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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

Positively selected and expanded key genes in stress resistance pathways of Acanthus ilicifolius. Genes, products and pathways for responding to salt-stress and for heat and ultraviolet-stress were marked in blue and orange shading, respectively
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Fig5: Positively selected and expanded key genes in stress resistance pathways of Acanthus ilicifolius. Genes, products and pathways for responding to salt-stress and for heat and ultraviolet-stress were marked in blue and orange shading, respectively

Mentions: To identify candidate genes under positive selection along the branch of A. ilicifolius, we further tested the 2245 pairs of orthologs among four species, A. ilicifolius, A. leucostachyus, Av. marina and S. indicum, using the improved branch-site likelihood method in the codeml module of PAML [18–20]. A total of 99 genes were identified as positively selected genes (PSGs) in A. ilicifolius. GO annotations revealed that 48 (20.8 %) and 42 (18.2 %) of the 99 genes were assigned to metabolic and cellular process, respectively (Additional file 6a). Of the 99 genes, 18 sequences were assigned to 13 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways (15 unique EC numbers) [21]. Detailed annotations were performed on these genes and the results are listed in Additional file 7. Interestingly, 23 genes were annotated with functions involving stimulus responses and reproduction, and 16 were found to be directly involved in response to abiotic stresses (Fig. 5; bold in Additional file 7). These genes fell into three functional groups. The first group consisted of four genes involved in salt-stress resistance. One gene of interest, Ail_c57143_g1_i2, catalyzes the transfer of an amino group from ornithine to the precursor of proline, L-glutamate 5-semialdehyde, which plays a key role in the proline synthesis pathway. Twelve genes with annotations of response to heat and UV stress were assigned to the second groups. Two genes, Ail_c48553_g1_i1 and Ail_c56385_g1_i1, were found to be involved in the last step of the synthesis of glutathione, which is an important antioxidant that protects important cellular components from damage caused by reactive oxygen species (ROS) in plants. The third groups included seven genes involved in seed germination and embryo development.Fig. 5


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)

Positively selected and expanded key genes in stress resistance pathways of Acanthus ilicifolius. Genes, products and pathways for responding to salt-stress and for heat and ultraviolet-stress were marked in blue and orange shading, respectively
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig5: Positively selected and expanded key genes in stress resistance pathways of Acanthus ilicifolius. Genes, products and pathways for responding to salt-stress and for heat and ultraviolet-stress were marked in blue and orange shading, respectively
Mentions: To identify candidate genes under positive selection along the branch of A. ilicifolius, we further tested the 2245 pairs of orthologs among four species, A. ilicifolius, A. leucostachyus, Av. marina and S. indicum, using the improved branch-site likelihood method in the codeml module of PAML [18–20]. A total of 99 genes were identified as positively selected genes (PSGs) in A. ilicifolius. GO annotations revealed that 48 (20.8 %) and 42 (18.2 %) of the 99 genes were assigned to metabolic and cellular process, respectively (Additional file 6a). Of the 99 genes, 18 sequences were assigned to 13 Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways (15 unique EC numbers) [21]. Detailed annotations were performed on these genes and the results are listed in Additional file 7. Interestingly, 23 genes were annotated with functions involving stimulus responses and reproduction, and 16 were found to be directly involved in response to abiotic stresses (Fig. 5; bold in Additional file 7). These genes fell into three functional groups. The first group consisted of four genes involved in salt-stress resistance. One gene of interest, Ail_c57143_g1_i2, catalyzes the transfer of an amino group from ornithine to the precursor of proline, L-glutamate 5-semialdehyde, which plays a key role in the proline synthesis pathway. Twelve genes with annotations of response to heat and UV stress were assigned to the second groups. Two genes, Ail_c48553_g1_i1 and Ail_c56385_g1_i1, were found to be involved in the last step of the synthesis of glutathione, which is an important antioxidant that protects important cellular components from damage caused by reactive oxygen species (ROS) in plants. The third groups included seven genes involved in seed germination and embryo development.Fig. 5

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