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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

Evolutionary analyses of Fejervarya cancrivora and its closely related species, F. limnocharis.(a) The species-tree. (b) Comparison of dN/dS ratios between F. cancrivora and F. limnocharis by GO functional categories. Blue and red dots represent categories with an elevated evolutionary rates in F. limnocharis and F. cancrivora, respectively. (c) The dN/dS of differentially expressed genes in kidney of F. cancrivora compared to F. limnocharis. Red (F. cancrivora) and blue (F. limnocharis) bars denote dN/dS of differentially expressed genes, and grey (F. cancrivora) and pink (F. limnocharis) bars give dN/dS of background genes. (d) Venn diagram of up-regulated genes in kidney, ventral skin and positively selected genes in F. cancrivora compared to F. limnocharis.
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f2: Evolutionary analyses of Fejervarya cancrivora and its closely related species, F. limnocharis.(a) The species-tree. (b) Comparison of dN/dS ratios between F. cancrivora and F. limnocharis by GO functional categories. Blue and red dots represent categories with an elevated evolutionary rates in F. limnocharis and F. cancrivora, respectively. (c) The dN/dS of differentially expressed genes in kidney of F. cancrivora compared to F. limnocharis. Red (F. cancrivora) and blue (F. limnocharis) bars denote dN/dS of differentially expressed genes, and grey (F. cancrivora) and pink (F. limnocharis) bars give dN/dS of background genes. (d) Venn diagram of up-regulated genes in kidney, ventral skin and positively selected genes in F. cancrivora compared to F. limnocharis.

Mentions: Analyses of orthologous genes suggested rapid evolution occurred in genes potentially involved in the adaptation to seawater. Among the 8698 predicted one-to-one orthologous gene pairs among the three species of frogs, 7173 were annotated as coding genes of X. tropicalis. After sequence alignment and trimming, 6959 high-confidence orthologous genes remained for estimating the evolutionary constraints acting on F. cancrivora, F. limnocharis and H. rugulosus (Fig. 2a)171819. We calculated the dN/dS value for each GO term in each branch by the free ratio model implemented in PAML424. In total, 54 GO categories harbored significantly higher dN/dS values in F. cancrivora than in F. limnocharis (P < 0.05, binomial test). These included transmembrane transport (GO:0055085, P = 2.31e-32), transporter activity (GO:0005215, P = 7.05e-14), transport (GO:0006810, P = 6.45e-08), cation transport (GO:0006812, P = 1.84e-04), cellular calcium ion homeostasis (GO:0006874, P = 3.38e-4), blood vessel development (GO:0001568, P = 0.002), electron carrier activity (GO:0009055, P = 0.004), sodium ion transport (GO:0006814, P = 0.004) and ion transport (GO:0006811, P = 0.009) (Fig. 2b and Dataset 5). In contrast, 62 GO categories exhibited accelerated evolutionary rates in F. limnocharis and these mainly involved metabolism, such as fatty acid metabolic process (GO:0006631, P = 1.19e-10), fatty acid beta-oxidation (GO:0006635, P = 1.39e-06), triglyceride biosynthetic process (GO:0019432, P = 4.83e-05) and fatty acid biosynthetic process (GO:0006633, P = 9.28e-05) (Dataset 5).


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)

Evolutionary analyses of Fejervarya cancrivora and its closely related species, F. limnocharis.(a) The species-tree. (b) Comparison of dN/dS ratios between F. cancrivora and F. limnocharis by GO functional categories. Blue and red dots represent categories with an elevated evolutionary rates in F. limnocharis and F. cancrivora, respectively. (c) The dN/dS of differentially expressed genes in kidney of F. cancrivora compared to F. limnocharis. Red (F. cancrivora) and blue (F. limnocharis) bars denote dN/dS of differentially expressed genes, and grey (F. cancrivora) and pink (F. limnocharis) bars give dN/dS of background genes. (d) Venn diagram of up-regulated genes in kidney, ventral skin and positively selected genes in F. cancrivora compared to F. limnocharis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Evolutionary analyses of Fejervarya cancrivora and its closely related species, F. limnocharis.(a) The species-tree. (b) Comparison of dN/dS ratios between F. cancrivora and F. limnocharis by GO functional categories. Blue and red dots represent categories with an elevated evolutionary rates in F. limnocharis and F. cancrivora, respectively. (c) The dN/dS of differentially expressed genes in kidney of F. cancrivora compared to F. limnocharis. Red (F. cancrivora) and blue (F. limnocharis) bars denote dN/dS of differentially expressed genes, and grey (F. cancrivora) and pink (F. limnocharis) bars give dN/dS of background genes. (d) Venn diagram of up-regulated genes in kidney, ventral skin and positively selected genes in F. cancrivora compared to F. limnocharis.
Mentions: Analyses of orthologous genes suggested rapid evolution occurred in genes potentially involved in the adaptation to seawater. Among the 8698 predicted one-to-one orthologous gene pairs among the three species of frogs, 7173 were annotated as coding genes of X. tropicalis. After sequence alignment and trimming, 6959 high-confidence orthologous genes remained for estimating the evolutionary constraints acting on F. cancrivora, F. limnocharis and H. rugulosus (Fig. 2a)171819. We calculated the dN/dS value for each GO term in each branch by the free ratio model implemented in PAML424. In total, 54 GO categories harbored significantly higher dN/dS values in F. cancrivora than in F. limnocharis (P < 0.05, binomial test). These included transmembrane transport (GO:0055085, P = 2.31e-32), transporter activity (GO:0005215, P = 7.05e-14), transport (GO:0006810, P = 6.45e-08), cation transport (GO:0006812, P = 1.84e-04), cellular calcium ion homeostasis (GO:0006874, P = 3.38e-4), blood vessel development (GO:0001568, P = 0.002), electron carrier activity (GO:0009055, P = 0.004), sodium ion transport (GO:0006814, P = 0.004) and ion transport (GO:0006811, P = 0.009) (Fig. 2b and Dataset 5). In contrast, 62 GO categories exhibited accelerated evolutionary rates in F. limnocharis and these mainly involved metabolism, such as fatty acid metabolic process (GO:0006631, P = 1.19e-10), fatty acid beta-oxidation (GO:0006635, P = 1.39e-06), triglyceride biosynthetic process (GO:0019432, P = 4.83e-05) and fatty acid biosynthetic process (GO:0006633, P = 9.28e-05) (Dataset 5).

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