Transcriptomic analysis of regulatory pathways involved in female reproductive physiology of Rhodnius prolixus under different nutritional states

Jimena Leyria,Ian Orchard,Angela B Lange

doi:10.1038/s41598-020-67932-4

Abstract

The triatomine Rhodnius prolixus, a vector of the etiological agent of Chagas disease, has long been used as model to understand important aspects of insect physiology. Despite this history, the impact of the nutritional state on regulatory pathways associated with reproductive performance in triatomines has never been studied. The insulin-like peptide/target of rapamycin (ILP/ToR) signaling pathway is typically responsible for detecting and interpreting nutrient levels. Here, we analyzed transcriptomes from the central nervous system, fat bodies and ovaries of adult females in unfed and fed conditions, with a focus on the ILP/ToR signaling. The results show an up-regulation of transcripts involved in ILP/ToR signaling in unfed insects. However, we demonstrate that this signaling is only activated in tissues from fed insects. Moreover, we report that FoxO (forkhead box O) factor, which regulates longevity via ILP signaling, is responsible for the up-regulation of transcripts related with ILP/ToR signaling in unfed insects. As a consequence, we reveal that unfed females are in a sensitized state to respond to an increase of ILP levels by rapidly activating ILP/ToR signaling. This is the first analysis that correlates gene expression and protein activation of molecules involved with ILP/ToR signaling in R. prolixus females in different nutritional states.

Highlights

The triatomine Rhodnius prolixus, a vector of the etiological agent of Chagas disease, has long been used as model to understand important aspects of insect physiology
This is the first analysis to correlate gene expression and protein activation involved with insulin-like peptide/target of rapamycin (ILP/target of rapamycin (ToR)) signaling in R. prolixus females in different nutritional conditions
In the fat bodies (FB), 28 transcripts involved with insulin-like peptides (ILPs)/ToR signaling were analyzed, and 9 are up-regulated in the unfed condition (UFC) (Table 3), including InR, venus kinase receptor (VKR), insulin receptor substrate 1 (IRS1), phosphatase and tensin homolog (PTEN), ribosomal protein S6 kinase (S6) and insulin growth factor (IGF)

Summary

Introduction

The triatomine Rhodnius prolixus, a vector of the etiological agent of Chagas disease, has long been used as model to understand important aspects of insect physiology. This is the first analysis to correlate gene expression and protein activation involved with ILP/ToR signaling in R. prolixus females in different nutritional conditions. In the FB, 28 transcripts involved with ILP/ToR signaling were analyzed, and 9 are up-regulated in the UFC (Table 3), including InR, venus kinase receptor (VKR), insulin receptor substrate 1 (IRS1), phosphatase and tensin homolog (PTEN), ribosomal protein S6 kinase (S6) and IGF.

Results

Conclusion