Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants

Wen Xu, Shu Yu Cai, Yun Zhang, Yu Wang, Golam Jalal Ahammed, Xiao Jian Xia, Kai Shi, Yan Hong Zhou, Jing Quan Yu, Russel J Reiter, Jie Zhou

Research output: Contribution to journalArticle

61 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)457-469
Number of pages13
JournalJournal of Pineal Research
Volume61
Issue number4
DOIs
StatePublished - Nov 1 2016

Fingerprint

Melatonin
Lycopersicon esculentum
Acetylserotonin O-Methyltransferase
Proteins
Hot Temperature
Heat-Shock Proteins
Thermotolerance
Ubiquitinated Proteins
Protein Refolding
Ribulose-Bisphosphate Carboxylase
Biological Phenomena
Protein Unfolding
Ubiquitination
Autophagy
Tissue Plasminogen Activator
Proteomics
Electrolytes
Genes
Temperature

Keywords

  • autophagy
  • heat-shock proteins
  • melatonin
  • N-acetylserotonin methyltransferase
  • protein protection
  • thermotolerance
  • tomato

ASJC Scopus subject areas

  • Endocrinology

Cite this

Xu, W., Cai, S. Y., Zhang, Y., Wang, Y., Ahammed, G. J., Xia, X. J., ... Zhou, J. (2016). Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. Journal of Pineal Research, 61(4), 457-469. https://doi.org/10.1111/jpi.12359

Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. / Xu, Wen; Cai, Shu Yu; Zhang, Yun; Wang, Yu; Ahammed, Golam Jalal; Xia, Xiao Jian; Shi, Kai; Zhou, Yan Hong; Yu, Jing Quan; Reiter, Russel J; Zhou, Jie.

In: Journal of Pineal Research, Vol. 61, No. 4, 01.11.2016, p. 457-469.

Research output: Contribution to journalArticle

Xu, W, Cai, SY, Zhang, Y, Wang, Y, Ahammed, GJ, Xia, XJ, Shi, K, Zhou, YH, Yu, JQ, Reiter, RJ & Zhou, J 2016, 'Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants', Journal of Pineal Research, vol. 61, no. 4, pp. 457-469. https://doi.org/10.1111/jpi.12359
Xu, Wen ; Cai, Shu Yu ; Zhang, Yun ; Wang, Yu ; Ahammed, Golam Jalal ; Xia, Xiao Jian ; Shi, Kai ; Zhou, Yan Hong ; Yu, Jing Quan ; Reiter, Russel J ; Zhou, Jie. / Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. In: Journal of Pineal Research. 2016 ; Vol. 61, No. 4. pp. 457-469.
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