The PSI-U1 snRNP interaction regulates male mating behavior in Drosophila.
Alternative pre-mRNA splicing (AS) is a critical regulatory mechanism that operates extensively in the nervous system to produce diverse protein isoforms. Fruitless AS isoforms have been shown to influence male courtship behavior, but the underlying mechanisms are unknown. Using genome-wide approaches and quantitative behavioral assays, we show that the P-element somatic inhibitor (PSI) and its interaction with the U1 small nuclear ribonucleoprotein complex (snRNP) control male courtship behavior. PSI mutants lacking the U1 snRNP-interacting domain (PSIΔAB mutant) exhibit extended but futile mating attempts. The PSIΔAB mutant results in significant changes in the AS patterns of ∼1,200 genes in the Drosophila brain, many of which have been implicated in the regulation of male courtship behavior. PSI directly regulates the AS of at least one-third of these transcripts, suggesting that PSI-U1 snRNP interactions coordinate the behavioral network underlying courtship behavior. Importantly, one of these direct targets is fruitless, the master regulator of courtship. Thus, PSI imposes a specific mode of regulatory control within the neuronal circuit controlling courtship, even though it is broadly expressed in the fly nervous system. This study reinforces the importance of AS in the control of gene activity in neurons and integrated neuronal circuits, and provides a surprising link between a pleiotropic pre-mRNA splicing pathway and the precise control of successful male mating behavior.
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720; Center for RNA Systems Biology, University of California, Berkeley, CA 94720; California Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA 94720;
Qingqing
Q
Wang
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720;
J Matthew
JM
Taliaferro
Joseph Henry Laboratories of Physics and Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544.
Ugne
U
Klibaite
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720;
Valérie
V
Hilgers
Joseph Henry Laboratories of Physics and Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544.
Joshua W
JW
Shaevitz
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720; Center for RNA Systems Biology, University of California, Berkeley, CA 94720; California Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA 94720; don_rio@berkeley.edu.
Donald C
DC
Rio
D017398:Alternative Splicing / Q000502:physiology*; D000818:Animals; D003380:Courtship; D004330:Drosophila / Q000502:physiology*; D029721:Drosophila Proteins / Q000502:physiology*; D005260:Female; D017344:Genes, Insect / Q000502:physiology*; D008297:Male; D009419:Nerve Tissue Proteins / Q000502:physiology; D009687:Nuclear Proteins / Q000502:physiology*; D016601:RNA-Binding Proteins / Q000502:physiology*; D017412:Ribonucleoprotein, U1 Small Nuclear / Q000502:physiology*; D012727:Sex Characteristics; D012726:Sexual Behavior, Animal / Q000502:physiology*
D029721:Drosophila Proteins; D009419:Nerve Tissue Proteins; D009687:Nuclear Proteins; C092281:PSI protein, Drosophila; D016601:RNA-Binding Proteins; D017412:Ribonucleoprotein, U1 Small Nuclear
PSI; U1 snRNP; alternative pre-mRNA splicing; male courtship behavior