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Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity

BACKGROUND: Soil salinization is becoming an increasingly serious problem worldwide, resulting in cultivated land loss and desertification, as well as having a serious impact on agriculture and the economy. The indoleamine melatonin (N-acetyl-5-methoxytryptamine) has a wide array of biological roles...

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Autores principales: Li, Junpeng, Liu, Yun, Zhang, Mingjing, Xu, Hualing, Ning, Kai, Wang, Baoshan, Chen, Min
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725383/
https://www.ncbi.nlm.nih.gov/pubmed/34983373
http://dx.doi.org/10.1186/s12870-021-03402-x
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author Li, Junpeng
Liu, Yun
Zhang, Mingjing
Xu, Hualing
Ning, Kai
Wang, Baoshan
Chen, Min
author_facet Li, Junpeng
Liu, Yun
Zhang, Mingjing
Xu, Hualing
Ning, Kai
Wang, Baoshan
Chen, Min
author_sort Li, Junpeng
collection PubMed
description BACKGROUND: Soil salinization is becoming an increasingly serious problem worldwide, resulting in cultivated land loss and desertification, as well as having a serious impact on agriculture and the economy. The indoleamine melatonin (N-acetyl-5-methoxytryptamine) has a wide array of biological roles in plants, including acting as an auxin analog and an antioxidant. Previous studies have shown that exogenous melatonin application alleviates the salt-induced growth inhibition in non-halophyte plants; however, to our knowledge, melatonin effects have not been examined on halophytes, and it is unclear whether melatonin provides similar protection to salt-exposed halophytic plants. RESULTS: We exposed the halophyte Limonium bicolor to salt stress (300 mM) and concomitantly treated the plants with 5 μM melatonin to examine the effect of melatonin on salt tolerance. Exogenous melatonin treatment promoted the growth of L. bicolor under salt stress, as reflected by increasing its fresh weight and leaf area. This increased growth was caused by an increase in net photosynthetic rate and water use efficiency. Treatment of salt-stressed L. bicolor seedlings with 5 μM melatonin also enhanced the activities of antioxidants (superoxide dismutase [SOD], peroxidase [POD], catalase [CAT], and ascorbate peroxidase [APX]), while significantly decreasing the contents of hydrogen peroxide (H(2)O(2)), superoxide anion (O(2)(•−)), and malondialdehyde (MDA). To screen for L. bicolor genes involved in the above physiological processes, high-throughput RNA sequencing was conducted. A gene ontology enrichment analysis indicated that genes related to photosynthesis, reactive oxygen species scavenging, the auxin-dependent signaling pathway and mitogen-activated protein kinase (MAPK) were highly expressed under melatonin treatment. These data indicated that melatonin improved photosynthesis, decreased reactive oxygen species (ROS) and activated MAPK-mediated antioxidant responses, triggering a downstream MAPK cascade that upregulated the expression of antioxidant-related genes. Thus, melatonin improves the salt tolerance of L. bicolor by increasing photosynthesis and improving cellular redox homeostasis under salt stress. CONCLUSIONS: Our results showed that melatonin can upregulate the expression of genes related to photosynthesis, reactive oxygen species scavenging and mitogen-activated protein kinase (MAPK) of L. bicolor under salt stress, which can improve photosynthesis and antioxidant enzyme activities. Thus melatonin can promote the growth of the species and maintain the homeostasis of reactive oxygen species to alleviate salt stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03402-x.
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spelling pubmed-87253832022-01-06 Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity Li, Junpeng Liu, Yun Zhang, Mingjing Xu, Hualing Ning, Kai Wang, Baoshan Chen, Min BMC Plant Biol Research BACKGROUND: Soil salinization is becoming an increasingly serious problem worldwide, resulting in cultivated land loss and desertification, as well as having a serious impact on agriculture and the economy. The indoleamine melatonin (N-acetyl-5-methoxytryptamine) has a wide array of biological roles in plants, including acting as an auxin analog and an antioxidant. Previous studies have shown that exogenous melatonin application alleviates the salt-induced growth inhibition in non-halophyte plants; however, to our knowledge, melatonin effects have not been examined on halophytes, and it is unclear whether melatonin provides similar protection to salt-exposed halophytic plants. RESULTS: We exposed the halophyte Limonium bicolor to salt stress (300 mM) and concomitantly treated the plants with 5 μM melatonin to examine the effect of melatonin on salt tolerance. Exogenous melatonin treatment promoted the growth of L. bicolor under salt stress, as reflected by increasing its fresh weight and leaf area. This increased growth was caused by an increase in net photosynthetic rate and water use efficiency. Treatment of salt-stressed L. bicolor seedlings with 5 μM melatonin also enhanced the activities of antioxidants (superoxide dismutase [SOD], peroxidase [POD], catalase [CAT], and ascorbate peroxidase [APX]), while significantly decreasing the contents of hydrogen peroxide (H(2)O(2)), superoxide anion (O(2)(•−)), and malondialdehyde (MDA). To screen for L. bicolor genes involved in the above physiological processes, high-throughput RNA sequencing was conducted. A gene ontology enrichment analysis indicated that genes related to photosynthesis, reactive oxygen species scavenging, the auxin-dependent signaling pathway and mitogen-activated protein kinase (MAPK) were highly expressed under melatonin treatment. These data indicated that melatonin improved photosynthesis, decreased reactive oxygen species (ROS) and activated MAPK-mediated antioxidant responses, triggering a downstream MAPK cascade that upregulated the expression of antioxidant-related genes. Thus, melatonin improves the salt tolerance of L. bicolor by increasing photosynthesis and improving cellular redox homeostasis under salt stress. CONCLUSIONS: Our results showed that melatonin can upregulate the expression of genes related to photosynthesis, reactive oxygen species scavenging and mitogen-activated protein kinase (MAPK) of L. bicolor under salt stress, which can improve photosynthesis and antioxidant enzyme activities. Thus melatonin can promote the growth of the species and maintain the homeostasis of reactive oxygen species to alleviate salt stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03402-x. BioMed Central 2022-01-04 /pmc/articles/PMC8725383/ /pubmed/34983373 http://dx.doi.org/10.1186/s12870-021-03402-x Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Li, Junpeng
Liu, Yun
Zhang, Mingjing
Xu, Hualing
Ning, Kai
Wang, Baoshan
Chen, Min
Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title_full Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title_fullStr Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title_full_unstemmed Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title_short Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity
title_sort melatonin increases growth and salt tolerance of limonium bicolor by improving photosynthetic and antioxidant capacity
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8725383/
https://www.ncbi.nlm.nih.gov/pubmed/34983373
http://dx.doi.org/10.1186/s12870-021-03402-x
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