Cellular and Behavioral Functions of fruitless Isoforms in Drosophila Courtship

Philipsborn, Anne C. von; Jörchel, Sabrina; Tirián, László; Demir, Ebru; Morita, Tomoko; Stern, David L.; Dickson, Barry J.

doi:10.1016/j.cub.2013.12.015

Cited by 82 publications

(100 citation statements)

References 45 publications

(48 reference statements)

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“…This quantitative comparison revealed 1,170 genes (identified by at least two independent computational methods) whose mRNA transcript splicing patterns were altered in PSIΔAB flies versus the full-length PSI strain. The PSIΔAB mutant affects the AS of the three male-specific fruitless mRNA isoforms that are functionally distinct for maintaining normal male courtship behavior (cruciality fru-C > fru-B > fru-A) (17). Here the 5′ and 3′ ends of the fruitless pre-mRNA are shown.…”

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

“…3D) (17). Each of the three transcripts differs from the others by only the last coding exon that encodes distinct zinc finger DNA binding domains, respectively, so that the fru-A, fru-B, and fru-C proteins can each potentially affect the expression of distinct sets of downstream target genes (17). Among them, the fru-C mRNA isoform was found to be the most important for normal male courtship behavior, fru-B less crucial than fru-C, and fru-A the least important (17).…”

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

“…Each of the three transcripts differs from the others by only the last coding exon that encodes distinct zinc finger DNA binding domains, respectively, so that the fru-A, fru-B, and fru-C proteins can each potentially affect the expression of distinct sets of downstream target genes (17). Among them, the fru-C mRNA isoform was found to be the most important for normal male courtship behavior, fru-B less crucial than fru-C, and fru-A the least important (17). Remarkably, the levels of fru-C and fru-B among the three isoforms significantly decreased in the PSIΔAB male fly heads compared with the fulllength PSI, consistent with the observed courtship behavior defects (Fig.…”

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

“…Specifically, AS further generates three functionally distinct male-specific fruitless transcripts (termed fru-A, fru-B, and fru-C), whose relative levels are critical in maintaining normal male courtship behavior (Fig. 3D) (17). Each of the three transcripts differs from the others by only the last coding exon that encodes distinct zinc finger DNA binding domains, respectively, so that the fru-A, fru-B, and fru-C proteins can each potentially affect the expression of distinct sets of downstream target genes (17).…”

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

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The PSI–U1 snRNP interaction regulates male mating behavior in Drosophila

Wang

Taliaferro

Klibaite

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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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.PSI | U1 snRNP | alternative pre-mRNA splicing | male courtship behavior H ow gene regulation modulates neuronal activities leading to cognition and behavior is an important question in biology. Although many behavior-associated genes and neuronal cell types have been identified, a detailed understanding that links the molecular events of gene regulation to specific behaviors is still lacking. Alternative pre-mRNA splicing (AS) is a crucial gene regulatory mechanism that enables a single gene to generate functionally distinct messenger RNA transcripts (mRNAs) and protein products (1). The nervous system makes extensive use of AS to generate diverse and complex neural mRNA expression patterns that determine numerous neuronal cell types and functions (2). AS is regulated by the small nuclear ribonucleoprotein complexes (snRNPs) that compose the spliceosome for intron recognition and removal, as well as a large repertoire of non-snRNP RNA-binding proteins that affect decisions on splice site use (3). This dynamic and complex AS regulatory network modulates diverse neuronal functions, like synaptic transmission and signal processing, hence further impacting higher brain functions, such as cognition and behavioral control (4).The Drosophila KH-domain RNA binding splicing factor P-element somatic inhibitor (PSI) is best known for regulating tissue-specific AS of the Drosophila P-element transposon transcripts to restrict transposition activity to germ-line tissues (5, 6). PSI directly interacts with the U1 snRNP through a 70-aa tandem direct ...

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Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

Section: Psi Is Broadly Expressed In Both Male and Female Drosophila mentioning

confidence: 99%

See 2 more Smart Citations

The PSI–U1 snRNP interaction regulates male mating behavior in Drosophila

Wang

Taliaferro

Klibaite

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Interestingly, enzymes (or their mRNAs) can also undergo AS and have isoform-specific effects on neurons, as exemplified by AS of Nmnat , resulting in isoforms with different abilities to protect neurons under stress [Ruan et al, 2015]. Studies on the sex-specific isoforms of Dsx and Fru illustrate their potential to shape sexually dimorphic neural circuits that enable the fly to perform sex-specific behaviors [Lee et al, 2002;Billeter et al, 2006;Sanders and Arbeitman, 2008;Rideout et al, 2010;von Philipsborn et al, 2011von Philipsborn et al, , 2014Rezával et al, 2012;Yamamoto and Koganezawa, 2013]. However, not all behavioral and anatomical differences can be explained by fru and/or dsx , suggesting that other factors contribute to sexual dimorphic behaviors and structures [Yamamoto and Koganezawa, 2013].…”

Section: Sex-specific Isoforms Of Tango13 Affect Courtship and Matingmentioning

confidence: 99%

Sex-Specific Transcript Diversity in the Fly Head Is Established during Pupal Stages and Adulthood and Is Largely Independent of the Mating Process and the Germline

Mohr¹,

Kleiner

Blanchette

et al. 2017

Sex Dev

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Alternative splicing (AS), the process which generates multiple RNA and protein isoforms from a single pre-mRNA, greatly contributes to transcript diversity and compensates for the fact that the gene number does not scale with organismal complexity. A number of genomic approaches have established that the extent of AS is much higher than previously expected, raising questions on its spatio-temporal regulation and function. In the present study, we address AS in the context of sex-specific neuronal development in the model Drosophila melanogaster. We report that at least 47 genes display sex-specific AS in the adult fly head. Unlike targets of the classical Sex lethal-dependent sex determination cascade, sex-specific isoforms of the vast majority of these genes are not present during larval development but start accumulating during metamorphosis or later, indicating the existence of novel mechanisms in the induction of sex-specific AS. We also established that sex-specific AS in the adult fly head is largely independent of the germline or the mating process. Finally, we investigated the role of sex-specific AS of the sulfotransferase Tango13 pre-mRNA and provide first evidence that differential expression of certain isoforms of this protein significantly affects courtship and mating behavior in male flies.

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Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

Kerwin

Philipsborn

2020

BioEssays

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Drosophila males sing a courtship song to achieve copulations with females. Females were recently found to sing a distinct song during copulation, which depends on male seminal fluid transfer and delays female remating. Here, it is hypothesized that female copulation song is a signal directed at the copulating male and changes ejaculate allocation. This may alter female remating and sperm usage, and thereby affect postcopulatory mate choice. Mechanisms of how female copulation song is elicited, how males respond to copulation song, and how remating is modulated, are considered. The potential adaptive value of female signaling during copulation is discussed with reference to vertebrate copulation calls and their proposed function in eliciting mate guarding. Female copulation song may be widespread within the Drosophila genus. This newly discovered behavior opens many interesting avenues for future research, including investigation of how sexually dimorphic neuronal circuits mediate communication between nervous system and reproductive organs.

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Cellular and Behavioral Functions of fruitless Isoforms in Drosophila Courtship

Cited by 82 publications

References 45 publications

The PSI–U1 snRNP interaction regulates male mating behavior in Drosophila

The PSI–U1 snRNP interaction regulates male mating behavior in Drosophila

Sex-Specific Transcript Diversity in the Fly Head Is Established during Pupal Stages and Adulthood and Is Largely Independent of the Mating Process and the Germline

Copulation Song inDrosophila: Do Females Sing to Change Male Ejaculate Allocation and Incite Postcopulatory Mate Choice?

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