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

Yang Y, Yang S, Li J, Deng Y, Zhang Z, Xu S, Guo W, Zhong C, Zhou R, Shi S - BMC Genomics (2015)

Bottom Line: 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.A total of 99 genes in A. ilicifolius were identified with signals of positive selection.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.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. yangyuchensysu@gmail.com.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus

Ka/Ks distribution of 6634 pairs of orthologs between Acanthus ilicifolius and Ac. leucostachyus. The solid line marks Ka/Ks = 1, whereas the red dots mark the genes with Ka/Ks ratio significantly larger than 1
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Fig4: Ka/Ks distribution of 6634 pairs of orthologs between Acanthus ilicifolius and Ac. leucostachyus. The solid line marks Ka/Ks = 1, whereas the red dots mark the genes with Ka/Ks ratio significantly larger than 1

Mentions: We calculated and plotted the non-synonymous to synonymous substitution ratio (Ka/Ks) for the 6634 pairs of orthologs between the two Acanthus species, A. ilicifolius and A. leucostachyus, as shown in Fig. 4. Only 13 pairs were identified with a Ka/Ks ratio that was significantly larger than 1, indicating signals of positive selection in these two species (red dots in Fig. 4). The functional descriptions of the 13 pairs are listed in Additional file 5. Of them, four were found to be involved in the response to biotic and/or abiotic stimuli (bold in Additional file 5).Fig. 4


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

Yang Y, Yang S, Li J, Deng Y, Zhang Z, Xu S, Guo W, Zhong C, Zhou R, Shi S - BMC Genomics (2015)

Ka/Ks distribution of 6634 pairs of orthologs between Acanthus ilicifolius and Ac. leucostachyus. The solid line marks Ka/Ks = 1, whereas the red dots mark the genes with Ka/Ks ratio significantly larger than 1
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4536770&req=5

Fig4: Ka/Ks distribution of 6634 pairs of orthologs between Acanthus ilicifolius and Ac. leucostachyus. The solid line marks Ka/Ks = 1, whereas the red dots mark the genes with Ka/Ks ratio significantly larger than 1
Mentions: We calculated and plotted the non-synonymous to synonymous substitution ratio (Ka/Ks) for the 6634 pairs of orthologs between the two Acanthus species, A. ilicifolius and A. leucostachyus, as shown in Fig. 4. Only 13 pairs were identified with a Ka/Ks ratio that was significantly larger than 1, indicating signals of positive selection in these two species (red dots in Fig. 4). The functional descriptions of the 13 pairs are listed in Additional file 5. Of them, four were found to be involved in the response to biotic and/or abiotic stimuli (bold in Additional file 5).Fig. 4

Bottom Line: 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.A total of 99 genes in A. ilicifolius were identified with signals of positive selection.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.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, 510275, China. yangyuchensysu@gmail.com.

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus