Genetics. Published Articles Ahead of Print: March 17, 2006, Copyright © 2006
doi:10.1534/genetics.106.055749


A more recent version of this article appeared on May 1, 2006.

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Searching for neuronal left/right asymmetry: Genome wide analysis of nematode receptor-type guanylyl cyclases

Christopher O Ortiz 1, John F Etchberger 1, Shoshana L Posy 1, Christian Frøkjær-Jensen 2, Shawn Lockery 2, Barry Honig 1 and Oliver Hobert 1*

1 Columbia University
2 University of Oregon

* To whom correspondence should be addressed. E-mail: or38{at}columbia.edu.

Submitted on January 12, 2006
Revised on March 2, 2006
Accepted on 3 March 2006


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 which 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 genome wide analysis of all gcy genes. We report the existence of a total of 27 receptor-type gcy genes and of seven soluble gcy genes in C. elegans. We describe the expression pattern of all previously uncharacterized receptor-type gcy genes and find them to be highly biased but not exclusively restricted to the nervous system. We find that more than 41% (11/27) of all gcy genes 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.

Key Words: C. elegans, guanylyl cyclase, left/right asymmetry, sensory neurons




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