Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells

Melatonin, a multifunctional signaling molecule, has been shown to play a significant role in response to abiotic stress. Several species have been reported to unveil melatonin’s effect on osmotic stress; however, the signal transduction mechanism of phytohormone-mediated melatonin biosynthesis in p...

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Main Authors: Manwen Yan, Mingyan Li, Zhuoying Ding, Fei Qiao, Xuefei Jiang
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Horticulturae
Subjects:
Online Access:https://www.mdpi.com/2311-7524/9/8/927
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author Manwen Yan
Mingyan Li
Zhuoying Ding
Fei Qiao
Xuefei Jiang
author_facet Manwen Yan
Mingyan Li
Zhuoying Ding
Fei Qiao
Xuefei Jiang
author_sort Manwen Yan
collection DOAJ
description Melatonin, a multifunctional signaling molecule, has been shown to play a significant role in response to abiotic stress. Several species have been reported to unveil melatonin’s effect on osmotic stress; however, the signal transduction mechanism of phytohormone-mediated melatonin biosynthesis in plant species remains unclear. In this study, although plants can biosynthesize melatonin, the exogenous application of melatonin to watermelon cells can improve cell growth in response to osmotic stress by regulating the antioxidant machinery of cells. Regarding the melatonin synthesis pathway, ClOMT (ClASMT and ClCOMT) is a multi-gene family, and ClSNAT has two members. Both <i>ClOMTs</i> and <i>ClSNATs</i> harbor the <i>cis</i>-elements in their promoter regions responding to various hormones. Among abscisic acid (ABA), methyl jasmonate (MeJA), and salicylic acid (SA), ABA treatment observably upregulated the expression of <i>ClOMTs</i> and <i>ClSNATs</i>, and the accumulation of melatonin with ABA treatment reached a level comparable to that with osmotic stress by mannitol treatment. Furthermore, when hormone biosynthesis inhibitors were added to cells before osmotic stress, the expression of <i>ClOMTs</i> and <i>ClSNATs</i>, as well as melatonin accumulation, were significantly suppressed with the ABA biosynthesis inhibitor. This study demonstrated the crucial role of melatonin biosynthesis in response to osmotic stress via plant hormone signal transduction. It showed that ABA signaling plays a dominant role in melatonin synthesis under osmotic stress.
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spelling doaj.art-15714dfa5bda472bb508a4758c9c93e62023-11-19T01:21:53ZengMDPI AGHorticulturae2311-75242023-08-019892710.3390/horticulturae9080927Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon CellsManwen Yan0Mingyan Li1Zhuoying Ding2Fei Qiao3Xuefei Jiang4Sanya Nanfan Research Institute, Hainan University, Sanya 572000, ChinaKey Laboratory for Quality Regulation of Tropical Horticultural Crops of Hainan Province/Key Laboratory of Tropical Agritourism in Greenhouse of Haikou, School of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, ChinaSanya Nanfan Research Institute, Hainan University, Sanya 572000, ChinaTropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaSanya Nanfan Research Institute, Hainan University, Sanya 572000, ChinaMelatonin, a multifunctional signaling molecule, has been shown to play a significant role in response to abiotic stress. Several species have been reported to unveil melatonin’s effect on osmotic stress; however, the signal transduction mechanism of phytohormone-mediated melatonin biosynthesis in plant species remains unclear. In this study, although plants can biosynthesize melatonin, the exogenous application of melatonin to watermelon cells can improve cell growth in response to osmotic stress by regulating the antioxidant machinery of cells. Regarding the melatonin synthesis pathway, ClOMT (ClASMT and ClCOMT) is a multi-gene family, and ClSNAT has two members. Both <i>ClOMTs</i> and <i>ClSNATs</i> harbor the <i>cis</i>-elements in their promoter regions responding to various hormones. Among abscisic acid (ABA), methyl jasmonate (MeJA), and salicylic acid (SA), ABA treatment observably upregulated the expression of <i>ClOMTs</i> and <i>ClSNATs</i>, and the accumulation of melatonin with ABA treatment reached a level comparable to that with osmotic stress by mannitol treatment. Furthermore, when hormone biosynthesis inhibitors were added to cells before osmotic stress, the expression of <i>ClOMTs</i> and <i>ClSNATs</i>, as well as melatonin accumulation, were significantly suppressed with the ABA biosynthesis inhibitor. This study demonstrated the crucial role of melatonin biosynthesis in response to osmotic stress via plant hormone signal transduction. It showed that ABA signaling plays a dominant role in melatonin synthesis under osmotic stress.https://www.mdpi.com/2311-7524/9/8/927<i>Citrullus lanatus</i>osmotic stressmelatoninplant hormone signalsgene expression
spellingShingle Manwen Yan
Mingyan Li
Zhuoying Ding
Fei Qiao
Xuefei Jiang
Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
Horticulturae
<i>Citrullus lanatus</i>
osmotic stress
melatonin
plant hormone signals
gene expression
title Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
title_full Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
title_fullStr Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
title_full_unstemmed Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
title_short Plant Hormone Signals Mediate Melatonin Synthesis to Enhance Osmotic Stress Tolerance in Watermelon Cells
title_sort plant hormone signals mediate melatonin synthesis to enhance osmotic stress tolerance in watermelon cells
topic <i>Citrullus lanatus</i>
osmotic stress
melatonin
plant hormone signals
gene expression
url https://www.mdpi.com/2311-7524/9/8/927
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AT zhuoyingding planthormonesignalsmediatemelatoninsynthesistoenhanceosmoticstresstoleranceinwatermeloncells
AT feiqiao planthormonesignalsmediatemelatoninsynthesistoenhanceosmoticstresstoleranceinwatermeloncells
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