Abstract
Functional left/right asymmetry (“laterality”) is a fundamental feature of many nervous systems, but only very few molecular correlates to functional laterality are known. At least two classes of chemosensory neurons in the nematode
Caenorhabditis elegans
are functionally lateralized. The gustatory neurons ASE left (ASEL) and ASE right (ASER) are two bilaterally symmetric neurons that sense distinct chemosensory cues and express a distinct set of four known chemoreceptors of the guanylyl cyclase (
gcy
) gene family. To examine the extent of lateralization of
gcy
gene expression patterns in the ASE neurons, we have undertaken a genomewide analysis of all
gcy
genes. We report the existence of a total of 27
gcy
genes encoding receptor-type guanylyl cyclases and of 7
gcy
genes encoding soluble guanylyl cyclases in the complete genome sequence of
C. elegans
. We describe the expression pattern of all previously uncharacterized receptor-type guanylyl cyclases and find them to be highly biased but not exclusively restricted to the nervous system. We find that >41% (11/27) of all receptor-type guanylyl cyclases are expressed in the ASE gustatory neurons and that one-third of all
gcy
genes (9/27) are expressed in a lateral, left/right asymmetric manner in the ASE neurons. The expression of all laterally expressed
gcy
genes is under the control of a gene regulatory network composed of several transcription factors and miRNAs. The complement of
gcy
genes in the related nematode
C. briggsae
differs from
C. elegans
as evidenced by differences in chromosomal localization, number of
gcy
genes, and expression patterns. Differences in
gcy
expression patterns in the ASE neurons of
C. briggsae
arise from a difference in
cis-
regulatory elements and
trans-
acting factors that control ASE laterality. In sum, our results indicate the existence of a surprising multitude of putative chemoreceptors in the gustatory ASE neurons and suggest the existence of a substantial degree of laterality in gustatory signaling mechanisms in nematodes.