Searching for Neuronal Left/Right Asymmetry: Genomewide Analysis of Nematode Receptor-Type Guanylyl Cyclases

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...

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Bibliographic Details
Published in:	Genetics (Austin) Vol. 173; no. 1; pp. 131 - 149
Main Authors:	Ortiz, Christopher O, Etchberger, John F, Posy, Shoshana L, Frokjaer-Jensen, Christian, Lockery, Shawn, Honig, Barry, Hobert, Oliver
Format:	Journal Article
Language:	English
Published:	United States Genetics Soc America 01-05-2006 Genetics Society of America Copyright © 2006 by the Genetics Society of America
Subjects:	Alleles Animals Body Patterning - genetics Caenorhabditis elegans Caenorhabditis elegans - cytology Caenorhabditis elegans - enzymology Caenorhabditis elegans - genetics Chromosomes - genetics Evolution, Molecular Gene expression Gene Expression Profiling Gene Expression Regulation Genes, Helminth - genetics Genes, Reporter Genetics Genome, Helminth - genetics Genomics Investigations Mutation - genetics Nematoda Nematodes Neurons Neurons - metabolism Phylogeny Receptors, Guanylate Cyclase-Coupled - chemistry Receptors, Guanylate Cyclase-Coupled - genetics Sequence Homology, Nucleic Acid Species Specificity Studies Synteny - genetics
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Summary:	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.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Communicating editor: K. Kemphues Corresponding author: Columbia University, 701 W. 68th St., HHSC 724, New York, NY. E-mail: or38@columbia.edu
ISSN:	0016-6731 1943-2631 1943-2631
DOI:	10.1534/genetics.106.055749