Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>

Melatonin, a widely known indoleamine molecule that mediates various animal and plant physiological processes, is formed from N-acetyl serotonin via N-acetylserotonin methyltransferase (ASMT). ASMT is an enzyme that catalyzes melatonin synthesis in plants in the rate-determining step and is homologo...

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Main Authors: Kexin Tan, Jiangzhu Zheng, Cheng Liu, Xianghan Liu, Xiaomin Liu, Tengteng Gao, Xinyang Song, Zhiwei Wei, Fengwang Ma, Chao Li
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/22/12425
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author Kexin Tan
Jiangzhu Zheng
Cheng Liu
Xianghan Liu
Xiaomin Liu
Tengteng Gao
Xinyang Song
Zhiwei Wei
Fengwang Ma
Chao Li
author_facet Kexin Tan
Jiangzhu Zheng
Cheng Liu
Xianghan Liu
Xiaomin Liu
Tengteng Gao
Xinyang Song
Zhiwei Wei
Fengwang Ma
Chao Li
author_sort Kexin Tan
collection DOAJ
description Melatonin, a widely known indoleamine molecule that mediates various animal and plant physiological processes, is formed from N-acetyl serotonin via N-acetylserotonin methyltransferase (ASMT). ASMT is an enzyme that catalyzes melatonin synthesis in plants in the rate-determining step and is homologous to hydroxyindole-O-methyltransferase (HIOMT) melatonin synthase in animals. To date, little is known about the effect of <i>HIOMT</i> on salinity in apple plants. Here, we explored the melatonin physiological function in the salinity condition response by heterologous expressing the homologous human <i>HIOMT</i> gene in apple plants. We discovered that the expression of melatonin-related gene (<i>MdASMT</i>) in apple plants was induced by salinity. Most notably, compared with the wild type, three transgenic lines indicated higher melatonin levels, and the heterologous expression of <i>HIOMT</i> enhanced the expression of melatonin synthesis genes. The transgenic lines showed reduced salt damage symptoms, lower relative electrolyte leakage, and less total chlorophyll loss from leaves under salt stress. Meanwhile, through enhanced activity of antioxidant enzymes, transgenic lines decreased the reactive oxygen species accumulation, downregulated the expression of the abscisic acid synthesis gene (<i>MdNCED3</i>), accordingly reducing the accumulation of abscisic acid under salt stress. Both mechanisms regulated morphological changes in the stomata synergistically, thereby mitigating damage to the plants’ photosynthetic ability. In addition, transgenic plants also effectively stabilized their ion balance, raised the expression of salt stress–related genes, as well as alleviated osmotic stress through changes in amino acid metabolism. In summary, heterologous expression of <i>HIOMT</i> improved the adaptation of apple leaves to salt stress, primarily by increasing melatonin concentration, maintaining a high photosynthetic capacity, reducing reactive oxygen species accumulation, and maintaining normal ion homeostasis.
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spelling doaj.art-dbcee07189764f94926718db615e687b2023-11-22T23:42:10ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-11-0122221242510.3390/ijms222212425Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>Kexin Tan0Jiangzhu Zheng1Cheng Liu2Xianghan Liu3Xiaomin Liu4Tengteng Gao5Xinyang Song6Zhiwei Wei7Fengwang Ma8Chao Li9State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling, Xianyang 712100, ChinaMelatonin, a widely known indoleamine molecule that mediates various animal and plant physiological processes, is formed from N-acetyl serotonin via N-acetylserotonin methyltransferase (ASMT). ASMT is an enzyme that catalyzes melatonin synthesis in plants in the rate-determining step and is homologous to hydroxyindole-O-methyltransferase (HIOMT) melatonin synthase in animals. To date, little is known about the effect of <i>HIOMT</i> on salinity in apple plants. Here, we explored the melatonin physiological function in the salinity condition response by heterologous expressing the homologous human <i>HIOMT</i> gene in apple plants. We discovered that the expression of melatonin-related gene (<i>MdASMT</i>) in apple plants was induced by salinity. Most notably, compared with the wild type, three transgenic lines indicated higher melatonin levels, and the heterologous expression of <i>HIOMT</i> enhanced the expression of melatonin synthesis genes. The transgenic lines showed reduced salt damage symptoms, lower relative electrolyte leakage, and less total chlorophyll loss from leaves under salt stress. Meanwhile, through enhanced activity of antioxidant enzymes, transgenic lines decreased the reactive oxygen species accumulation, downregulated the expression of the abscisic acid synthesis gene (<i>MdNCED3</i>), accordingly reducing the accumulation of abscisic acid under salt stress. Both mechanisms regulated morphological changes in the stomata synergistically, thereby mitigating damage to the plants’ photosynthetic ability. In addition, transgenic plants also effectively stabilized their ion balance, raised the expression of salt stress–related genes, as well as alleviated osmotic stress through changes in amino acid metabolism. In summary, heterologous expression of <i>HIOMT</i> improved the adaptation of apple leaves to salt stress, primarily by increasing melatonin concentration, maintaining a high photosynthetic capacity, reducing reactive oxygen species accumulation, and maintaining normal ion homeostasis.https://www.mdpi.com/1422-0067/22/22/12425hydroxyindole-O-methyltransferase genemelatoninROSABAion homeostasisamino acids
spellingShingle Kexin Tan
Jiangzhu Zheng
Cheng Liu
Xianghan Liu
Xiaomin Liu
Tengteng Gao
Xinyang Song
Zhiwei Wei
Fengwang Ma
Chao Li
Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
International Journal of Molecular Sciences
hydroxyindole-O-methyltransferase gene
melatonin
ROS
ABA
ion homeostasis
amino acids
title Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
title_full Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
title_fullStr Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
title_full_unstemmed Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
title_short Heterologous Expression of the Melatonin-Related Gene <i>HIOMT</i> Improves Salt Tolerance in <i>Malus domestica</i>
title_sort heterologous expression of the melatonin related gene i hiomt i improves salt tolerance in i malus domestica i
topic hydroxyindole-O-methyltransferase gene
melatonin
ROS
ABA
ion homeostasis
amino acids
url https://www.mdpi.com/1422-0067/22/22/12425
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