Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants - PubMed (original) (raw)
. 2016 Nov;61(4):457-469.
doi: 10.1111/jpi.12359. Epub 2016 Aug 19.
Affiliations
- PMID: 27484733
- DOI: 10.1111/jpi.12359
Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants
Wen Xu et al. J Pineal Res. 2016 Nov.
Abstract
Melatonin is a pleiotropic signaling molecule that provides physiological protection against diverse environmental stresses in plants. Nonetheless, the mechanisms for melatonin-mediated thermotolerance remain largely unknown. Here, we report that endogenous melatonin levels increased with a rise in ambient temperature and that peaked at 40°C. Foliar pretreatment with an optimal dose of melatonin (10 μmol/L) or the overexpression of N-acetylserotonin methyltransferase (ASMT) gene effectively ameliorated heat-induced photoinhibition and electrolyte leakage in tomato plants. Both exogenous melatonin treatment and endogenous melatonin manipulation by overexpression of ASMT decreased the levels of insoluble and ubiquitinated proteins, but enhanced the expression of heat-shock proteins (HSPs) to refold denatured and unfolded proteins under heat stress. Meanwhile, melatonin also induced expression of several ATG genes and formation of autophagosomes to degrade aggregated proteins under the same stress. Proteomic profile analyses revealed that protein aggregates for a large number of biological processes accumulated in wild-type plants. However, exogenous melatonin treatment or overexpression of ASMT reduced the accumulation of aggregated proteins. Aggregation responsive proteins such as HSP70 and Rubisco activase were preferentially accumulated and ubiquitinated in wild-type plants under heat stress, while melatonin mitigated heat stress-induced accumulation and ubiquitination of aggregated proteins. These results suggest that melatonin promotes cellular protein protection through induction of HSPs and autophagy to refold or degrade denatured proteins under heat stress in tomato plants.
Keywords: N-acetylserotonin methyltransferase; autophagy; heat-shock proteins; melatonin; protein protection; thermotolerance; tomato.
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Similar articles
- Melatonin Alleviates High Temperature-Induced Pollen Abortion in Solanum lycopersicum.
Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J. Qi ZY, et al. Molecules. 2018 Feb 11;23(2):386. doi: 10.3390/molecules23020386. Molecules. 2018. PMID: 29439470 Free PMC article. - SlSNAT Interacts with HSP40, a Molecular Chaperone, to Regulate Melatonin Biosynthesis and Promote Thermotolerance in Tomato.
Wang X, Zhang H, Xie Q, Liu Y, Lv H, Bai R, Ma R, Li X, Zhang X, Guo YD, Zhang N. Wang X, et al. Plant Cell Physiol. 2020 May 1;61(5):909-921. doi: 10.1093/pcp/pcaa018. Plant Cell Physiol. 2020. PMID: 32065633 - Melatonin mediates elevated carbon dioxide-induced photosynthesis and thermotolerance in tomato.
Hasan MK, Xing QF, Zhou CY, Wang KX, Xu T, Yang P, Qi ZY, Shao SJ, Ahammed GJ, Zhou J. Hasan MK, et al. J Pineal Res. 2023 Apr;74(3):e12858. doi: 10.1111/jpi.12858. Epub 2023 Feb 15. J Pineal Res. 2023. PMID: 36732033 - HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants.
Cai SY, Zhang Y, Xu YP, Qi ZY, Li MQ, Ahammed GJ, Xia XJ, Shi K, Zhou YH, Reiter RJ, Yu JQ, Zhou J. Cai SY, et al. J Pineal Res. 2017 Mar;62(2). doi: 10.1111/jpi.12387. Epub 2017 Feb 10. J Pineal Res. 2017. PMID: 28095626 - Phytomelatonin as a signaling molecule for protein quality control via chaperone, autophagy, and ubiquitin-proteasome systems in plants.
Lee HY, Hwang OJ, Back K. Lee HY, et al. J Exp Bot. 2022 Sep 30;73(17):5863-5873. doi: 10.1093/jxb/erac002. J Exp Bot. 2022. PMID: 35246975 Review.
Cited by
- Physiological and Gene Expression Changes of Clematis crassifolia and Clematis cadmia in Response to Heat Stress.
Hu Q, Qian R, Zhang Y, Zhang X, Ma X, Zheng J. Hu Q, et al. Front Plant Sci. 2021 Mar 26;12:624875. doi: 10.3389/fpls.2021.624875. eCollection 2021. Front Plant Sci. 2021. PMID: 33841457 Free PMC article. - Autophagy in the Lifetime of Plants: From Seed to Seed.
Wang S, Hu W, Liu F. Wang S, et al. Int J Mol Sci. 2022 Sep 27;23(19):11410. doi: 10.3390/ijms231911410. Int J Mol Sci. 2022. PMID: 36232711 Free PMC article. Review. - Analysis of the ASMT Gene Family in Pepper (Capsicum annuum L.): Identification, Phylogeny, and Expression Profiles.
Pan L, Zheng J, Liu J, Guo J, Liu F, Liu L, Wan H. Pan L, et al. Int J Genomics. 2019 Apr 2;2019:7241096. doi: 10.1155/2019/7241096. eCollection 2019. Int J Genomics. 2019. PMID: 31065551 Free PMC article. - Melatonin Alleviates High Temperature-Induced Pollen Abortion in Solanum lycopersicum.
Qi ZY, Wang KX, Yan MY, Kanwar MK, Li DY, Wijaya L, Alyemeni MN, Ahmad P, Zhou J. Qi ZY, et al. Molecules. 2018 Feb 11;23(2):386. doi: 10.3390/molecules23020386. Molecules. 2018. PMID: 29439470 Free PMC article. - Overexpression of ovine AANAT and HIOMT genes in switchgrass leads to improved growth performance and salt-tolerance.
Huang YH, Liu SJ, Yuan S, Guan C, Tian DY, Cui X, Zhang YW, Yang FY. Huang YH, et al. Sci Rep. 2017 Sep 22;7(1):12212. doi: 10.1038/s41598-017-12566-2. Sci Rep. 2017. PMID: 28939842 Free PMC article.
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources