Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor

Abstract Background Salt, a common environmental stress factor, inhibits plant growth and reduces yields. Melatonin is a pleiotropic molecule that regulates plant growth and can alleviate environmental stress in plants. All previous research on this topic has focused on the use of melatonin to impro...

Full description

Bibliographic Details
Main Authors: Junpeng Li, Fang Yuan, Yanlu Liu, Mingjing Zhang, Yun Liu, Yang Zhao, Baoshan Wang, Min Chen
Format: Article
Language:English
Published: BMC 2020-10-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-020-02703-x
id doaj-6101c7cef4c349aaa02469fb75c7168a
record_format Article
spelling doaj-6101c7cef4c349aaa02469fb75c7168a2020-11-25T04:02:09ZengBMCBMC Plant Biology1471-22292020-10-0120111110.1186/s12870-020-02703-xExogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolorJunpeng Li0Fang Yuan1Yanlu Liu2Mingjing Zhang3Yun Liu4Yang Zhao5Baoshan Wang6Min Chen7Shandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityShandong Provincial Key Laboratory of Plant Stress, College of Life Science, Shandong Normal UniversityAbstract Background Salt, a common environmental stress factor, inhibits plant growth and reduces yields. Melatonin is a pleiotropic molecule that regulates plant growth and can alleviate environmental stress in plants. All previous research on this topic has focused on the use of melatonin to improve the relatively low salt tolerance of glycophytes by promoting growth and enhancing antioxidant ability. It is unclear whether exogenous melatonin can increase the salt tolerance of halophytes, particularly recretohalophytes, by enhancing salt secretion from the salt glands. Results To examine the mechanisms of melatonin-mediated salt tolerance, we explored the effects of exogenous applications of melatonin on the secretion of salt from the salt glands of Limonium bicolor (a kind of recretohalophyte) seedlings and on the expression of associated genes. A pretreatment with 5 μM melatonin significantly improved the growth of L. bicolor seedlings under 300 mM NaCl. Furthermore, exogenous melatonin significantly increased the dry weight and endogenous melatonin content of L. bicolor. In addition, this treatment reduced the content of Na+ and Cl− in leaves, but increased the K+ content. Both the salt secretion rate of the salt glands and the expression level of genes encoding ion transporters (LbHTK1, LbSOS1, LbPMA, and LbNHX1) and vesicular transport proteins (LbVAMP721, LbVAP27, and LbVAMP12) were significantly increased by exogenous melatonin treatment. These results indicate that melatonin improves the salt tolerance of the recretohalophyte L. bicolor via the upregulation of salt secretion by the salt glands. Conclusions Our results showed that melatonin can upregulate the expression of genes encoding ion transporters and vesicle transport proteins to enhance salt secretion from the salt glands. Combining the results of the current study with previous research, we formulated a novel mechanism by which melatonin increases salt secretion in L. bicolor. Ions in mesophyll cells are transported to the salt glands through ion transporters located at the plasma membrane. After the ions enter the salt glands, they are transported to the collecting chamber adjacent to the secretory pore through vesicle transport and ions transporter and then are secreted from the secretory pore of salt glands, which maintain ionic homeostasis in the cells and alleviate NaCl-induced growth inhibition.http://link.springer.com/article/10.1186/s12870-020-02703-xIon homeostasisLimonium bicolorMelatoninSalt glandSalt secretion
collection DOAJ
language English
format Article
sources DOAJ
author Junpeng Li
Fang Yuan
Yanlu Liu
Mingjing Zhang
Yun Liu
Yang Zhao
Baoshan Wang
Min Chen
spellingShingle Junpeng Li
Fang Yuan
Yanlu Liu
Mingjing Zhang
Yun Liu
Yang Zhao
Baoshan Wang
Min Chen
Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
BMC Plant Biology
Ion homeostasis
Limonium bicolor
Melatonin
Salt gland
Salt secretion
author_facet Junpeng Li
Fang Yuan
Yanlu Liu
Mingjing Zhang
Yun Liu
Yang Zhao
Baoshan Wang
Min Chen
author_sort Junpeng Li
title Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
title_short Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
title_full Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
title_fullStr Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
title_full_unstemmed Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor
title_sort exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in limonium bicolor
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2020-10-01
description Abstract Background Salt, a common environmental stress factor, inhibits plant growth and reduces yields. Melatonin is a pleiotropic molecule that regulates plant growth and can alleviate environmental stress in plants. All previous research on this topic has focused on the use of melatonin to improve the relatively low salt tolerance of glycophytes by promoting growth and enhancing antioxidant ability. It is unclear whether exogenous melatonin can increase the salt tolerance of halophytes, particularly recretohalophytes, by enhancing salt secretion from the salt glands. Results To examine the mechanisms of melatonin-mediated salt tolerance, we explored the effects of exogenous applications of melatonin on the secretion of salt from the salt glands of Limonium bicolor (a kind of recretohalophyte) seedlings and on the expression of associated genes. A pretreatment with 5 μM melatonin significantly improved the growth of L. bicolor seedlings under 300 mM NaCl. Furthermore, exogenous melatonin significantly increased the dry weight and endogenous melatonin content of L. bicolor. In addition, this treatment reduced the content of Na+ and Cl− in leaves, but increased the K+ content. Both the salt secretion rate of the salt glands and the expression level of genes encoding ion transporters (LbHTK1, LbSOS1, LbPMA, and LbNHX1) and vesicular transport proteins (LbVAMP721, LbVAP27, and LbVAMP12) were significantly increased by exogenous melatonin treatment. These results indicate that melatonin improves the salt tolerance of the recretohalophyte L. bicolor via the upregulation of salt secretion by the salt glands. Conclusions Our results showed that melatonin can upregulate the expression of genes encoding ion transporters and vesicle transport proteins to enhance salt secretion from the salt glands. Combining the results of the current study with previous research, we formulated a novel mechanism by which melatonin increases salt secretion in L. bicolor. Ions in mesophyll cells are transported to the salt glands through ion transporters located at the plasma membrane. After the ions enter the salt glands, they are transported to the collecting chamber adjacent to the secretory pore through vesicle transport and ions transporter and then are secreted from the secretory pore of salt glands, which maintain ionic homeostasis in the cells and alleviate NaCl-induced growth inhibition.
topic Ion homeostasis
Limonium bicolor
Melatonin
Salt gland
Salt secretion
url http://link.springer.com/article/10.1186/s12870-020-02703-x
work_keys_str_mv AT junpengli exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT fangyuan exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT yanluliu exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT mingjingzhang exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT yunliu exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT yangzhao exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT baoshanwang exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
AT minchen exogenousmelatoninenhancessaltsecretionfromsaltglandsbyupregulatingtheexpressionofiontransporterandvesicletransportgenesinlimoniumbicolor
_version_ 1724444179483852800