The role of the glucose-sensing transcription factor carbohydrate-responsive element-binding protein pathway in termite queen fertility.

David Sillam-Dussès,Maryline Favier,Michael Poulsen,Mireille Vasseur-Cognet,Robert Hanus,Virginie Roy

doi:10.1098/rsob.160080

Abstract

Termites are among the few animals that themselves can digest the most abundant organic polymer, cellulose, into glucose. In mice and Drosophila, glucose can activate genes via the transcription factor carbohydrate-responsive element-binding protein (ChREBP) to induce glucose utilization and de novo lipogenesis. Here, we identify a termite orthologue of ChREBP and its downstream lipogenic targets, including acetyl-CoA carboxylase and fatty acid synthase. We show that all of these genes, including ChREBP, are upregulated in mature queens compared with kings, sterile workers and soldiers in eight different termite species. ChREBP is expressed in several tissues, including ovaries and fat bodies, and increases in expression in totipotent workers during their differentiation into neotenic mature queens. We further show that ChREBP is regulated by a carbohydrate diet in termite queens. Suppression of the lipogenic pathway by a pharmacological agent in queens elicits the same behavioural alterations in sterile workers as observed in queenless colonies, supporting that the ChREBP pathway partakes in the biosynthesis of semiochemicals that convey the signal of the presence of a fertile queen. Our results highlight ChREBP as a likely key factor for the regulation and signalling of queen fertility.

Highlights

Glucose is the most widely used sugar in animals, serving in energy production and in the provision of macromolecular precursors, and glucose is a signalling molecule in the liver and fat tissues [1]
We have shown that the transcription factor carbohydrate-responsive element-binding protein (ChREBP), an evolutionarily conserved glucose sensor that regulates gene expression to drive fatty-acid biosynthesis in mice and in the fruit fly, has a unique expression profile in termites, which are the oldest social insects
ChREBP is highly expressed in mature reproductive females of eight different termite species, compared with reproductive males and sterile worker and soldier individuals

Summary

Introduction

Glucose is the most widely used sugar in animals, serving in energy production and in the provision of macromolecular precursors, and glucose is a signalling molecule in the liver and fat tissues [1]. ChREBP-deficient mice have impaired activation of glucoseinduced target genes as well as a number of dysregulated metabolic phenotypes, including elevated plasma glucose and liver glycogen levels and reduced adiposity [14]. These mice survive poorly on high-sugar diets [14]. Because of the essential role of this transcription factor in the Drosophila fat body [16,17], the counterpart of mammalian liver and adipose tissue, it has been proposed that the liver and adipose tissue-specific ChREBP, rather than the muscle-specific Mondo A, represents the ancestral function of the protein [16]

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Conclusion