rep. 7: 41236.
10. Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S, Yuan M (2018) Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiol. Plant 164: 349-363.
11. Zhang J, Shi Y, Zhang X, Du H, Xu B, Huang B (2017) Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ. Exp. Bot. 138: 36-45.
12. Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J (2018) Melatonin alleviates high temperature-induced pollen abortion in Solanum lycopersicum. Molecules 23: 386.
13. Li H, Chang J, Zheng J, Dong Y, Liu Q, Yang X, Wei C, Zhang Y, Ma J, Zhang X (2017) Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci. Rep. 7: 40858.
14. Ding F, Wang M, Liu B, Zhang S (2017) Exogenous melatonin mitigates photoinhibition by accelerating non-photochemical quenching in tomato seedlings exposed to moderate light during chilling. Front. Plant Sci. 8: 244.
15. Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol. Plant 160: 396-409.
16. Wang L, Feng C, Zheng X, Guo Y, Zhou F, Shan D, Liu X, Kong J (2017) Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. J. Pineal Res. 63: e12429.
17. Zhang J, Zeng B, Mao Y, Kong X, Wang X, Yang Y, Zhang J, Xu J, Rengel Z, Chen Q (2017) Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean. Funct. Plant Biol. 44: 961–968.
18. Lee HY, Back K (2018) Melatonin induction and its role in high light stress tolerance in Arabidopsis thaliana. J. Pineal Res. 65: e12504.
19. Liang D, Gao F, Ni Z, Lin L, Deng Q, Tang Y, Wang X, Luo X, Xia H (2018) Melatonin improves heat tolerance in kiwifruits seedlings through promoting antioxidant enzymatic activity and glutathione S-transferase transcription. Molecule 23: 584.
20. Wei J, Li DX, Zhang JR, Shan C, Rengel Z, Song ZB, Chen Q (2018) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J. Pineal Res. 65: e12500.
21. Suofu Y, Li W, Jean-Alphonse FG, et al. (2017) Dual role of mitochondria in producing melatonin and driving GPCR signaling to block cytochrome c release. Proc. Natl. Acad. Sci. USA 114: E7997-E8006.
22. Arnao MB, Hernández-Ruiz J (2018) Melatonin and its relationship to pant hormones. Ann. Bot. 121: 195-207.
23. Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Galpha protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J. 82: 280-301.
24. Choi SI, Kim KS, Oh JY, Jin JY, Lee GH, Kim EK (2013) Melatonin induces autophagy via an mTOR-dependent pathway and enhances clearance of mutant-TGFBIp. J. Pineal Res. 54: 361-372.
25. Fernández A, Ordónez R, Reiter RJ, González-Gallego J, Mauriz JL (2015) Melatonin and endoplasmic reticulum stress: relation to autophagy and apoptosis. J. Pineal Res. 59: 292-307.
26. Wang P, Sun X, Wang N, Tan DX, Ma F (2015) Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J. Pineal Res. 58: 479-489.
27. Pu Y, Bassham DC (2013) Links between ER stress and autophagy in plants. Plant Signal Behav, 8: e24297.
28. Nawkar GM, Lee ES, Shelake RM, Park JH, Ryu SW, Kang CH, Lee SY (2018) Activation of the transducers of unfolded protein response in plants. Front. Plant Sci. 9: 214
29. Lee HY, Back K (2016) Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. J. Pineal Res. 60: 327-335.
30. Sagor GHM, Chawla P, Kim DW, Berberich T, Kojima S, Niitsu M, Kusano T (2015) The poluamine spermidine induces the unfolded protein response via the MAPK cascade in Arabidopsis. Front. Plant Sci. 6: 687.
31. Lee HY, Back K (2017) Melatonin is required for H2O2-and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J. Pineal Res. 62: e12379.
32. Hong Z, Jin H, Tzfira T, Li J (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20: 3418-3429.
33. Lee HY, Bowen CH, Popescu GV, Kang HG, Kato N, Ma S, Dinesh-Kumar S, Snyder M, Popescu SC (2011) Arabidopsis RTNLB1 and RTNLB2 reticulon-like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell 23: 3374-3391.
34. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 15: 764-767.
35. Kang K, Lee K, Park S, Kim YS, Back K (2010) Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings. J. Pineal Res. 49: 176-182.
36. Szarka A, Tomasskovics B, Bánhegyi G (2012) The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int. J. Mol. Sci. 13: 4458-4483.
37. Byeon Y, Lee HY, Hwang OJ, Lee HJ, Lee K, Back K (2015). Coordinated regulation of melatonin synthesis and degradation genes in rice leaves in response to cadmium treatment. J. Pineal Res. 58: 470-478.
38. Galano A, Reiter RJ (2018) Melatonin and its metabolites vs oxidative stress: From individual actions to collective protection. J. Pineal Res. 65: e12514.
39. Lee K, Choi GH, Back K (2017) Cadmium-induced melatonin synthesis in rice requires light, hydrogen peroxide, and nitric oxide: key regulatory roles for tryptophan decarboxylase and caffeic acid O-methyltransferase. J. Pineal Res. 63: e12441.
Published
2018-12-03
How to Cite
[1]
Lee, H. and Back, K. 2018. Melatonin plays a pivotal role in conferring tolerance against endoplasmic reticulum stress via mitogen-activated protein kinases and bZIP60 in Arabidopsis thaliana. Melatonin Research. 1, 1 (Dec. 2018), 94-108. DOI:https://doi.org/https://doi.org/10.32794/mr11250006.
Section
Research Articles
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