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


RESULTS
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.


CONCLUSIONS
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.
Ortiz
Christopher O
CO
Howard Hughes Medical Institute, Department of Biochemistry and Molecular Biophysics, Columbia University Medical Center, New York, NY 10032, USA.
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
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D017173:Caenorhabditis elegans / Q000033:anatomy & histology / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D002633:Chemotaxis / Q000502:physiology; D007839:Functional Laterality / Q000502:physiology*; D006162:Guanylate Cyclase / Q000235:genetics / Q000378:metabolism*; D007477:Ions / Q000737:chemistry; D009154:Mutation; D009474:Neurons / Q000166:cytology / Q000502:physiology; D050705:Receptors, Guanylate Cyclase-Coupled / Q000235:genetics / Q000378:metabolism; D012492:Salts / Q000737:chemistry; D013649:Taste / Q000502:physiology*
D029742:Caenorhabditis elegans Proteins; D007477:Ions; D012492:Salts; D006162:Guanylate Cyclase; D050705:Receptors, Guanylate Cyclase-Coupled