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Science 22 November 1996:
Vol. 274. no. 5291, pp. 1389 - 1391
DOI: 10.1126/science.274.5291.1389
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Reports

Control of C. elegans Larval Development by Neuronal Expression of a TGF-beta Homolog

Peifeng Ren, * Chang-Su Lim, *dagger Robert Johnsen, ddagger Patrice S. Albert, David Pilgrim, Donald L. Riddle §

The Caenorhabditis elegans dauer larva is specialized for dispersal without growth and is formed under conditions of overcrowding and limited food. The daf-7 gene, required for transducing environmental cues that support continuous development with plentiful food, encodes a transforming growth factor-beta (TGF-beta ) superfamily member. A daf-7 reporter construct is expressed in the ASI chemosensory neurons. Dauer-inducing pheromone inhibits daf-7 expression and promotes dauer formation, whereas food reactivates daf-7 expression and promotes recovery from the dauer state. When the food/pheromone ratio is high, the level of daf-7 mRNA peaks during the L1 larval stage, when commitment to non-dauer development is made.

P. Ren, C.-S. Lim, R. Johnsen, P. S. Albert, D. L. Riddle, Molecular Biology Program and Division of Biological Sciences, 311 Tucker Hall, University of Missouri, Columbia, MO 65211, USA.
D. Pilgrim, Department of Biological Sciences, G-507 Biological Sciences Building, University of Alberta, Edmonton, Alberta, Canada T6G 2E9.
*   These authors contributed equally to this work.

dagger    Present address: Department of Microbiology, Chungbuk National University, Cheongju, Chungbuk 360-763, Korea.

ddagger    Present address: Department of Medical Genetics, University of British Columbia, 6174 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z3.

§   To whom correspondence should be addressed. E-mail: riddle{at}biosci.mbp.missouri.edu

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   Abstract »    Full Text »    PDF »
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