Abstract

In the postgenomics era, comparative genomics have advanced the understanding of evolutionary processes of neuropeptidergic signaling systems. The evolutionary origin of many neuropeptidergic signaling systems can be traced date back to early metazoan evolution based on the conserved sequences. Insect parathyroid hormone receptor (iPTHR) was previously described as an ortholog of vertebrate PTHR that has a well-known function in controlling bone remodeling. However, there was no sequence homologous to PTH sequence in insect genomes, leaving the iPTHR as an orphan receptor. Here, we identified the authentic ligand insect PTH (iPTH) for the iPTHR. The taxonomic distribution of iPTHR, which is lacking in Diptera and Lepidoptera, provided a lead for identifying the authentic ligand. We found that a previously described orphan ligand known as PXXXamide (where X is any amino acid) described in the cuttlefish Sepia officinalis has a similar taxonomic distribution pattern as iPTHR. Tests of this peptide, iPTH, in functional reporter assays confirmed the interaction of the ligand-receptor pair. Study of a model beetle, Tribolium castaneum, was used to investigate the function of the iPTH signaling system by RNA interference followed by RNA sequencing and phenotyping. The results suggested that the iPTH system is likely involved in the regulation of cuticle formation that culminates with a phenotype of defects in wing exoskeleton maturation at the time of adult eclosion. Moreover, RNAi of iPTHRs also led to significant reductions in egg numbers and hatching rates after parental RNAi.

Highlights

  • Discoveries of neuropeptides and their receptors in various taxa in the postgenomic era have provided nearly comprehensive lists that provide crucial information for understanding their evolutionary processes and physiological functions

  • Vertebrate parathyroid hormone (PTH) and its receptors have been extensively studied with respect to their function in bone remodeling and calcium metabolism

  • In our survey of insect PTH (iPTH), the neuropeptide originally described as PXXXamide [16], we identified iPTHs in many species of insect and in other arthropod taxa, but lacking in Diptera and Lepidoptera genome sequences

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Summary

Introduction

Discoveries of neuropeptides and their receptors in various taxa in the postgenomic era have provided nearly comprehensive lists that provide crucial information for understanding their evolutionary processes and physiological functions. The ligand PTH has undergone gene duplication and losses in vertebrates [9]. Likewise, our previous study has described two receptors in the red flour beetle, Tribolium castaneum, as an orthologous group similar to the PTH-receptors of vertebrates in the G protein-coupled receptor (GPCR) B group [13, 14]. The ligand for these receptors has not yet been identified [15]

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