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


RESULTS
We 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.


CONCLUSIONS
We 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.
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. yangyuchensysu@gmail.com.
Yuchen
Y
Yang
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. yangshuhuan8909@hotmail.com.
Shuhuan
S
Yang
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. lijf0711@163.com.
Jianfang
J
Li
Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Science, Guangzhou, 510650, China. yfdeng@scbg.ac.cn.
Yunfei
Y
Deng
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. lylazhang@foxmail.com.
Zhang
Z
Zhang
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. xushaohua08@163.com.
Shaohua
S
Xu
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. qingting7906@126.com.
Wuxia
W
Guo
Hainan Dongzhai Harbor National Nature Reserve, Haikou, 571129, China. crzhong169@163.com.
Cairong
C
Zhong
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. zhrench@mail.sysu.edu.cn.
Renchao
R
Zhou
State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. lssssh@mail.sysu.edu.cn.
Suhua
S
Shi
D027901:Acanthaceae / Q000145:classification / Q000235:genetics* / Q000502:physiology; D000220:Adaptation, Biological; D019143:Evolution, Molecular; D020869:Gene Expression Profiling / Q000379:methods*; D063990:Gene Ontology; D010802:Phylogeny; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA / Q000379:methods*; D053833:Wetlands