Abstract

BackgroundMangroves 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.ResultsWe 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.ConclusionsThis 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.

Highlights

  • Mangroves have adapted to intertidal zones - the interface between terrestrial and marine ecosystems

  • Identification of differentially expressed genes and expression patterns To generate genomic resources and begin elucidating the mechanisms of salt tolerance in S. alba, we performed RNA-seq experiments on leaves and roots from plants reared in media with various salt levels

  • Our analyses report several candidate genes and major pathways including sulfur metabolism, flavone and flavonol biosynthesis, nicotinate and nicotinamide metabolism, and cysteine and methionine metabolism, that are involved in adaptation to high-salt environments

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Summary

Introduction

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 These studies paid little attention to gene regulation of salt adaptation by transcriptome profiles. Located at the interface between terrestrial and marine ecosystems, intertidal zones impose many harsh or extreme conditions on local organisms, including high salinity, hypoxia, salt fluctuations, strong ultraviolet (UV) light, and high temperature [1]. Mangroves are a major group of marine halophytes that thrive and complete their life cycles in high-salinity environments that arise due to fluctuating seawater levels. They are good model systems for investigating adaptive evolution. Little attention has been paid to transcriptional regulation even though it has been strongly selected for rapid adaptation to changes in environmental conditions and may play a critical role at ecological and evolutionary timescales [11]

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