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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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Three genes encoding –PRXamide peptide in the T. castaneum (a) and abdominal segments of a larva showing endocrine organs for ETH and CAPA visualized by immunohistochemistry (b).(a) Schematic diagrams for CAPA, PBAN, and ETH genes are shown on the top line of each gene product. Mature peptides are shown as color coded boxes for each peptide family. Empty boxes to the left in each diagram indicate signal peptides. Sequences for each putative mature peptide are aligned according to conserved C-terminal amino acid sequence motifs marked in bold. The italic used in the N-terminus of sequence ETH-2 indicates uncertainty with the canonical cleavage signal in the middle of the ETH-2 as GK. This study used the shorter version of ETH-2 starting with FFM in the alternative predictions. (b) Immunostaining of –PRXamide-expressing neurons. The top inset is a schematic diagram depicting stained elements visible below. Ventral larval abdominal segments are shown for the CNS and trachea containing the cells for CAPA and for ETH (Inka cell), respectively, and for the perisympathetic organ, which serves as a neurohemal release site for the neuropeptide CAPA.
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f1: Three genes encoding –PRXamide peptide in the T. castaneum (a) and abdominal segments of a larva showing endocrine organs for ETH and CAPA visualized by immunohistochemistry (b).(a) Schematic diagrams for CAPA, PBAN, and ETH genes are shown on the top line of each gene product. Mature peptides are shown as color coded boxes for each peptide family. Empty boxes to the left in each diagram indicate signal peptides. Sequences for each putative mature peptide are aligned according to conserved C-terminal amino acid sequence motifs marked in bold. The italic used in the N-terminus of sequence ETH-2 indicates uncertainty with the canonical cleavage signal in the middle of the ETH-2 as GK. This study used the shorter version of ETH-2 starting with FFM in the alternative predictions. (b) Immunostaining of –PRXamide-expressing neurons. The top inset is a schematic diagram depicting stained elements visible below. Ventral larval abdominal segments are shown for the CNS and trachea containing the cells for CAPA and for ETH (Inka cell), respectively, and for the perisympathetic organ, which serves as a neurohemal release site for the neuropeptide CAPA.

Mentions: The insect PRXamide cluster includes four families of neuropeptides (Fig. 1a): cardioacceleratory peptide 2b (hereafter named as CAPA), pyrokinin/diapausing hormone (PK1/DH or PK1), pyrokinin/pheromone biosynthesis activating hormone (PK2/PBAN or PK2), and ecdysis triggering hormone (ETH). Functions of this peptide group have been intensively studied over the past several decades, although information remains fragmented in some insect species and is limited to results from a few specific physiological assays, often chosen for ease of use rather than authentic physiological function(s) that are often unknown. It is notable that PRXamide peptides are predominantly hormonal signaling molecules, which allows for interactions with a broad diversity of receptors and for possible evolutionary selection based on adaptive influences of pleiotropism.


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)

Three genes encoding –PRXamide peptide in the T. castaneum (a) and abdominal segments of a larva showing endocrine organs for ETH and CAPA visualized by immunohistochemistry (b).(a) Schematic diagrams for CAPA, PBAN, and ETH genes are shown on the top line of each gene product. Mature peptides are shown as color coded boxes for each peptide family. Empty boxes to the left in each diagram indicate signal peptides. Sequences for each putative mature peptide are aligned according to conserved C-terminal amino acid sequence motifs marked in bold. The italic used in the N-terminus of sequence ETH-2 indicates uncertainty with the canonical cleavage signal in the middle of the ETH-2 as GK. This study used the shorter version of ETH-2 starting with FFM in the alternative predictions. (b) Immunostaining of –PRXamide-expressing neurons. The top inset is a schematic diagram depicting stained elements visible below. Ventral larval abdominal segments are shown for the CNS and trachea containing the cells for CAPA and for ETH (Inka cell), respectively, and for the perisympathetic organ, which serves as a neurohemal release site for the neuropeptide CAPA.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: Three genes encoding –PRXamide peptide in the T. castaneum (a) and abdominal segments of a larva showing endocrine organs for ETH and CAPA visualized by immunohistochemistry (b).(a) Schematic diagrams for CAPA, PBAN, and ETH genes are shown on the top line of each gene product. Mature peptides are shown as color coded boxes for each peptide family. Empty boxes to the left in each diagram indicate signal peptides. Sequences for each putative mature peptide are aligned according to conserved C-terminal amino acid sequence motifs marked in bold. The italic used in the N-terminus of sequence ETH-2 indicates uncertainty with the canonical cleavage signal in the middle of the ETH-2 as GK. This study used the shorter version of ETH-2 starting with FFM in the alternative predictions. (b) Immunostaining of –PRXamide-expressing neurons. The top inset is a schematic diagram depicting stained elements visible below. Ventral larval abdominal segments are shown for the CNS and trachea containing the cells for CAPA and for ETH (Inka cell), respectively, and for the perisympathetic organ, which serves as a neurohemal release site for the neuropeptide CAPA.
Mentions: The insect PRXamide cluster includes four families of neuropeptides (Fig. 1a): cardioacceleratory peptide 2b (hereafter named as CAPA), pyrokinin/diapausing hormone (PK1/DH or PK1), pyrokinin/pheromone biosynthesis activating hormone (PK2/PBAN or PK2), and ecdysis triggering hormone (ETH). Functions of this peptide group have been intensively studied over the past several decades, although information remains fragmented in some insect species and is limited to results from a few specific physiological assays, often chosen for ease of use rather than authentic physiological function(s) that are often unknown. It is notable that PRXamide peptides are predominantly hormonal signaling molecules, which allows for interactions with a broad diversity of receptors and for possible evolutionary selection based on adaptive influences of pleiotropism.

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