Abstract
In fruit flies, the male-specific fruitless (fru) gene product FruBM plays a central role in establishing the neural circuitry for male courtship behavior by orchestrating the transcription of genes required for the male-type specification of individual neurons. We herein identify the core promoter recognition factor gene Trf2 as a dominant modifier of fru actions. Trf2 knockdown in the sexually dimorphic mAL neurons leads to the loss of a male-specific neurite and a reduction in male courtship vigor. TRF2 forms a repressor complex with FruBM, strongly enhancing the repressor activity of FruBM at the promoter region of the robo1 gene, whose function is required for inhibiting the male-specific neurite formation. In females that lack FruBM, TRF2 stimulates robo1 transcription. Our results suggest that TRF2 switches its own role from an activator to a repressor of transcription upon binding to FruBM, thereby enabling the ipsilateral neurite formation only in males.
Highlights
In fruit flies, the male-specific fruitless gene product FruBM plays a central role in establishing the neural circuitry for male courtship behavior by orchestrating the transcription of genes required for the male-type specification of individual neurons
By focusing on the fru-expressing neuronal cluster mAL, which displays sexual dimorphisms in the cell number, the contralateral neurite branching pattern, and the presence or absence of the ipsilateral neurite[28], we successfully demonstrated that the core promoter regulator TRF2-S preferentially supports FruBM in the male-specific ipsilateral neurite formation, with only minor effects on two other aspects of mAL sexual dimorphisms
TRF2-S was found to assist FruBM by enhancing the repressor effect of FruBM on the promoter of robo[1], the gene encoding a receptor for the axon guidance factor that inhibits the male-specific neurite formation in mAL neurons[27]
Summary
The male-specific fruitless (fru) gene product FruBM plays a central role in establishing the neural circuitry for male courtship behavior by orchestrating the transcription of genes required for the male-type specification of individual neurons. TRF2 forms a repressor complex with FruBM, strongly enhancing the repressor activity of FruBM at the promoter region of the robo[1] gene, whose function is required for inhibiting the male-specific neurite formation. Our results suggest that TRF2 switches its own role from an activator to a repressor of transcription upon binding to FruBM, thereby enabling the ipsilateral neurite formation only in males. The female and male of a sexually reproducing animal are, in principle, different from each other in structure and function at the molecular, cellular, and organismal levels. The fruit fly Drosophila melanogaster, an excellent model for studying the genetic organization of complex traits, shows remarkable sexual dimorphisms in many aspects of its structure and function, including its behavior[2].
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