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Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases.

ABSTRACT: Even though functional lateralization is a common feature of many nervous systems, it is poorly understood how lateralized neural function is linked to lateralized gene activity. A bilaterally symmetric pair of C. elegans gustatory neurons, ASEL and ASER, senses a number of chemicals in a left/right asymmetric manner and therefore serves as a model to study the genetic basis of functional lateralization. The extent of functional lateralization of the ASE neurons and genes responsible for the left/right asymmetric activity of ASEL and ASER is unknown.We show here that a substantial number of salt ions are sensed in a left/right asymmetric manner and that lateralized salt responses allow the worm to discriminate between distinct salt cues. To identify molecules that may be involved in sensing salt ions and/or transmitting such sensory information, we examined the chemotaxis behavior of animals harboring mutations in eight different receptor-type, transmembrane guanylyl cyclases (encoded by gcy genes), which are expressed in either ASEL (gcy-6, gcy-7, gcy-14), ASER (gcy-1, gcy-4, gcy-5, gcy-22), or ASEL and ASER (gcy-19). Disruption of a particular ASER-expressed gcy gene, gcy-22, results in a broad chemotaxis defect to nearly all salts sensed by ASER, as well as to a left/right asymmetrically sensed amino acid. In contrast, disruption of other gcy genes resulted in highly salt ion-specific chemosensory defects.Our findings broaden our understanding of lateralities in neural function, provide insights into how this laterality is molecularly encoded, and reveal an unusual multitude of molecules involved in gustatory signal transduction.

SUBMITTER: Ortiz CO

PROVIDER: S-EPMC2730525 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases.

Ortiz Christopher O CO Faumont Serge S Takayama Jun J Ahmed Heidi K HK Goldsmith Andrew D AD Pocock Roger R McCormick Kathryn E KE Kunimoto Hirofumi H Iino Yuichi Y Lockery Shawn S Hobert Oliver O

Current biology : CB 20090611 12

<h4>Background</h4>Even though functional lateralization is a common feature of many nervous systems, it is poorly understood how lateralized neural function is linked to lateralized gene activity. A bilaterally symmetric pair of C. elegans gustatory neurons, ASEL and ASER, senses a number of chemicals in a left/right asymmetric manner and therefore serves as a model to study the genetic basis of functional lateralization. The extent of functional lateralization of the ASE neurons and genes resp ...[more]

PMID: 19523832

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Project description: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.

Dataset Information

Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases.

Publications

Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases.

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