The PSI-U1 snRNP interaction regulates male mating behavior in Drosophila.

TitleThe PSI-U1 snRNP interaction regulates male mating behavior in Drosophila.
Publication TypeJournal Article
Year of Publication2016
AuthorsWang, Q, J Taliaferro, M, Klibaite, U, Hilgers, V, Shaevitz, JW, Rio, DC
JournalProc Natl Acad Sci U S A
Volume113
Issue19
Pagination5269-74
Date Published2016 May 10
ISSN1091-6490
KeywordsAlternative Splicing, Animals, Courtship, Drosophila, Drosophila Proteins, Female, Genes, Insect, Male, Nerve Tissue Proteins, Nuclear Proteins, Ribonucleoprotein, U1 Small Nuclear, RNA-Binding Proteins, Sex Characteristics, Sexual Behavior, Animal
Abstract

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.

DOI10.1073/pnas.1600936113
Alternate JournalProc. Natl. Acad. Sci. U.S.A.
PubMed ID27114556
PubMed Central IDPMC4868454
Grant ListR01 GM094890 / GM / NIGMS NIH HHS / United States
R01 GM097352 / GM / NIGMS NIH HHS / United States
R01 GM098090 / GM / NIGMS NIH HHS / United States
T32 HG003284 / HG / NHGRI NIH HHS / United States