Cargando…

Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba

BACKGROUND: Mangroves have adapted to intertidal zones - the interface between terrestrial and marine ecosystems. Various studies have shown adaptive evolution in mangroves at physiological, ecological, and genomic levels. However, these studies paid little attention to gene regulation of salt adapt...

Descripción completa

Detalles Bibliográficos
Autores principales: Feng, Xiao, Xu, Shaohua, Li, Jianfang, Yang, Yuchen, Chen, Qipian, Lyu, Haomin, Zhong, Cairong, He, Ziwen, Shi, Suhua
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7178616/
https://www.ncbi.nlm.nih.gov/pubmed/32321423
http://dx.doi.org/10.1186/s12870-020-02395-3
_version_ 1783525497265717248
author Feng, Xiao
Xu, Shaohua
Li, Jianfang
Yang, Yuchen
Chen, Qipian
Lyu, Haomin
Zhong, Cairong
He, Ziwen
Shi, Suhua
author_facet Feng, Xiao
Xu, Shaohua
Li, Jianfang
Yang, Yuchen
Chen, Qipian
Lyu, Haomin
Zhong, Cairong
He, Ziwen
Shi, Suhua
author_sort Feng, Xiao
collection PubMed
description BACKGROUND: Mangroves have adapted to intertidal zones - the interface between terrestrial and marine ecosystems. Various studies have shown adaptive evolution in mangroves at physiological, ecological, and genomic levels. However, these studies paid little attention to gene regulation of salt adaptation by transcriptome profiles. RESULTS: We sequenced the transcriptomes of Sonneratia alba under low (fresh water), medium (half the seawater salinity), and high salt (seawater salinity) conditions and investigated the underlying transcriptional regulation of salt adaptation. In leaf tissue, 64% potential salinity-related genes were not differentially expressed when salinity increased from freshwater to medium levels, but became up- or down-regulated when salt concentrations further increased to levels found in sea water, indicating that these genes are well adapted to the medium saline condition. We inferred that both maintenance and regulation of cellular environmental homeostasis are important adaptive processes in S. alba. i) The sulfur metabolism as well as flavone and flavonol biosynthesis KEGG pathways were significantly enriched among up-regulated genes in leaves. They are both involved in scavenging ROS or synthesis and accumulation of osmosis-related metabolites in plants. ii) There was a significantly increased percentage of transcription factor-encoding genes among up-regulated transcripts. High expressions of salt tolerance-related TF families were found under high salt conditions. iii) Some genes up-regulated in response to salt treatment showed signs of adaptive evolution at the amino acid level and might contribute to adaptation to fluctuating intertidal environments. CONCLUSIONS: This study first elucidates the mechanism of high-salt adaptation in mangroves at the whole-transcriptome level by salt gradient experimental treatments. It reveals that several candidate genes (including salt-related genes, TF-encoding genes, and PSGs) and major pathways are involved in adaptation to high-salt environments. Our study also provides a valuable resource for future investigation of adaptive evolution in extreme environments.
format Online
Article
Text
id pubmed-7178616
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-71786162020-04-24 Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba Feng, Xiao Xu, Shaohua Li, Jianfang Yang, Yuchen Chen, Qipian Lyu, Haomin Zhong, Cairong He, Ziwen Shi, Suhua BMC Plant Biol Research Article BACKGROUND: Mangroves have adapted to intertidal zones - the interface between terrestrial and marine ecosystems. Various studies have shown adaptive evolution in mangroves at physiological, ecological, and genomic levels. However, these studies paid little attention to gene regulation of salt adaptation by transcriptome profiles. RESULTS: We sequenced the transcriptomes of Sonneratia alba under low (fresh water), medium (half the seawater salinity), and high salt (seawater salinity) conditions and investigated the underlying transcriptional regulation of salt adaptation. In leaf tissue, 64% potential salinity-related genes were not differentially expressed when salinity increased from freshwater to medium levels, but became up- or down-regulated when salt concentrations further increased to levels found in sea water, indicating that these genes are well adapted to the medium saline condition. We inferred that both maintenance and regulation of cellular environmental homeostasis are important adaptive processes in S. alba. i) The sulfur metabolism as well as flavone and flavonol biosynthesis KEGG pathways were significantly enriched among up-regulated genes in leaves. They are both involved in scavenging ROS or synthesis and accumulation of osmosis-related metabolites in plants. ii) There was a significantly increased percentage of transcription factor-encoding genes among up-regulated transcripts. High expressions of salt tolerance-related TF families were found under high salt conditions. iii) Some genes up-regulated in response to salt treatment showed signs of adaptive evolution at the amino acid level and might contribute to adaptation to fluctuating intertidal environments. CONCLUSIONS: This study first elucidates the mechanism of high-salt adaptation in mangroves at the whole-transcriptome level by salt gradient experimental treatments. It reveals that several candidate genes (including salt-related genes, TF-encoding genes, and PSGs) and major pathways are involved in adaptation to high-salt environments. Our study also provides a valuable resource for future investigation of adaptive evolution in extreme environments. BioMed Central 2020-04-22 /pmc/articles/PMC7178616/ /pubmed/32321423 http://dx.doi.org/10.1186/s12870-020-02395-3 Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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 Article
Feng, Xiao
Xu, Shaohua
Li, Jianfang
Yang, Yuchen
Chen, Qipian
Lyu, Haomin
Zhong, Cairong
He, Ziwen
Shi, Suhua
Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title_full Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title_fullStr Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title_full_unstemmed Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title_short Molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree Sonneratia alba
title_sort molecular adaptation to salinity fluctuation in tropical intertidal environments of a mangrove tree sonneratia alba
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7178616/
https://www.ncbi.nlm.nih.gov/pubmed/32321423
http://dx.doi.org/10.1186/s12870-020-02395-3
work_keys_str_mv AT fengxiao molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT xushaohua molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT lijianfang molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT yangyuchen molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT chenqipian molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT lyuhaomin molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT zhongcairong molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT heziwen molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba
AT shisuhua molecularadaptationtosalinityfluctuationintropicalintertidalenvironmentsofamangrovetreesonneratiaalba