Genetic Analysis of Chemosensory Control of Dauer Formation in Caenorhabditis elegans

INVESTIGATIONS

Genetic Analysis of Chemosensory Control of Dauer Formation in Caenorhabditis elegans

J. J. Vowels and J. H. Thomas
Department of Genetics, University of Washington, Seattle, Washington 98195

Dauer larva formation in Caenorhabditis elegans is controlled by chemosensory cells that respond to environmental cues. Genetic interactions among mutations in 23 genes that affect dauer larva formation were investigated. Mutations in seven genes that cause constitutive dauer formation, and mutations in 16 genes that either block dauer formation or result in the formation of abnormal dauers, were analyzed. Double mutants between dauer-constitutive and dauer-defective mutations were constructed and characterized for their capacity to form dauer larvae. Many of the genes could be interpreted to lie in a simple linear epistasis pathway. Three genes, daf-16, daf-18 and daf-20, may affect downstream steps in a branched part of the pathway. Three other genes, daf-2, daf-3 and daf-5, displayed partial or complex epistasis interactions that were difficult to interpret as part of a simple linear pathway. Dauer-defective mutations in nine genes cause structurally defective chemosensory cilia, thereby blocking chemosensation. Mutations in all nine of these genes appear to fall at a single step in the epistasis pathway. Dauer-constitutive mutations in one gene, daf-11, were strongly suppressed for dauer formation by mutations in the nine cilium-structure genes. Mutations in the other six dauer-constitutive genes caused dauer formation despite the absence of functional chemosensory endings. These results suggest that daf-11 is directly involved in chemosensory transduction essential for dauer formation, while the other Daf-c genes play roles downstream of the chemosensory step.

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				T. Yabe, N. Suzuki, T. Furukawa, T. Ishihara, and I. Katsura Multidrug resistance-associated protein MRP-1 regulates dauer diapause by its export activity in Caenorhabditis elegans Development, July 15, 2005; 132(14): 3197 - 3207. [Abstract] [Full Text] [PDF]

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				J. Li, G. Brown, M. Ailion, S. Lee, and J. H. Thomas NCR-1 and NCR-2, the C. elegans homologs of the human Niemann-Pick type C1 disease protein, function upstream of DAF-9 in the dauer formation pathways Development, November 15, 2004; 131(22): 5741 - 5752. [Abstract] [Full Text] [PDF]

				Y. Aoyama, S. Urushiyama, M. Yamada, C. Kato, H. Ide, S. Higuchi, T. Akiyama, and H. Shibuya MFB-1, an F-box-type ubiquitin ligase, regulates TGF-{beta} signalling Genes Cells, November 1, 2004; 9(11): 1093 - 1101. [Abstract] [Full Text] [PDF]

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				C. A. Wolkow, M. J. Munoz, D. L. Riddle, and G. Ruvkun Insulin Receptor Substrate and p55 Orthologous Adaptor Proteins Function in the Caenorhabditis elegans daf-2/Insulin-like Signaling Pathway J. Biol. Chem., December 13, 2002; 277(51): 49591 - 49597. [Abstract] [Full Text] [PDF]

				K. M. Nolan, T. R. Sarafi-Reinach, J. G. Horne, A. M. Saffer, and P. Sengupta The DAF-7 TGF-beta signaling pathway regulates chemosensory receptor gene expression in C. elegans Genes & Dev., December 1, 2002; 16(23): 3061 - 3073. [Abstract] [Full Text] [PDF]

				D. Garigan, A.-L. Hsu, A. G. Fraser, R. S. Kamath, J. Ahringer, and C. Kenyon Genetic Analysis of Tissue Aging in Caenorhabditis elegans: A Role for Heat-Shock Factor and Bacterial Proliferation Genetics, July 1, 2002; 161(3): 1101 - 1112. [Abstract] [Full Text] [PDF]

				C. Haycraft, P Swoboda, P. Taulman, J. Thomas, and B. Yoder The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms Development, January 5, 2001; 128(9): 1493 - 1505. [Abstract] [PDF]

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				S. A. Daniels, M. Ailion, J. H. Thomas, and P. Sengupta egl-4 Acts Through a Transforming Growth Factor-{beta}/SMAD Pathway in Caenorhabditis elegans to Regulate Multiple Neuronal Circuits in Response to Sensory Cues Genetics, September 1, 2000; 156(1): 123 - 141. [Abstract] [Full Text]

				A. Antebi, W.-H. Yeh, D. Tait, E. M. Hedgecock, and D. L. Riddle daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans Genes & Dev., June 15, 2000; 14(12): 1512 - 1527. [Abstract] [Full Text]

				D. A. Birnby, E. M. Link, J. J. Vowels, H. Tian, P. L. Colacurcio, and J. H. Thomas A Transmembrane Guanylyl Cyclase (DAF-11) and Hsp90 (DAF-21) Regulate a Common Set of Chemosensory Behaviors in Caenorhabditis elegans Genetics, May 1, 2000; 155(1): 85 - 104. [Abstract] [Full Text]

				Y. HONDA and S. HONDA The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans FASEB J, August 1, 1999; 13(11): 1385 - 1393. [Abstract] [Full Text]

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				S. Guo, G. Rena, S. Cichy, X. He, P. Cohen, and T. Unterman Phosphorylation of Serine 256 by Protein Kinase B Disrupts Transactivation by FKHR and Mediates Effects of Insulin on Insulin-like Growth Factor-binding Protein-1 Promoter Activity through a Conserved Insulin Response Sequence J. Biol. Chem., June 11, 1999; 274(24): 17184 - 17192. [Abstract] [Full Text] [PDF]

				S. Paradis, M. Ailion, A. Toker, J. H. Thomas, and G. Ruvkun A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans Genes & Dev., June 1, 1999; 13(11): 1438 - 1452. [Abstract] [Full Text]

				E. B. Gil, E. Malone Link, L. X. Liu, C. D. Johnson, and J. A. Lees Regulation of the insulin-like developmental pathway of Caenorhabditis elegans by a homolog of the PTEN tumor suppressor gene PNAS, March 16, 1999; 96(6): 2925 - 2930. [Abstract] [Full Text] [PDF]

				M Koga, M Take-uchi, T Tameishi, and Y Ohshima Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans Development, January 12, 1999; 126(23): 5387 - 5398. [Abstract] [PDF]

				J. Zallen, S. Kirch, and C. Bargmann Genes required for axon pathfinding and extension in the C. elegans nerve ring Development, January 8, 1999; 126(16): 3679 - 3692. [Abstract] [PDF]