Sexual dimorphism varies enormously from the morphologically indistinct yeast mating types, to extreme differences that can lead to the misclassification of males and females as distinct species. While the Drosophila
sexes show relatively modest sexually dimorphic somatic body plans there is striking sexual dimorphism in the germline [1
]. Indeed, it is difficult to imagine cell types that differ more than eggs and sperm. During the last century a handful of genes involved in the regulation of somatic (for example, Sex-lethal
]) and germline sexual identity (for example, ovo
], sans fille
], ovarian tumor
], and stand still
]) have been identified, but we know very little about the effector genes that actually result in a sexually dimorphic state. Major terminal genes in the current models of somatic and germline sex determination are a transcription factor (doublesex
) and an RNA binding protein (Sex-lethal
]. These molecules must orchestrate a cascade of effector functions that result in sexually dimorphic gametes and the somatic support functions required for their union at fertilization.
Whilst we know relatively little about how germline sexual identity is determined in Drosophila
, the downstream process of oogenesis has been well studied. Egg production occurs in the ovary [13
]; each ovary consists of a cluster of 16-20 ovarioles where the assembly line-like production of germline and somatic cell units (egg chambers) progresses along the length of the ovariole. The germline component of each egg chamber contains the differentiated products of a single germline stem cell division. The differentiating stem cell daughter undergoes four rounds of incomplete cytokinesis to produce an interconnected 16-cell cyst surrounded by a somatic follicular epithelium.
One of these 16 germline cells becomes the oocyte and the remaining 15 cells develop into supporting nurse cells. The 16-germline cells within cysts are connected by an intercellular network facilitating the active transport of macromolecules from the nurse cells into the growing oocyte. These components include basic cellular machinery such as ribosomes, and a vast assortment of proteins and RNA species that support early embryonic development. For example, the dorsal/ventral and anterior/posterior axes of the future embryo are laid down during oogenesis [14
]. The somatic follicular epithelium surrounding each egg chamber is an important source of structural proteins, such as yolk and egg shell proteins, that become incorporated into the oocyte, as well as patterning information. Most of the yolk proteins are produced distantly in non-gonadal fat body tissue [15
]. Thus, while much of the egg is constructed by the cells of the egg chamber, there is significant contribution from distant organs. Finally, additional somatic functions in the female reproductive tract and female mating behaviors are required for productive gamete function [16
]. A global analysis of gene expression in adult females therefore captures the genes required for all of the stages of oogenesis from stem cell to early embryo.
Analogously, the Drosophila
testis contains developing gametes, from the stem cells at the apical tip of the testis to fully functional sperm [17
]. As in the ovary, the germline stem cell division in the testis produces cysts of 16 primary spermatocytes. However, in males all these primary spermatocytes undergo meiosis resulting in a cyst of 64 spermatids. Each spermatid then follows an elaborate differentiation program of cytoskeletal and nuclear rearrangements to form a mature sperm cell. These changes are quite remarkable. For example, sperm chromatin is nearly crystalline and the nucleus changes from a round structure to a highly elongated and slightly hooked shape. Cytoskeletal rearrangement is equally dramatic. The round spermatid forms a flagellar axoneme that is nearly half the length of the adult. Mitochondrial differentiation in the axoneme is also striking. Individual mitochondria fuse into two large and interleaved structures extending along the length of the flagellum. Thus, while the structure of a sperm cell might suggest a simplistic developmental program for spermatogenesis (DNA and a motor), shedding the features that characterize virtually all other cells in the body (such as packing DNA into nucleosomes) is an enormous reengineering feat. As is the case in females, the male reproductive tract and male behavior are required for fertility [18
]. Therefore a global analysis of gene expression in adult males captures the genes required for all of the stages of spermatogenesis from stem cell to the fertilized egg.
Not surprisingly, both genetic and classic molecular studies indicate that spermatogenesis and oogenesis are complex events requiring extensive and often sex-specifically deployed information [13
]. More recently, global gene expression studies using printed cDNAs, expressed sequence tags (ESTs), and full transcriptome microarrays have revealed extensive overall sex differential expression [19
], with gene expression in the germline and gonads being particularly striking [19
]. Here we report gene expression profiles as a function of sexual dimorphism and sex determination in Drosophila
as analyzed using a platform including 93% of predicted genes from version 1.0 of the Drosophila
] and 75% of release 3.1. This article includes the dataset from Parisi et al.
] on gene expression in adults, augmented with additional microarray experiments to further track the source of sexually dimorphic expression.
There are many stories embedded in the expression data reported here. We touch on only a few to illustrate the value of the dataset. The most significant aspect of the survey we report here is the creation of a dataset that can be mined by other researchers interested in gametogenesis and sexual dimorphism. To that end, genes showing differential expression have been organized into easy to browse tables that include internet links to FlyBase [26
], the compendium of genome information for Drosophila
. We have also deposited all the data at the Gene Expression Omnibus [28
] so that those interested in large-scale reanalysis can easily download the entire dataset.