Two central processes in the development of metazoans are the production of multiple cell types and the morphogenesis of complex multicellular structures. Morphogenesis requires that reproducible homotypic and heterotypic cellular contacts and interactions be established following precise cell recognition

Two central processes in the development of metazoans are the production of multiple cell types and the morphogenesis of complex multicellular structures. Morphogenesis requires that reproducible homotypic and heterotypic cellular contacts and interactions be established following precise cell recognition events. In such morphogenetic interactions, cells of a single overt cell type may not all act the same. Pattern forming mechanisms that generate non-equivalent cell properties thus play a crucial role in establishment of the form of the organism. This process is particularly acute in development of the nervous system, where neurons acquire distinct characteristics necessary to generate a complex network of cell contacts. We have been studying development and morphogenesis of the copulatory structures of the C. elegans male tail (Emmons, 1992). Because its cellular structure is completely defined (Wood, 1988), C. elegans provides an opportunity for investigating, in detail, the relationship between pattern formation and morphogenesis. We have shown previously that the distinctive arrangement of sense organs in the male tail is dependent on a pattern formation mechanism in the epidermis (Baird et al., 1991). This pattern formation mechanism generates differences between cells of the peripheral nervous system necessary for organelle assembly at reproducible positions. Here we show that two genes encoding Antennapedia-class homeodomain transcription factors, members of the C. elegans HOM-C/Hox gene cluster, as well as several genetic modifiers of HOM-C/Hox gene mutations, play a role in the pattern formation mechanism. The C. elegans epidermis consists of a large syncytium covering most of the body, distinctly shaped cells and syncytia constructing the head and tail regions, and left and right lateral rows of seam cells (White, 1988). The male-specific sense organs that are the subject of this paper are generated by seam cells. At hatching, there are nine seam cells arrayed in single file on each side of the body. During postembryonic development, seam cells generally divide in a stem cell pattern to generate an anterior daughter that fuses with the large hypodermal syncytium, and a posterior daughter that remains as a seam cell (Sulston and Horvitz, 1977; Fig. 1A). In certain regions of the body, however, seam cells generate neuroblasts. Seam cell lineages can therefore serve as a model to study the mechanism of axial pattern formation in C. elegans. During the L1 larval stage in both sexes, the embryonic seam cell T generates the phasmid, a chemosensory sensillum. During the L2 larval stage in both sexes, a descendant of the embryonic seam cell V5 generates the postdeirid. The postdeirid is a 2579 Development 120, 2579-2593 (1994) Printed in Great Britain © The Company of Biologists Limited 1994