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Transcriptomes reveal the genetic mechanisms underlying ionic regulatory adaptations to salt in the crab-eating frog.

Shao Y, Wang LJ, Zhong L, Hong ML, Chen HM, Murphy RW, Wu DD, Zhang YP, Che J - Sci Rep (2015)

Bottom Line: Genes in categories associated with ion transport appear to have evolved rapidly in F. cancrivora.Four genes involved in the regulation of body fluid levels show signs of positive selection and increased expression.Significant up-regulation occurs in several genes of F. cancrivora associated with renin-angiotensin system and aldosterone-regulated sodium reabsorption pathways, which relate to osmotic regulation.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650204, China.

ABSTRACT
The crab-eating frog, Fejervarya cancrivora, is the only frog that lives near seas. It tolerates increased environmental concentrations of sodium, chloride and potassium partly by raising ion and urea levels in its blood plasma. The molecular mechanism of the adaptation remains rarely documented. Herein, we analyze transcriptomes of the crab-eating frog and its closely related saline-intolerant species, F. limnocharis, to explore the molecular basis of adaptations to such extreme environmental conditions. Analyses reveal the potential genetic mechanism underlying the adaptation to salinity for the crab-eating frog. Genes in categories associated with ion transport appear to have evolved rapidly in F. cancrivora. Both positively selected and differentially expressed genes exhibit enrichment in the GO category regulation of renal sodium excretion. In this category, the positively selected sites of ANPEP and AVPR2 encode CD13 and V2 receptors, respectively; they fall precisely on conserved domains. More differentially expressed rapidly evolved genes occur in the kidney of F. cancrivora than in F. limnocharis. Four genes involved in the regulation of body fluid levels show signs of positive selection and increased expression. Significant up-regulation occurs in several genes of F. cancrivora associated with renin-angiotensin system and aldosterone-regulated sodium reabsorption pathways, which relate to osmotic regulation.

No MeSH data available.


Related in: MedlinePlus

Visualization of differentially expressed genes in brain (a), ventral skin (b) and kidney (c) between Fejervarya cancrivora and F. limnocharis.X-axis represents differential folds of genes (log FC) and the Y-axis shows -log P value of differentially expressed genes. Red denotes significantly up- and down-regulated genes in F. cancrivora compared to F. limnocharis. Blue denotes show genes without significant differences in levels of expressions.
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f4: Visualization of differentially expressed genes in brain (a), ventral skin (b) and kidney (c) between Fejervarya cancrivora and F. limnocharis.X-axis represents differential folds of genes (log FC) and the Y-axis shows -log P value of differentially expressed genes. Red denotes significantly up- and down-regulated genes in F. cancrivora compared to F. limnocharis. Blue denotes show genes without significant differences in levels of expressions.

Mentions: Because changes in gene expression have been considered to play more important roles in phenotypic evolution than mutations in protein-coding sequences26, we identified differentially expressed genes between F. cancrivora and its closely related species F. limnocharis. Kidney harbored far more differentially expressed genes (3239) (Dataset 8) than ventral skin (1104) (Dataset 9) and brain (35) (Fig. 4 and Dataset 10). In F. cancrivora the dN/dS values of differentially expressed genes in kidney were significantly higher than those of background genes (P = 0.0019, Mann-Whitney U test), but this pattern was not found in F. limnocharis (P = 0.5869, Mann-Whitney U test). This discovery suggested that the differentially expressed genes in F. cancrivora evolved rapidly (Fig. 2c). Further, in F. cancrivora a higher number of positively selected genes were found to harbor elevated expressions in kidney (39 positively selected genes) compared with ventral skin (24 positively selected genes) and brain (1 positively selected gene). Gene enrichment analysis of up-regulated genes in kidney found categories such as transport, regulation of urine volume, regulation of renal sodium excretion, regulation of excretion, sodium ion homeostasis and regulation of vasodilation to be over-represented (Dataset 11). Although this might be associated with adaptation to the high salinity of sea-water, the exact functions of changes in expression remained largely unclear and in need of experimental verification. Consistently, up-regulated genes in the ventral skin also showed similar enrichment. In contrast, down-regulated genes generally were involved in macromolecule metabolic processes and macromolecule modification (Dataset 12).


Transcriptomes reveal the genetic mechanisms underlying ionic regulatory adaptations to salt in the crab-eating frog.

Shao Y, Wang LJ, Zhong L, Hong ML, Chen HM, Murphy RW, Wu DD, Zhang YP, Che J - Sci Rep (2015)

Visualization of differentially expressed genes in brain (a), ventral skin (b) and kidney (c) between Fejervarya cancrivora and F. limnocharis.X-axis represents differential folds of genes (log FC) and the Y-axis shows -log P value of differentially expressed genes. Red denotes significantly up- and down-regulated genes in F. cancrivora compared to F. limnocharis. Blue denotes show genes without significant differences in levels of expressions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4664912&req=5

f4: Visualization of differentially expressed genes in brain (a), ventral skin (b) and kidney (c) between Fejervarya cancrivora and F. limnocharis.X-axis represents differential folds of genes (log FC) and the Y-axis shows -log P value of differentially expressed genes. Red denotes significantly up- and down-regulated genes in F. cancrivora compared to F. limnocharis. Blue denotes show genes without significant differences in levels of expressions.
Mentions: Because changes in gene expression have been considered to play more important roles in phenotypic evolution than mutations in protein-coding sequences26, we identified differentially expressed genes between F. cancrivora and its closely related species F. limnocharis. Kidney harbored far more differentially expressed genes (3239) (Dataset 8) than ventral skin (1104) (Dataset 9) and brain (35) (Fig. 4 and Dataset 10). In F. cancrivora the dN/dS values of differentially expressed genes in kidney were significantly higher than those of background genes (P = 0.0019, Mann-Whitney U test), but this pattern was not found in F. limnocharis (P = 0.5869, Mann-Whitney U test). This discovery suggested that the differentially expressed genes in F. cancrivora evolved rapidly (Fig. 2c). Further, in F. cancrivora a higher number of positively selected genes were found to harbor elevated expressions in kidney (39 positively selected genes) compared with ventral skin (24 positively selected genes) and brain (1 positively selected gene). Gene enrichment analysis of up-regulated genes in kidney found categories such as transport, regulation of urine volume, regulation of renal sodium excretion, regulation of excretion, sodium ion homeostasis and regulation of vasodilation to be over-represented (Dataset 11). Although this might be associated with adaptation to the high salinity of sea-water, the exact functions of changes in expression remained largely unclear and in need of experimental verification. Consistently, up-regulated genes in the ventral skin also showed similar enrichment. In contrast, down-regulated genes generally were involved in macromolecule metabolic processes and macromolecule modification (Dataset 12).

Bottom Line: Genes in categories associated with ion transport appear to have evolved rapidly in F. cancrivora.Four genes involved in the regulation of body fluid levels show signs of positive selection and increased expression.Significant up-regulation occurs in several genes of F. cancrivora associated with renin-angiotensin system and aldosterone-regulated sodium reabsorption pathways, which relate to osmotic regulation.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Genetic Resources and Evolution, and Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650204, China.

ABSTRACT
The crab-eating frog, Fejervarya cancrivora, is the only frog that lives near seas. It tolerates increased environmental concentrations of sodium, chloride and potassium partly by raising ion and urea levels in its blood plasma. The molecular mechanism of the adaptation remains rarely documented. Herein, we analyze transcriptomes of the crab-eating frog and its closely related saline-intolerant species, F. limnocharis, to explore the molecular basis of adaptations to such extreme environmental conditions. Analyses reveal the potential genetic mechanism underlying the adaptation to salinity for the crab-eating frog. Genes in categories associated with ion transport appear to have evolved rapidly in F. cancrivora. Both positively selected and differentially expressed genes exhibit enrichment in the GO category regulation of renal sodium excretion. In this category, the positively selected sites of ANPEP and AVPR2 encode CD13 and V2 receptors, respectively; they fall precisely on conserved domains. More differentially expressed rapidly evolved genes occur in the kidney of F. cancrivora than in F. limnocharis. Four genes involved in the regulation of body fluid levels show signs of positive selection and increased expression. Significant up-regulation occurs in several genes of F. cancrivora associated with renin-angiotensin system and aldosterone-regulated sodium reabsorption pathways, which relate to osmotic regulation.

No MeSH data available.


Related in: MedlinePlus