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.

Centre for Social Evolution Section for Ecology and Evolution Department of Biology University of Copenhagen 2100 Copenhagen East Denmark

Institut National de la Santé et de la Recherche Médicale Unité 1016 Institut Cochin 75014 Paris France

Institute of Organic Chemistry and Biochemistry Academy of Sciences of the Czech Republic 16610 Prague Czech Republic

Laboratoire d'Ethologie Expérimentale et Comparée Université Paris 13 EA4443 93430 Villetaneuse France UMR IRD 242 UPEC CNRS 7618 UPMC 113 INRA 1392 PARIS 7 113 Institut d'Ecologie et des Sciences de l'Environnement de Paris 93140 Bondy France Sorbonne Paris Cité Paris France Sorbonne Universités Paris France

UMR IRD 242 UPEC CNRS 7618 UPMC 113 INRA 1392 PARIS 7 113 Institut d'Ecologie et des Sciences de l'Environnement de Paris 93140 Bondy France Sorbonne Paris Cité Paris France Sorbonne Universités Paris France

UMR IRD 242 UPEC CNRS 7618 UPMC 113 INRA 1392 PARIS 7 113 Institut d'Ecologie et des Sciences de l'Environnement de Paris 93140 Bondy France Sorbonne Paris Cité Paris France Sorbonne Universités Paris France Institut National de la Santé et de la Recherche Médicale Unité 1016 Institut Cochin 75014 Paris France

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Open Biol. 2016 Oct;6(10):160237. doi: 10.1098/rsob.160237. PubMed

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