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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

Interactions of positively selected genes and differentially expressed genes involved in the adaptation of F.cancrivora to high salinity.Red italics denote candidate positively selected genes, blue italics indicate significantly up-regulated genes and green italics genes experiencing positive selection and increased expression. (1) AVPR2, expressed mainly in kidney tubules, primarily serves to respond to the pituitary hormone arginine vasopressin (AVP) to maintain water homeostasis; production of ALB can facilitate blood plasma volume expansion, which serves to regulate blood pressure. (2) AGT, PREP, ANPEP and CTSA play roles in the renin-angiotenin system pathway; NR3C2, PIK3CG, PDPK1 and SCNN1G associate with aldosterone-regulated sodium reabsorption pathway. (3) EHHADH provides energy for tubule reabsorption through the oxidation of fatty acids in the proximal tubule; ATP6V1G3 and ATP6V1F are v-type-H+ ATPases and they participate in Na+ uptake as energizers.
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f6: Interactions of positively selected genes and differentially expressed genes involved in the adaptation of F.cancrivora to high salinity.Red italics denote candidate positively selected genes, blue italics indicate significantly up-regulated genes and green italics genes experiencing positive selection and increased expression. (1) AVPR2, expressed mainly in kidney tubules, primarily serves to respond to the pituitary hormone arginine vasopressin (AVP) to maintain water homeostasis; production of ALB can facilitate blood plasma volume expansion, which serves to regulate blood pressure. (2) AGT, PREP, ANPEP and CTSA play roles in the renin-angiotenin system pathway; NR3C2, PIK3CG, PDPK1 and SCNN1G associate with aldosterone-regulated sodium reabsorption pathway. (3) EHHADH provides energy for tubule reabsorption through the oxidation of fatty acids in the proximal tubule; ATP6V1G3 and ATP6V1F are v-type-H+ ATPases and they participate in Na+ uptake as energizers.

Mentions: The renin-angiotensin-aldosterone system plays a primary role in the hormonal osmoregulation of amphibians13. In expression levels, except for ANPEP with its changes in sequence and expression, AGT, PREP and CTSA also exhibit significant enrichment and markedly higher levels of expressions. Among these genes, AGT encodes the precursor protein angiotensinogen40, CTSA encodes a protein involved in the conversion of angiotensin I to angiotensin II41 and PREP plays a role in the degradation of angiotensin I and II42. Thus, they are important candidate genes for participating in the maintenance of osmotic equilibrium. Importantly, NR3C2, PIK3CG, PDPK1 and SCNN1G, which associate with the aldosterone-regulated sodium reabsorption pathway as the downstream target pathway of renin-angiotensin system pathway, also possess significantly elevated levels of gene expression. In particular, NR3C2 encodes MR (mineralocorticoid receptor), which can be activated by mineralocorticoid-aldosterone to regulate Na+ homeostasis, largely through multiple mechanisms that modulate the activity of the epithelial Na+ channel (ENaC)43. Thus, the candidate genes of both pathways plus the candidate positively selected genes (Fig. 6) very likely constitute adaptations of crab-eating frog to their hypertonic environment. Further functional experimentation is necessary to verify this implication.


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)

Interactions of positively selected genes and differentially expressed genes involved in the adaptation of F.cancrivora to high salinity.Red italics denote candidate positively selected genes, blue italics indicate significantly up-regulated genes and green italics genes experiencing positive selection and increased expression. (1) AVPR2, expressed mainly in kidney tubules, primarily serves to respond to the pituitary hormone arginine vasopressin (AVP) to maintain water homeostasis; production of ALB can facilitate blood plasma volume expansion, which serves to regulate blood pressure. (2) AGT, PREP, ANPEP and CTSA play roles in the renin-angiotenin system pathway; NR3C2, PIK3CG, PDPK1 and SCNN1G associate with aldosterone-regulated sodium reabsorption pathway. (3) EHHADH provides energy for tubule reabsorption through the oxidation of fatty acids in the proximal tubule; ATP6V1G3 and ATP6V1F are v-type-H+ ATPases and they participate in Na+ uptake as energizers.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f6: Interactions of positively selected genes and differentially expressed genes involved in the adaptation of F.cancrivora to high salinity.Red italics denote candidate positively selected genes, blue italics indicate significantly up-regulated genes and green italics genes experiencing positive selection and increased expression. (1) AVPR2, expressed mainly in kidney tubules, primarily serves to respond to the pituitary hormone arginine vasopressin (AVP) to maintain water homeostasis; production of ALB can facilitate blood plasma volume expansion, which serves to regulate blood pressure. (2) AGT, PREP, ANPEP and CTSA play roles in the renin-angiotenin system pathway; NR3C2, PIK3CG, PDPK1 and SCNN1G associate with aldosterone-regulated sodium reabsorption pathway. (3) EHHADH provides energy for tubule reabsorption through the oxidation of fatty acids in the proximal tubule; ATP6V1G3 and ATP6V1F are v-type-H+ ATPases and they participate in Na+ uptake as energizers.
Mentions: The renin-angiotensin-aldosterone system plays a primary role in the hormonal osmoregulation of amphibians13. In expression levels, except for ANPEP with its changes in sequence and expression, AGT, PREP and CTSA also exhibit significant enrichment and markedly higher levels of expressions. Among these genes, AGT encodes the precursor protein angiotensinogen40, CTSA encodes a protein involved in the conversion of angiotensin I to angiotensin II41 and PREP plays a role in the degradation of angiotensin I and II42. Thus, they are important candidate genes for participating in the maintenance of osmotic equilibrium. Importantly, NR3C2, PIK3CG, PDPK1 and SCNN1G, which associate with the aldosterone-regulated sodium reabsorption pathway as the downstream target pathway of renin-angiotensin system pathway, also possess significantly elevated levels of gene expression. In particular, NR3C2 encodes MR (mineralocorticoid receptor), which can be activated by mineralocorticoid-aldosterone to regulate Na+ homeostasis, largely through multiple mechanisms that modulate the activity of the epithelial Na+ channel (ENaC)43. Thus, the candidate genes of both pathways plus the candidate positively selected genes (Fig. 6) very likely constitute adaptations of crab-eating frog to their hypertonic environment. Further functional experimentation is necessary to verify this implication.

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