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Functional phylogenetics reveals contributions of pleiotropic peptide action to ligand-receptor coevolution.

Jiang H, Wei Z, Nachman RJ, Adams ME, Park Y - Sci Rep (2014)

Bottom Line: The evolution of peptidergic signaling has been accompanied by a significant degree of ligand-receptor coevolution.Closely related clusters of peptide signaling molecules are observed to activate related groups of receptors, implying that genes encoding these ligands may orchestrate an array of functions, a phenomenon known as pleiotropy.Disparities between evolutionary trees deduced from receptor sequences vs. functional ligand-receptor specificities lead to the conclusion that pleiotropy exhibited by peptide genes influences ligand-receptor coevolution.

View Article: PubMed Central - PubMed

Affiliation: 1] Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, P. R. China [2] Department of Entomology, Kansas State University, Manhattan, Kansas 66506, United States.

ABSTRACT
The evolution of peptidergic signaling has been accompanied by a significant degree of ligand-receptor coevolution. Closely related clusters of peptide signaling molecules are observed to activate related groups of receptors, implying that genes encoding these ligands may orchestrate an array of functions, a phenomenon known as pleiotropy. Here we examine whether pleiotropic actions of peptide genes might influence ligand-receptor coevolution. Four test groups of neuropeptides characterized by conserved C-terminal amino acid sequence motifs and their cognate receptors were examined in the red flour beetle (Tribolium castaneum): 1) cardioacceleratory peptide 2b (CAPA); CAPAr, 2) pyrokinin/diapause hormone (PK1/DH); PKr-A, -B, 3) pyrokinin/pheromone biosynthesis activating hormone (PK2/PBAN); PKr-C, and 4) ecdysis triggering hormone (ETH); ETHr-b. Ligand-receptor specificities were established through heterologous expression of receptors in cell-based assays for 9 endogenous ligands. Based on ligand-receptor specificity analysis, we found positive pleiotropism exhibited by ETH on ETHR-b and CAPAr, whereas PK1/DH and CAPA are more highly selective for their respective authentic receptors than would be predicted by phylogenetic analysis. Disparities between evolutionary trees deduced from receptor sequences vs. functional ligand-receptor specificities lead to the conclusion that pleiotropy exhibited by peptide genes influences ligand-receptor coevolution.

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Dose-response curves of five different PRXamide receptors of T. castaneum for nine endogenous ligands.Left panel shows dose-response curves for each receptor with 9 putative endogenous ligands. Right panel shows names of ligands and their EC50s in rank order. Values of data points are found in Supplementary Data 1.
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f3: Dose-response curves of five different PRXamide receptors of T. castaneum for nine endogenous ligands.Left panel shows dose-response curves for each receptor with 9 putative endogenous ligands. Right panel shows names of ligands and their EC50s in rank order. Values of data points are found in Supplementary Data 1.

Mentions: We characterized all PRXamide GPCRs through assays of 9 endogenous ligands. Ligand activities were quantified by detection of luminescence responses from CHO cells transiently transfected with GPCR (see Methods and Materials section for details). Dose-response curves were generated by logistic fitting of the log transformed ligand concentrations ranging from 0.01 nM to 10 μM (Fig. 3). All results, shown as averages, were replicated in three independent experiments (see Supplementary Data 1 for details). TcETHr-b, a splicing variant used in this study, showed relatively lower activity than those of other receptors, likely due to inefficient coupling to the reporter system.


Functional phylogenetics reveals contributions of pleiotropic peptide action to ligand-receptor coevolution.

Jiang H, Wei Z, Nachman RJ, Adams ME, Park Y - Sci Rep (2014)

Dose-response curves of five different PRXamide receptors of T. castaneum for nine endogenous ligands.Left panel shows dose-response curves for each receptor with 9 putative endogenous ligands. Right panel shows names of ligands and their EC50s in rank order. Values of data points are found in Supplementary Data 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4210869&req=5

f3: Dose-response curves of five different PRXamide receptors of T. castaneum for nine endogenous ligands.Left panel shows dose-response curves for each receptor with 9 putative endogenous ligands. Right panel shows names of ligands and their EC50s in rank order. Values of data points are found in Supplementary Data 1.
Mentions: We characterized all PRXamide GPCRs through assays of 9 endogenous ligands. Ligand activities were quantified by detection of luminescence responses from CHO cells transiently transfected with GPCR (see Methods and Materials section for details). Dose-response curves were generated by logistic fitting of the log transformed ligand concentrations ranging from 0.01 nM to 10 μM (Fig. 3). All results, shown as averages, were replicated in three independent experiments (see Supplementary Data 1 for details). TcETHr-b, a splicing variant used in this study, showed relatively lower activity than those of other receptors, likely due to inefficient coupling to the reporter system.

Bottom Line: The evolution of peptidergic signaling has been accompanied by a significant degree of ligand-receptor coevolution.Closely related clusters of peptide signaling molecules are observed to activate related groups of receptors, implying that genes encoding these ligands may orchestrate an array of functions, a phenomenon known as pleiotropy.Disparities between evolutionary trees deduced from receptor sequences vs. functional ligand-receptor specificities lead to the conclusion that pleiotropy exhibited by peptide genes influences ligand-receptor coevolution.

View Article: PubMed Central - PubMed

Affiliation: 1] Key Laboratory of Entomology and Pest Control Engineering, College of Plant Protection, Southwest University, Chongqing 400715, P. R. China [2] Department of Entomology, Kansas State University, Manhattan, Kansas 66506, United States.

ABSTRACT
The evolution of peptidergic signaling has been accompanied by a significant degree of ligand-receptor coevolution. Closely related clusters of peptide signaling molecules are observed to activate related groups of receptors, implying that genes encoding these ligands may orchestrate an array of functions, a phenomenon known as pleiotropy. Here we examine whether pleiotropic actions of peptide genes might influence ligand-receptor coevolution. Four test groups of neuropeptides characterized by conserved C-terminal amino acid sequence motifs and their cognate receptors were examined in the red flour beetle (Tribolium castaneum): 1) cardioacceleratory peptide 2b (CAPA); CAPAr, 2) pyrokinin/diapause hormone (PK1/DH); PKr-A, -B, 3) pyrokinin/pheromone biosynthesis activating hormone (PK2/PBAN); PKr-C, and 4) ecdysis triggering hormone (ETH); ETHr-b. Ligand-receptor specificities were established through heterologous expression of receptors in cell-based assays for 9 endogenous ligands. Based on ligand-receptor specificity analysis, we found positive pleiotropism exhibited by ETH on ETHR-b and CAPAr, whereas PK1/DH and CAPA are more highly selective for their respective authentic receptors than would be predicted by phylogenetic analysis. Disparities between evolutionary trees deduced from receptor sequences vs. functional ligand-receptor specificities lead to the conclusion that pleiotropy exhibited by peptide genes influences ligand-receptor coevolution.

Show MeSH
Related in: MedlinePlus