Transcriptome analysis of the Holly mangrove Acanthus ilicifolius and its terrestrial relative, Acanthus leucostachyus, provides insights into adaptation to intertidal zones.

Cairong Zhong,Wuxia Guo,Jianfang Li,Shaohua Xu,Zhang Zhang,Yuchen Yang,Yunfei Deng,Renchao Zhou,Shuhuan Yang,Suhua Shi

doi:10.1186/s12864-015-1813-9

Abstract

BackgroundAcanthus is a unique genus consisting of both true mangrove and terrestrial species; thus, it represents an ideal system for studying the origin and adaptive evolution of mangrove plants to intertidal environments. However, little is known regarding the two respects of mangrove species in Acanthus. In this study, we sequenced the transcriptomes of the pooled roots and leaves tissues for a mangrove species, Acanthus ilicifolius, and its terrestrial congener, A. leucostachyus, to illustrate the origin of the mangrove species in this genus and their adaptive evolution to harsh habitats.ResultsWe obtained 73,039 and 69,580 contigs with N50 values of 741 and 1557 bp for A. ilicifolius and A. leucostachyus, respectively. Phylogenetic analyses based on four nuclear segments and three chloroplast fragments revealed that mangroves and terrestrial species in Acanthus fell into different clades, indicating a single origin of the mangrove species in Acanthus. Based on 6634 orthologs, A. ilicifolius and A. leucostachyus were found to be highly divergent, with a peak of synonymous substitution rate (Ks) distribution of 0.145 and an estimated divergence time of approximately 16.8 million years ago (MYA). The transgression in the Early to Middle Miocene may be the major reason for the entry of the mangrove lineage of Acanthus into intertidal environments. Gene ontology (GO) classifications of the full transcriptomes did not show any apparent differences between A. ilicifolius and A. leucostachyus, suggesting the absence of gene components specific to the mangrove transcriptomes. A total of 99 genes in A. ilicifolius were identified with signals of positive selection. Twenty-three of the 99 positively selected genes (PSGs) were found to be involved in salt, heat and ultraviolet stress tolerance, seed germination and embryo development under periodic inundation. These stress-tolerance related PSGs may be crucial for the adaptation of the mangrove species in this genus to stressful marine environments and may contribute to speciation in Acanthus.ConclusionsWe characterized the transcriptomes of one mangrove species of Acanthus, A. ilicifolius, and its terrestrial relative, A. leucostachyus, and provided insights into the origin of the mangrove Acanthus species and their adaptive evolution to abiotic stresses in intertidal environments.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1813-9) contains supplementary material, which is available to authorized users.

Highlights

Acanthus is a unique genus consisting of both true mangrove and terrestrial species; it represents an ideal system for studying the origin and adaptive evolution of mangrove plants to intertidal environments
Transcriptome sequencing and de novo assembly A total of 44.04 million 90-bp and 46.89 million 100-bp paired-end reads were sequenced for A. ilicifolius and A. leucostachyus, respectively (Table 1)
The results showed that the peak of Synonymous substitution rate (Ks) distribution was 0.145 between A. ilicifolius and A. leucostachyus, while it was 0.605 and 0.585 between Av. marina and A. ilicifolius and A. leucostachyus, respectively (Fig. 1a)

Summary

Introduction

Acanthus is a unique genus consisting of both true mangrove and terrestrial species; it represents an ideal system for studying the origin and adaptive evolution of mangrove plants to intertidal environments. We sequenced the transcriptomes of the pooled roots and leaves tissues for a mangrove species, Acanthus ilicifolius, and its terrestrial congener, A. leucostachyus, to illustrate the origin of the mangrove species in this genus and their adaptive evolution to harsh habitats. As the dominant forest community and ecosystem in the coasts, mangrove plants struggle and survive in these environments with remarkable morphological and physiological characteristic, for example, exposed breathing roots, support roots and buttresses, salt-excreting leaves, and viviparous waterdispersed propagules [1, 2]. Mangroves are constituent plants of approximately 70 species from 28 genera belonging to 20 families [3]. The divergent time and the species radiation within some genera are still unclear and are of great interest to many botanists

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