Successful fertilization in angiosperms requires the growth of pollen tubes through the female reproductive tract as they seek out unfertilized ovules. In Arabidopsis , the reproductive tract begins with the stigma, where pollen grains initially adhere, and extends through the transmitting tract of the style and ovary. In wild-type plants, cells within the transmitting tract produce a rich extracellular matrix and undergo programmed cell death to facilitate pollen movement. Here, we show that the HAF, BEE1 and BEE3 genes encode closely related bHLH transcription factors that act redundantly to specify reproductive tract tissues. These three genes are expressed in distinct but overlapping patterns within the reproductive tract, and in haf bee1 bee3 triple mutants extracellular matrix formation and cell death fail to occur within the transmitting tract. We used a minimal pollination assay to show that HAF is necessary and sufficient to promote fertilization efficiency. Our studies further show that HAF expression depends on the NTT gene and on an auxin signaling pathway mediated by the ARF6, ARF8 and HEC genes.

The vertebrate nuclear hormone receptor steroidogenic factor 1 (SF1; NR5A1)controls reproductive development and regulates the transcription of steroid-modifying cytochrome P450 genes. We find that the SF1-related Drosophila nuclear hormone receptor HR39 is also essential for sexual development. In Hr39 mutant females, the sperm-storing spermathecae and glandular parovaria are absent or defective, causing sterility. Our results indicate that spermathecae and parovaria secrete reproductive tract proteins required for sperm maturation and function, like the mammalian epididymis and female reproductive tract. Hr39 controls the expression of specific cytochrome P450 genes and is required in females both to activate spermathecal secretion and repress male-specific courtship genes such as takeout . Thus, a pathway that, in vertebrates, controls sex-specific steroid hormone production, also mediates reproductive functions in an invertebrate. Our findings suggest that Drosophila can be used to model more aspects of mammalian reproductive biology than previously believed.