The Consequences of Regulation of desat1 Expression for Pheromone Emission and Detection in Drosophila melanogaster by ProQuest


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									Copyright Ó 2010 by the Genetics Society of America
DOI: 10.1534/genetics.110.117226

    The Consequences of Regulation of desat1 Expression for Pheromone
             Emission and Detection in Drosophila melanogaster

                                             x                          x
                         Benjamin Houot, Francois Bousquet and Jean-Francois Ferveur1
        Centre des Sciences du Gout et de l’Alimentation, UMR6265 Centre National de la Recherche Scientifique, UMR1324 Institut
                   National de la Recherche Agronomique, Universite de Bourgogne, Agrosup Dijon, F-21000 Dijon, France
                                                        Manuscript received April 1, 2010
                                                      Accepted for publication May 12, 2010

               Sensory communication depends on the precise matching between the emission and the perception of
             sex- and species-specific signals; understanding both the coevolutionary process and the genes involved in
             both production and detection is a major challenge. desat1 determines both aspects of communication—a
             mutation in desat1 simultaneously alters both sex pheromone emission and perception in Drosophila
             melanogaster flies. We investigated whether the alteration of pheromonal perception is a consequence of
             the altered production of pheromones or if the two phenotypes are independently controlled by the same
             locus. Using several genetic tools, we were able to separately manipulate the two pheromonal phenotypes,
             implying that desat1 is the sole gene responsible, exerting a pleiotropic effect on both transmission and
             detection. The levels of the five desat1 trancripts, measured in the head and body of manipulated flies,
             were related to variation in pheromone production. This suggests that the pleiotropic action of desat1 on
             pheromonal communication depends on the fine regulation of its transcriptional activity.

P    HEROMONES are frequently used for sexual
       communication by vertebrate and invertebrates
alike (Bradbury and Vehrencamp 1998; Wyatt 2003).
                                                                           enes), which stimulate conspecific females and inhibit
                                                                           conspecific males (Jallon 1984; Ferveur and Sureau
                                                                           1996; Grillet et al. 2006; Lacaille et al. 2007). Females
In particular, pheromones play an important role                           produce dienes (with two double bonds), which slightly
in attraction and discrimination of sexual partners                        stimulate conspecific males but strongly inhibit males of
( Johansson and Jones 2007) and can be subjected to                        the sibling D. simulans species (Savarit et al. 1999). The
sexual selection (Darwin 1883). In moths, phero-                           biosynthesis of these sexually dimorphic CHs requires
mones can affect premating behavior (Roelofs and                           several desaturase enzymes that show sex- and species-
Rooney 2003; Smadja and Butlin 2009). Pheromones                           specific expression (Legendre et al. 2008). We pre-
have also been studied in several groups of Drosophila                     viously characterized the mutational effects of a specific
species (Toolson and Kupersimbron 1989; Tompkins                           PGal4 transposable element inserted in the regulatory
et al. 1993; Higgie et al. 2000; Ferveur 2005), including                  sequence of the desat1 gene (1573-1). This mutation
Drosophila melanogaster, a model species used to dissect                   affected not only the production of monoenes and
the molecular, genetic, physiological, neural, and evolu-                  dienes in male and female flies (Marcillac et al. 2005a)
tionary basis of pheromonal communication (Coyne et al.                    but also the male discrimination of sex pheromones
1994; Jallon and Wicker-Thomas 2003; Lacaille et al.                       (Marcillac et al. 2005b). The precise excision of the
2007; Koganezawa et al. 2010).                                             transposon completely rescued the two phenotypes,
   In moths, sex pheromone communication has                               demonstrating that desat1 can simultaneously affect
evolved to make use of complex blends of relatively                        the emission and the reception of sex pheromones.
simple long-chain fatty acid precursors and species                           To explore the genetic relationship between these
specificity is derived from the introduction of double                      two pheromo
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