Multiple cell interactions are required for fate specification during male spicule development in Caenorhabditis elegans

Abstract

The B blast cell divides postembryonically in C. elegans males to produce 47 progeny that include all of the cells of the copulatory spicules. During the early development of the B lineage, the anterior daughter of B, B.a, generates eight cells. These cells migrate to form four pairs of cells that flank the developing cloaca (ventral, dorsal, and two identical lateral pairs). For each pair, the more anterior cell produces a distinct lineage ('anterior fate') from the posterior cell ('posterior fate'). For the ventral and dorsal pairs, either cell can migrate to the anterior position and produce the anterior lineage, and the other cell migrates posterior and produces the posterior lineage (Sulston and Horvitz, 1977, Dev. Biol. 56, 110–156). The migration is variable, although the resultant fate pattern is invariant. In the two lateral pairs, both the migration and fate pattern are invariant. Using a laser microbeam to selectively ablate neighboring cells we have found that the cells of the lateral pair also respond to positional cues. For all four pairs other male-specific blast cells provide extracellular cues. In general, F and U promote anterior fates, Y promotes some posterior fates, and the B.a progeny promote posterior fates. Several of these cues are redundant. By ablating combinations of cells we have deduced how these signals may act in concert to specify the fates of the B.a progeny. We propose that fate specification in these pairs depends on three general classes of extracellular cues: positional cues, modulators of positional cues, and lateral signals. The B lineage thus provides an opportunity to study with single cell resolution the integration of multiple intercellular signals.