Abstract
Dauer formation in Caenorhabditis elegans is regulated by several environmental stimuli, including a pheromone and temperature. Dauer formation is moderately induced as the growth temperature increases from 15 degrees to 25 degrees. Here we show that dauer formation is very strongly induced at a temperature of 27 degrees in both wild-type animals and mutants such as unc-64, unc-31, and unc-3, which do not form dauers at 25 degrees. A 27 degrees temperature stimulus is sufficient to induce dauer formation in wild-type animals independent of pheromone. Analysis of previously described dauer mutants at 27 degrees reveals a number of surprising results. Several classes of mutants (dyf, daf-3, tax-4, and tax-2) that are defective in dauer formation at lower temperatures reverse their phenotypes at 27 degrees and form dauers constitutively. Epistasis experiments place unc-64 and unc-31 at a different position in the dauer pathway from unc-3. We also uncover new branches of the dauer pathway at 27 degrees that are not detected at 25 degrees. We show that epistatic gene interactions can show both quantitative and qualitative differences depending on environmental conditions. Finally, we discuss some of the possible ecological implications of dauer induction by high temperatures.
Full Text
The Full Text of this article is available as a PDF (342.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ailion M., Inoue T., Weaver C. I., Holdcraft R. W., Thomas J. H. Neurosecretory control of aging in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7394–7397. doi: 10.1073/pnas.96.13.7394. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Albert P. S., Brown S. J., Riddle D. L. Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol. 1981 May 20;198(3):435–451. doi: 10.1002/cne.901980305. [DOI] [PubMed] [Google Scholar]
- Ann K., Kowalchyk J. A., Loyet K. M., Martin T. F. Novel Ca2+-binding protein (CAPS) related to UNC-31 required for Ca2+-activated exocytosis. J Biol Chem. 1997 Aug 8;272(32):19637–19640. doi: 10.1074/jbc.272.32.19637. [DOI] [PubMed] [Google Scholar]
- Apfeld J., Kenyon C. Regulation of lifespan by sensory perception in Caenorhabditis elegans. Nature. 1999 Dec 16;402(6763):804–809. doi: 10.1038/45544. [DOI] [PubMed] [Google Scholar]
- Avery L., Bargmann C. I., Horvitz H. R. The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions. Genetics. 1993 Jun;134(2):455–464. doi: 10.1093/genetics/134.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Avery L., Horvitz H. R. A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell. 1987 Dec 24;51(6):1071–1078. doi: 10.1016/0092-8674(87)90593-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Avery L. The genetics of feeding in Caenorhabditis elegans. Genetics. 1993 Apr;133(4):897–917. doi: 10.1093/genetics/133.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bargmann C. I., Horvitz H. R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science. 1991 Mar 8;251(4998):1243–1246. doi: 10.1126/science.2006412. [DOI] [PubMed] [Google Scholar]
- Bargmann C. I. Neurobiology of the Caenorhabditis elegans genome. Science. 1998 Dec 11;282(5396):2028–2033. doi: 10.1126/science.282.5396.2028. [DOI] [PubMed] [Google Scholar]
- Birnby D. A., Link E. M., Vowels J. J., Tian H., Colacurcio P. L., Thomas J. H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in caenorhabditis elegans. Genetics. 2000 May;155(1):85–104. doi: 10.1093/genetics/155.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cassada R. C., Russell R. L. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol. 1975 Oct;46(2):326–342. doi: 10.1016/0012-1606(75)90109-8. [DOI] [PubMed] [Google Scholar]
- Caterina M. J., Schumacher M. A., Tominaga M., Rosen T. A., Levine J. D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997 Oct 23;389(6653):816–824. doi: 10.1038/39807. [DOI] [PubMed] [Google Scholar]
- Coburn C. M., Bargmann C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 1996 Oct;17(4):695–706. doi: 10.1016/s0896-6273(00)80201-9. [DOI] [PubMed] [Google Scholar]
- Coburn C. M., Mori I., Ohshima Y., Bargmann C. I. A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development. 1998 Jan;125(2):249–258. doi: 10.1242/dev.125.2.249. [DOI] [PubMed] [Google Scholar]
- Colbert H. A., Smith T. L., Bargmann C. I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci. 1997 Nov 1;17(21):8259–8269. doi: 10.1523/JNEUROSCI.17-21-08259.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Daniels S. A., Ailion M., Thomas J. H., Sengupta P. 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. 2000 Sep;156(1):123–141. doi: 10.1093/genetics/156.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dorman J. B., Albinder B., Shroyer T., Kenyon C. The age-1 and daf-2 genes function in a common pathway to control the lifespan of Caenorhabditis elegans. Genetics. 1995 Dec;141(4):1399–1406. doi: 10.1093/genetics/141.4.1399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Estevez M., Attisano L., Wrana J. L., Albert P. S., Massagué J., Riddle D. L. The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature. 1993 Oct 14;365(6447):644–649. doi: 10.1038/365644a0. [DOI] [PubMed] [Google Scholar]
- Georgi L. L., Albert P. S., Riddle D. L. daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell. 1990 May 18;61(4):635–645. doi: 10.1016/0092-8674(90)90475-t. [DOI] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone. Mol Gen Genet. 1985;198(3):534–536. doi: 10.1007/BF00332953. [DOI] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone. Mol Gen Genet. 1985;198(3):534–536. doi: 10.1007/BF00332953. [DOI] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science. 1982 Nov 5;218(4572):578–580. doi: 10.1126/science.6896933. [DOI] [PubMed] [Google Scholar]
- Golden J. W., Riddle D. L. A pheromone-induced developmental switch in Caenorhabditis elegans: Temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc Natl Acad Sci U S A. 1984 Feb;81(3):819–823. doi: 10.1073/pnas.81.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gottlieb S., Ruvkun G. daf-2, daf-16 and daf-23: genetically interacting genes controlling Dauer formation in Caenorhabditis elegans. Genetics. 1994 May;137(1):107–120. doi: 10.1093/genetics/137.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hedgecock E. M., Culotti J. G., Thomson J. N., Perkins L. A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol. 1985 Sep;111(1):158–170. doi: 10.1016/0012-1606(85)90443-9. [DOI] [PubMed] [Google Scholar]
- Hedgecock E. M., Russell R. L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1975 Oct;72(10):4061–4065. doi: 10.1073/pnas.72.10.4061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herman R. K. Analysis of genetic mosaics of the nematode Caneorhabditis elegans. Genetics. 1984 Sep;108(1):165–180. doi: 10.1093/genetics/108.1.165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hobert O., Mori I., Yamashita Y., Honda H., Ohshima Y., Liu Y., Ruvkun G. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron. 1997 Aug;19(2):345–357. doi: 10.1016/s0896-6273(00)80944-7. [DOI] [PubMed] [Google Scholar]
- Horvitz H. R., Brenner S., Hodgkin J., Herman R. K. A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol Gen Genet. 1979 Sep;175(2):129–133. doi: 10.1007/BF00425528. [DOI] [PubMed] [Google Scholar]
- Inoue T., Thomas J. H. Targets of TGF-beta signaling in Caenorhabditis elegans dauer formation. Dev Biol. 2000 Jan 1;217(1):192–204. doi: 10.1006/dbio.1999.9545. [DOI] [PubMed] [Google Scholar]
- Iwasaki K., Staunton J., Saifee O., Nonet M., Thomas J. H. aex-3 encodes a novel regulator of presynaptic activity in C. elegans. Neuron. 1997 Apr;18(4):613–622. doi: 10.1016/s0896-6273(00)80302-5. [DOI] [PubMed] [Google Scholar]
- Katsura I., Kondo K., Amano T., Ishihara T., Kawakami M. Isolation, characterization and epistasis of fluoride-resistant mutants of Caenorhabditis elegans. Genetics. 1994 Jan;136(1):145–154. doi: 10.1093/genetics/136.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kenyon C., Chang J., Gensch E., Rudner A., Tabtiang R. A C. elegans mutant that lives twice as long as wild type. Nature. 1993 Dec 2;366(6454):461–464. doi: 10.1038/366461a0. [DOI] [PubMed] [Google Scholar]
- Kimura K. D., Tissenbaum H. A., Liu Y., Ruvkun G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science. 1997 Aug 15;277(5328):942–946. doi: 10.1126/science.277.5328.942. [DOI] [PubMed] [Google Scholar]
- Kingsley D. M. The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 1994 Jan;8(2):133–146. doi: 10.1101/gad.8.2.133. [DOI] [PubMed] [Google Scholar]
- Koga M., Take-uchi M., Tameishi T., Ohshima Y. Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans. Development. 1999 Dec;126(23):5387–5398. doi: 10.1242/dev.126.23.5387. [DOI] [PubMed] [Google Scholar]
- Komatsu H., Jin Y. H., L'Etoile N., Mori I., Bargmann C. I., Akaike N., Ohshima Y. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 1999 Mar 6;821(1):160–168. doi: 10.1016/s0006-8993(99)01111-7. [DOI] [PubMed] [Google Scholar]
- Komatsu H., Mori I., Rhee J. S., Akaike N., Ohshima Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron. 1996 Oct;17(4):707–718. doi: 10.1016/s0896-6273(00)80202-0. [DOI] [PubMed] [Google Scholar]
- Larsen P. L., Albert P. S., Riddle D. L. Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics. 1995 Apr;139(4):1567–1583. doi: 10.1093/genetics/139.4.1567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis J. A., Hodgkin J. A. Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. J Comp Neurol. 1977 Apr 1;172(3):489–510. doi: 10.1002/cne.901720306. [DOI] [PubMed] [Google Scholar]
- Lin K., Dorman J. B., Rodan A., Kenyon C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science. 1997 Nov 14;278(5341):1319–1322. doi: 10.1126/science.278.5341.1319. [DOI] [PubMed] [Google Scholar]
- Malone E. A., Inoue T., Thomas J. H. Genetic analysis of the roles of daf-28 and age-1 in regulating Caenorhabditis elegans dauer formation. Genetics. 1996 Jul;143(3):1193–1205. doi: 10.1093/genetics/143.3.1193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malone E. A., Thomas J. H. A screen for nonconditional dauer-constitutive mutations in Caenorhabditis elegans. Genetics. 1994 Mar;136(3):879–886. doi: 10.1093/genetics/136.3.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature. 1995 Jul 27;376(6538):344–348. doi: 10.1038/376344a0. [DOI] [PubMed] [Google Scholar]
- Morris J. Z., Tissenbaum H. A., Ruvkun G. A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature. 1996 Aug 8;382(6591):536–539. doi: 10.1038/382536a0. [DOI] [PubMed] [Google Scholar]
- Ogawa H., Harada S., Sassa T., Yamamoto H., Hosono R. Functional properties of the unc-64 gene encoding a Caenorhabditis elegans syntaxin. J Biol Chem. 1998 Jan 23;273(4):2192–2198. doi: 10.1074/jbc.273.4.2192. [DOI] [PubMed] [Google Scholar]
- Ogg S., Paradis S., Gottlieb S., Patterson G. I., Lee L., Tissenbaum H. A., Ruvkun G. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature. 1997 Oct 30;389(6654):994–999. doi: 10.1038/40194. [DOI] [PubMed] [Google Scholar]
- Paradis S., Ailion M., Toker A., Thomas J. H., Ruvkun G. A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev. 1999 Jun 1;13(11):1438–1452. doi: 10.1101/gad.13.11.1438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Paradis S., Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 1998 Aug 15;12(16):2488–2498. doi: 10.1101/gad.12.16.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patterson G. I., Koweek A., Wong A., Liu Y., Ruvkun G. The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev. 1997 Oct 15;11(20):2679–2690. doi: 10.1101/gad.11.20.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perkins L. A., Hedgecock E. M., Thomson J. N., Culotti J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol. 1986 Oct;117(2):456–487. doi: 10.1016/0012-1606(86)90314-3. [DOI] [PubMed] [Google Scholar]
- Prasad B. C., Ye B., Zackhary R., Schrader K., Seydoux G., Reed R. R. unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development. 1998 Apr;125(8):1561–1568. doi: 10.1242/dev.125.8.1561. [DOI] [PubMed] [Google Scholar]
- Saifee O., Wei L., Nonet M. L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol Biol Cell. 1998 Jun;9(6):1235–1252. doi: 10.1091/mbc.9.6.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schackwitz W. S., Inoue T., Thomas J. H. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron. 1996 Oct;17(4):719–728. doi: 10.1016/s0896-6273(00)80203-2. [DOI] [PubMed] [Google Scholar]
- Spray D. C. Cutaneous temperature receptors. Annu Rev Physiol. 1986;48:625–638. doi: 10.1146/annurev.ph.48.030186.003205. [DOI] [PubMed] [Google Scholar]
- Starich T. A., Herman R. K., Kari C. K., Yeh W. H., Schackwitz W. S., Schuyler M. W., Collet J., Thomas J. H., Riddle D. L. Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics. 1995 Jan;139(1):171–188. doi: 10.1093/genetics/139.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Swoboda P., Adler H. T., Thomas J. H. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell. 2000 Mar;5(3):411–421. doi: 10.1016/s1097-2765(00)80436-0. [DOI] [PubMed] [Google Scholar]
- Sze J. Y., Victor M., Loer C., Shi Y., Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature. 2000 Feb 3;403(6769):560–564. doi: 10.1038/35000609. [DOI] [PubMed] [Google Scholar]
- Take-Uchi M., Kawakami M., Ishihara T., Amano T., Kondo K., Katsura I. An ion channel of the degenerin/epithelial sodium channel superfamily controls the defecation rhythm in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11775–11780. doi: 10.1073/pnas.95.20.11775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas J. H., Birnby D. A., Vowels J. J. Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics. 1993 Aug;134(4):1105–1117. doi: 10.1093/genetics/134.4.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tissenbaum H. A., Hawdon J., Perregaux M., Hotez P., Guarente L., Ruvkun G. A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):460–465. doi: 10.1073/pnas.97.1.460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vowels J. J., Thomas J. H. Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans. Genetics. 1994 Oct;138(2):303–316. doi: 10.1093/genetics/138.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walent J. H., Porter B. W., Martin T. F. A novel 145 kd brain cytosolic protein reconstitutes Ca(2+)-regulated secretion in permeable neuroendocrine cells. Cell. 1992 Sep 4;70(5):765–775. doi: 10.1016/0092-8674(92)90310-9. [DOI] [PubMed] [Google Scholar]
- Wittenburg N., Baumeister R. Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10477–10482. doi: 10.1073/pnas.96.18.10477. [DOI] [PMC free article] [PubMed] [Google Scholar]