How to cite this WIREs title:
WIREs Dev Biol

Impact Factor: 3.883

Phenotypic plasticity and remodeling in the stress‐induced Caenorhabditis elegans dauer

Focus Article

Rebecca J. Androwski, Kristen M. Flatt, Nathan E. Schroeder

Published Online: May 24 2017

DOI: 10.1002/wdev.278

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

Organisms are often capable of modifying their development to better suit their environment. Under adverse conditions, the nematode Caenorhabditis elegans develops into a stress‐resistant alternative larval stage called dauer. The dauer stage is the primary survival stage for C. elegans in nature. Large‐scale tissue remodeling during dauer conveys resistance to harsh environments. The environmental and genetic regulation of the decision to enter dauer has been extensively studied. However, less is known about the mechanisms regulating tissue remodeling. Changes to the cuticle and suppression of feeding in dauers lead to an increased resistance to external stressors. Meanwhile reproductive development arrests during dauer while preserving the ability to reproduce once favorable environmental conditions return. Dramatic remodeling of neurons, glia, and muscles during dauer likely facilitate dauer‐specific behaviors. Dauer‐specific pulsation of the excretory duct likely mediates a response to osmotic stress. The power of C. elegans genetics has uncovered some of the molecular pathways regulating dauer tissue remodeling. In addition to genes that regulate single remodeling events, several mutants result in pleiotropic defects in dauer remodeling. This review details the individual aspects of morphological changes that occur during dauer formation and discusses molecular mechanisms regulating these processes. The dauer stage provides us with an excellent model for understanding phenotypic plasticity and remodeling from the individual cell to an entire animal. WIREs Dev Biol 2017, 6:e278. doi: 10.1002/wdev.278 This article is categorized under: Invertebrate Organogenesis > Worms Comparative Development and Evolution > Model Systems

The life cycle of C. elegans. In an environment of plentiful food and low dauer pheromone, C. elegans molts through four larval stages followed by the reproductive adult. Under conditions of low levels of food and high levels of pheromone (signaling population density) during L1 they will enter into a developmentally arrested dauer stage. Following a return to favorable environmental conditions, they will recover from dauer and resume development into a reproductive adult.

[ Normal View | Magnified View ]

The nonfeeding dauer stage is characterized by buccal cavity occlusion and pharyngeal bulb shrinkage. DIC micrographs of L3 (top) and dauer (bottom) animals demonstrating changes to the buccal cavity (a, red arrow) and the pharynx (b). Shrinkage of the pharynx is most obvious in the terminal bulb (red arrow). Scale bars, 10 µm.

[ Normal View | Magnified View ]

IL2 dendrites arborize during dauer. Confocal micrographs of an L3 (a) and dauer (b) animal expressing klp‐6p::gfp in the six IL2 neurons. During nondauer stages the IL2s are unbranched with a single dendrite projecting anteriorly (left) and a single axon projecting posteriorly (right) from the cell body. During dauer the IL2s arborize extensively, increasing their total dendritic length threefold, with the bulk of their arbors originating from just four of the six cells. Scale bars, 10 µm.

[ Normal View | Magnified View ]

Seam cell shrinkage and cuticle remodeling occur during dauer formation. Nomarski (a) and fluorescent (b) images of nondauer L3 (top) and dauer (bottom) ajm‐1::gfp larvae. During dauer the lateral cuticle contains raised ridges called alae (red arrows). Production of alae is correlated with shrinkage of the underlying epithelial seam cells as seen with the ajm‐1::gfp transgene. Scale bars, 10 µm.

[ Normal View | Magnified View ]

The dauer formation decision pathway. The decision to enter dauer begins with environmental components and proceeds through two parallel pathways before converging onto a lipid hormone signaling pathway. Mutating the encoding genes of this pathway may lead to either constitutive dauer formation (daf‐c, dauer formation constitutive) or an inability to form dauers (daf‐d, dauer formation defective). Lines ending with arrows indicate increased activity of the downstream component. Lines ending with bars indicate suppression or downregulation of the downstream component.

[ Normal View | Magnified View ]

Nictation and swarming are dauer‐specific behaviors. Micrographs (left) and cartoon schematics (right) of an individual nictating dauer (a) and a swarm of elevated dauers (b) on top of a polydimethylsiloxane (PDMS) pedestal. Individual dauers are capable of standing on their tail while remaining in a rigid posture for several seconds. Swarms consist of tens of dauers undulating in the air together, essentially using the neighboring animal as a structure to climb. The base of the swarm is indicated with a red arrow while the top is indicated with a yellow arrow.

[ Normal View | Magnified View ]

References

West‐Eberhard, MJ. Developmental Plasticity and Evolution. New York, NY: Oxford University Press; 2003.
McEwen, BS, Nasca, C, Gray, JD. Stress effects on neuronal structure: hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 2016, 41:3–23. https://doi.org/10.1038/npp.2015.171.
Pener, MP, Simpson, SJ. Locust phase polyphenism: an update. Adv Insect Physiol 2009, 36:1–272. https://doi.org/10.1016/S0065‐2806(08)36001‐9.
Shuel, RW, Dixon, SE. The early establishment of dimorphism in the female honeybee, Apis mellifera L. Insectes Soc 1960, 7:265–282. https://doi.org/10.1007/BF02224497.
Mao, W, Schuler, MA, Berenbaum, MR. A dietary phytochemical alters caste‐associated gene expression in honey bees. Sci Adv 2015, 1:e1500795. https://doi.org/10.1126/sciadv.1500795.
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71–94.
Sulston, JE, Schierenberg, E, White, JG, Thomson, JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983, 100:64–119. https://doi.org/10.1016/0012‐1606(83)90201‐4.
Sulston, JE, Horvitz, HR. Post‐embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 1977, 56:110–156. https://doi.org/10.1016/0012‐1606(77)90158‐0.
White, JG, Southgate, E, Thomson, JN, Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 1986, 314:1–340.
Mello, CC, Kramer, JM, Stinchcomb, D, Ambros, V. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 1991, 10:3959–3970.
Fire, A, Xu, S, Montgomery, MK, Kostas, SA, Driver, SE, Mello, CC. Potent and specific genetic interference by double‐stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806–811. https://doi.org/10.1038/35888.
Dickinson, DJ, Goldstein, B. CRISPR‐based methods for Caenorhabditis elegans genome engineering. Genetics 2016, 202:885–901. https://doi.org/10.1534/genetics.115.182162.
Golden, JW, Riddle, DL. The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 1984, 102:368–378. https://doi.org/10.1016/0012‐1606(84)90201‐X.
Klass, M, Hirsh, D. Non‐ageing developmental variant of Caenorhabditis elegans. Nature 1976, 260:523–525.
Cassada, RC, Russell, RL. The dauerlarva, a post‐embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 1975, 46:326–342. https://doi.org/10.1016/0012‐1606(75)90109‐8.
Hodgkin, J, Doniach, T. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 1997, 146:149–164.
Nicholas, WL, Dougherty, EC, Hansen, EL. Axenic cultivation of Caenorhabditis briggsae (Nematoda: Rhabditidae) with chemically undefined supplements; comparative studies with related nematodes. Ann N Y Acad Sci 1959, 77:218–236. https://doi.org/10.1111/j.1749‐6632.1959.tb36902.x.
Staniland, LN. Experiments on the control of chrysanthemum eelworm (Aphelenchoides ritzema‐bosi, Schwartz) hot water treatment. Ann Appl Biol 1950, 37:11–18. https://doi.org/10.1111/j.1744‐7348.1950.tb00946.x.
Staniland, LN. Now we`ll try oils. Savannah, GA: Foley House; 1950.
Staniland, LN. The Principles of Line Illustration with Emphasis on the Requirements of Biological and Other Scientific Workers. Cambridge, UK: Cambridge University Press; 1953.
Southey, JF, Staniland, LN. Observations and experiments on stem eelworm, Ditylenchus dipsaci (Kühn, 1857) Filipjev, 1936, with special reference to weed hosts. J Helminthol 1950, 24:145–154. https://doi.org/10.1017/S0022149X00019210.
Staniland, L. The swarming of Rhabditid eelworms in mushroom houses. Plant Pathol 1957, 6:61–62.
Burr, AH. The photomovement of Caenorhabditis elegans, a nematode which lacks ocelli. Proof that the response is to light not radiant heating. Photochem Photobiol 1985, 41:577–582. https://doi.org/10.1111/j.1751‐1097.1985.tb03529.x.
Kiontke, K, Sudhaus, W. Ecology of Caenorhabditis species. In: Fitch, DH, ed. WormBook. The C. elegans Research Community; 2006. Available at: http://www.wormbook.org/citewb.html.
Lee, H, Choi, M, Lee, D, Kim, H, Hwang, H, Kim, H, Park, S, Paik, Y, Lee, J. Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat Neurosci 2012, 15:107–112. https://doi.org/10.1038/nn.2975.
Frézal, L. Félix M‐A. C. elegans outside the Petri dish. Elife 2015, 4:e05849. https://doi.org/10.1016/j.cub.2010.09.050.
Félix, M‐A, Braendle, C. The natural history of Caenorhabditis elegans. Curr Biol 2010, 20:R965–R969. https://doi.org/10.1016/j.cub.2010.09.050.
Crook, M. The dauer hypothesis and the evolution of parasitism: 20 years on and still going strong. Int J Parasitol 2014, 44:1–8. https://doi.org/10.1016/j.ijpara.2013.08.004.
Castelletto, ML, Gang, SS, Okubo, RP, Tselikova, AA, Nolan, TJ, Platzer, EG, Lok, JB, Hallem, EA. Diverse host‐seeking behaviors of skin‐penetrating nematodes. PLoS Pathog 2014, 10:e1004305. https://doi.org/10.1371/journal.ppat.1004305.
Ashton, FT, Zhu, X, Boston, R, Lok, JB, Schad, GA. Strongyloides stercoralis: amphidial neuron pair ASJ triggers significant resumption of development by infective larvae under host‐mimicking in vitro conditions. Exp Parasitol 2007, 115:92–97. https://doi.org/10.1016/j.exppara.2006.08.010.
Procko, C, Lu, Y, Shaham, S. Sensory organ remodeling in Caenorhabditis elegans requires the zinc‐finger protein ZTF‐16. Genetics 2012, 190:1405–1415. https://doi.org/10.1534/genetics.111.137786.
Hallem, EA, Rengarajan, M, Ciche, TA, Sternberg, PW. Nematodes, bacteria, and flies : a tripartite model for nematode parasitism. Curr Biol 2007, 17:898–904. https://doi.org/10.1016/j.cub.2007.04.027.
Albarqi, MMY, Stoltzfus, JD, Pilgrim, AA, Nolan, TJ, Wang, Z, Kliewer, SA, Mangelsdorf, DJ, Lok, JB. Regulation of life cycle checkpoints and developmental activation of infective larvae in Strongyloides stercoralis by dafachronic acid. PLoS Pathog 2016, 12:e1005358. https://doi.org/10.1371/journal.ppat.1005358.
Ogawa, A, Streit, A, Antebi, A, Sommer, RJ. A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Curr Biol 2009, 19:67–71.
Fielenbach, N, Antebi, A. C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 2008, 22:2149–2165. https://doi.org/10.1101/gad.1701508.
Hu, PJ. Dauer. In: Riddle, DL, ed. WormBook. WormBook; 2007, 1–19. https://doi.org/10.1895/wormbook.1.144.1. Available at: http://www.wormbook.org/citewb.html.
Riddle, DL, Albert, PS. Genetic and environmental regulation of dauer larva development. In: Riddle, DL, Blumenthal, T, Meyer, BJ, Priess, JR, eds. C. elegans II. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1998.
Golden, JW, Riddle, DL. A Caenorhabditis elegans dauer‐inducing pheromone and an antagonistic component of the food supply. J Chem Ecol 1984, 10:1265–1280. https://doi.org/10.1007/BF00988553.
Golden, J, Riddle, D. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 1982, 218:578–580.
Ailion, M, Thomas, JH. Dauer formation induced by high temperatures in Caenorhabditis elegans. Genetics 2000, 156:1047–1067.
Vowels, JJ, Thomas, JH. Multiple chemosensory defects in daf‐11 and daf‐21 mutants of Caenorhabditis elegans. Genetics 1994, 138:303–316.
Ren, P, Lim, C‐S, Johnsen, R, Albert, PS, Pilgrim, D, Riddle, DL. Control of C. elegans larval development by neuronal expression of a TGF‐beta homolog. Science 1996, 274:1389–1391. https://doi.org/10.1126/science.274.5291.1389.
Li, W, Kennedy, SG, Ruvkun, G. daf‐28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF‐2 signaling pathway. Genes Dev 2003, 17:844–858. https://doi.org/10.1101/gad.1066503.
Schackwitz, WS, Inoue, T, Thomas, JH. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 1996, 17:719–728. https://doi.org/10.1016/S0896‐6273(00)80203‐2.
Kimura, KD, Tissenbaum, HA, Liu, Y, Ruvkun, G. daf‐2, an insulin receptor‐like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 1997, 277:942–946.
Ogg, S, Paradis, S, Gottlieb, S, Patterson, GI, Lee, L, Tissenbaum, HA. The Fork head transcription factor DAF‐16 transduces insulin‐like metabolic and longevity signals in C. elegans. Nature 1997, 389:994–999.
Lin, K, Dorman, JB, 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, 278:1319–1322.
Thomas, JH, Birnby, DA, Vowels, JJ. Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 1993, 134:1105–1117.
Gerisch, B, Antebi, A. Hormonal signals produced by DAF‐9/cytochrome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 2004, 131:1765–1776. https://doi.org/10.1242/dev.01068.
Mak, HY, Ruvkun, G. Intercellular signaling of reproductive development by the C. elegans DAF‐9 cytochrome P450. Development 2004, 131:1777–1786.
Gerisch, B, Weitzel, C, Kober‐Eisermann, C, Rottiers, V, Antebi, A. A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev Cell 2001, 1:841–851. https://doi.org/10.1016/S1534‐5807(01)00085‐5.
Jia, K, Albert, PS, Riddle, DL. DAF‐9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 2002, 129:221–231.
Motola, DL, Cummins, CL, Rottiers, V, Sharma, KK, Li, T, Li, Y, Suino‐Powell, K, Xu, HE, Auchus, RJ, Antebi, A, et al. Identification of ligands for DAF‐12 that govern dauer formation and reproduction in C. elegans. Cell 2006, 124:1209–1223. https://doi.org/10.1016/j.cell.2006.01.037.
Antebi, A, Yeh, WH, Tait, D, Hedgecock, EM, Riddle, DL. daf‐12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev 2000, 14:1512–1527. https://doi.org/10.1101/gad.14.12.1512.
Wang, J, Kim, SK. Global analysis of dauer gene expression in Caenorhabditis elegans. Development 2003, 130:1621–1634.
Jeong, P‐Y, Kwon, M‐S, Joo, H‐J, Paik, Y‐K. Molecular time‐course and the metabolic basis of entry into dauer in Caenorhabditis elegans. PLoS One 2009, 4:e4162. https://doi.org/10.1371/journal.pone.0004162.
Nika, L, Gibson, T, Konkus, R, Karp, X. Fluorescent beads are a versatile tool for staging Caenorhabditis elegans in different life histories. G3 (Bethesda) 2016, 6:1923–1933. https://doi.org/10.1534/g3.116.030163.
Bird, AF, Bird, J. The Structure of Nematodes. 2nd ed. San Diego, CA: Academic Press; 1991.
Cox, GN, Staprans, S, Edgar, RS. The cuticle of Caenorhabditis elegans. Dev Biol 1981, 86:456–470. https://doi.org/10.1016/0012‐1606(81)90204‐9.
Blaxter, ML. Cuticle surface proteins of wild type and mutant Caenorhabditis elegans. J Biol Chem 1993, 268:6600–6609.
Proudfoot, L, Kusel, JR, Smith, HV, Harnett, W, Worms, MJ, Kennedy, MW. Rapid changes in the surface of parasitic nematodes during transition from pre‐ to post‐parasitic forms. Parasitology 1993, 107:107–117.
Link, CD, Silverman, MA, Breen, M, Watt, KE, Dames, SA. Characterization of Caenorhabditis elegans lectin‐binding mutants. Genetics 1992, 131:867–881.
Höflich, J, Berninsone, P, Göbel, C, Gravato‐Nobre, MJ, Libby, BJ, Darby, C, Politz, SM, Hodgkin, J, Hirschberg, CB, Baumeister, R. Loss of srf‐3‐encoded nucleotide sugar transporter activity in Caenorhabditis elegans alters surface antigenicity and prevents bacterial adherence. J Biol Chem 2004, 279:30440–30448. https://doi.org/10.1074/jbc.M402429200.
Krall, EL. Root Parasitic Nematodes Family Hoploaimidae. English ed. New Delhi, India: Amerind Publishing; 1990.
Chitwood, BG, Chitwood, M. Introduction to Nematology. Consolidat. Baltimore, MD: University Park Press; 1974.
Singh, RN, Sulston, JE. Some observations on moulting in Caenorhabditis elegans. Nematologica 1978, 24:63–71.
Melendez, A, Talloczy, Z, Seaman, M, Eskelinen, EL, Hall, DH, Levine, B. Autophagy genes are essential for dauer development and life‐span extension in C. elegans. Science 2003, 301:1387–1391. https://doi.org/10.1126/science.1087782.
Fujimoto, D, Kanaya, S. Cuticlin: a noncollagen structural protein from Ascaris cuticle. Arch Biochem Biophys 1973, 157:1–6. https://doi.org/10.1016/0003‐9861(73)90382‐2.
Sapio, MR, Hilliard, MA, Cermola, M, Favre, R, Bazzicalupo, P. The Zona Pellucida domain containing proteins, CUT‐1, CUT‐3 and CUT‐5, play essential roles in the development of the larval alae in Caenorhabditis elegans. Dev Biol 2005, 282:231–245. https://doi.org/10.1016/j.ydbio.2005.03.011.
Muriel, JM, Brannan, M, Taylor, K, Johnstone, IL, Lithgow, GJ, Tuckwell, D. M142.2 (cut‐6), a novel Caenorhabditis elegans matrix gene important for dauer body shape. Dev Biol 2003, 260:339–351. https://doi.org/10.1016/S0012‐1606(03)00237‐9.
Ambros, V, Horvitz, HR. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 1984, 226:409–416. https://doi.org/10.1126/science.6494891.
Liu, Z, Ambros, V. Heterochronic genes control the stage‐specific initiation and expression of the dauer larva developmental program in Caenorhabditis elegans. Genes Dev 1989, 3:2039–2049. https://doi.org/10.1101/gad.3.12b.2039.
Euling, S, Ambros, V. Reversal of cell fate determination in Caenorhabditis elegans vulval development. Development 1996, 122:2507–2515.
Liu, Z, Ambros, V. Alternative temporal control systems for hypodermal cell differentiation in Caenorhabditis elegans. Nature 1991, 350:162–165.
Abrahante, JE, Miller, EA, Rougvie, AE. Identification of heterochronic mutants in Caenorhabditis elegans: temporal misexpression of a collagen: green fluorescent protein fusion gene. Genetics 1998, 149:1335–1351.
Abrahante, JE, Daul, AL, Li, M, Volk, ML, Tennessen, JM, Miller, EA, Rougvie, AE. The Caenorhabditis elegans hunchback‐like gene lin‐57/hbl‐1 controls developmental time and is regulated by microRNAs. Dev Cell 2003, 4:625–637.
Morita, K, Han, M. Multiple mechanisms are involved in regulating the expression of the developmental timing regulator lin‐28 in Caenorhabditis elegans. EMBO J 2006, 25:5794–5804.
Karp, X, Ambros, V. Dauer larva quiescence alters the circuitry of microRNA pathways regulating cell fate progression in C. elegans. Development 2012, 139:2177–2186.
Hall, SE, Beverly, M, Russ, C, Nusbaum, C, Sengupta, P. A cellular memory of developmental history generates phenotypic diversity in C. elegans. Curr Biol 2010, 20:149–155. https://doi.org/10.1016/j.cub.2009.11.035.
Popham, JD, Webster, JM. Aspects of the fine structure of the dauer larva of the nematode Caenorhabditis elegans. Can J Zool 1979, 57:794–800. https://doi.org/10.1139/z79‐098.
Hellerer, T, Axäng, C, Brackmann, C, Hillertz, P, Pilon, M, Enejder, A. Monitoring of lipid storage in Caenorhabditis elegans using coherent anti‐Stokes Raman scattering (CARS) microscopy. Proc Natl Acad Sci U S A 2007, 104:14658–14663. https://doi.org/10.1073/pnas.0703594104.
White, JG, Southgate, E, Thomson, JN, Brenner, S. The structure of the ventral nerve of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 1976, 275:327–348.
Dixon, SJ, Alexander, M, Chan, KKM, Roy, PJ. Insulin‐like signaling negatively regulates muscle arm extension through DAF‐12 in Caenorhabditis elegans. Dev Biol 2008, 318:153–161. https://doi.org/10.1016/j.ydbio.2008.03.019.
Ward, S, Thomson, N, White, JG, Brenner, S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J Comp Neurol 1975, 160:313–337. https://doi.org/10.1002/cne.901600305.
Albert, PS, Riddle, DL. Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva. J Comp Neurol 1983, 219:461–481. https://doi.org/10.1002/cne.902190407.
Mori, I, Ohshima, Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344–348. https://doi.org/10.1038/376344a0.
Hedgecock, EM, Russell, RL. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 1975, 72:4061–4065. https://doi.org/10.1073/pnas.72.10.4061.
Procko, C, Lu, Y, Shaham, S. Glia delimit shape changes of sensory neuron receptive endings in C. elegans. Development 2011, 138:1371–1381. https://doi.org/10.1242/dev.058305.
Bacaj, T, Tevlin, M, Lu, Y, Shaham, S. Glia are essential for sensory organ function in C. elegans. Science 2008, 322:744–747.
Bargmann, CI, Horvitz, HR. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 1991, 251:1243–1246. https://doi.org/10.1126/science.2006412.
Peckol, EL, Troemel, ER, Bargmann, CI. Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2001, 98:11032–11038. https://doi.org/10.1073/pnas.191352498.
Han, Z, Boas, S, Schroeder, NE. Unexpected variation in neuroanatomy among diverse nematode species. Front Neuroanat 2016, 9:1–11. https://doi.org/10.3389/fnana.2015.00162.
Schroeder, NE, Androwski, RJ, Rashid, A, Lee, H, Lee, J, Barr, MM. Dauer‐specific dendrite arborization in C. elegans is regulated by KPC‐1/Furin. Curr Biol 2013, 23:1527–1535. https://doi.org/10.1016/j.cub.2013.06.058.
Smith, CJ, Watson, JD, Spencer, WC, Brien, TO, Cha, B, Albeg, A, Treinin, M, Miller, DM. Time‐lapse imaging and cell‐specific expression profiling reveal dynamic branching and molecular determinants of a multi‐dendritic nociceptor in C. elegans. Dev Biol 2010, 345:18–33. https://doi.org/10.1016/j.ydbio.2010.05.502.
Sawin, ER, Ranganathan, R. Horvitz HR. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619–631. https://doi.org/10.1016/S0896‐6273(00)81199‐X.
Li, W, Kang, L, Piggott, BJ, Feng, Z, Xu, XZS. The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun 2011, 2:315. https://doi.org/10.1038/ncomms1308.
Cinar, HN, Chisholm, AD. Genetic analysis of the Caenorhabditis elegans pax‐6 locus: roles of paired domain‐containing and nonpaired domain‐containing isoforms. Genetics 2004, 168:1307–1322. https://doi.org/10.1534/genetics.104.031724.
Keane, J, Avery, L. Mechanosensory inputs influence Caenorhabditis elegans pharyngeal activity via ivermectin sensitivity genes. Genetics 2003, 164:153–162.
Choe, A, von Reuss, SH, Kogan, D, Gasser, RB, Platzer, EG, Schroeder, FC, Sternberg, PW. Ascaroside signaling is widely conserved among nematodes. Curr Biol 2012, 22:772–780. https://doi.org/10.1016/j.cub.2012.03.024.
Gems, D, McElwee, JJ. Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF‐1 signaling? Mech Ageing Dev 2005, 126:381–387. https://doi.org/10.1016/j.mad.2004.09.001.
Wolkow, C, Hall, DH. The Dauer Cuticle. Wormatlas; 2011. Available at: http://www.wormatlas.org/dauer/cuticle/Cutframeset.html.
Colella, E, Li, S, Roy, R. Developmental and cell cycle quiescence is mediated by the nuclear hormone receptor co‐regulator DIN‐1S in the C. elegans dauer larva. Genetics 2016, 203:1763–1776. https://doi.org/10.1534/genetics.116.191858.
Narbonne, P, Roy, R. Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 2006, 133:611–619. https://doi.org/10.1242/dev.02232.
Nelson, FK, Riddle, DL. Functional study of the Caenorhabditis elegans secretory‐excretory system using laser microsurgery. J Exp Zool 1984, 231:45–56. https://doi.org/10.1002/jez.1402310107.
Nelson, FK, Albert, PS, Riddle, DL. Fine structure of the Caenorhabditis elegans secretory—excretory system. J Ultrastruct Res 1983, 82:156–171. https://doi.org/10.1016/S0022‐5320(83)90050‐3.
Schaedel, ON, Gerisch, B, Antebi, A, Sternberg, PW. Hormonal signal amplification mediates environmental conditions during development and controls an irreversible commitment to adulthood. PLoS Biol 2012, 10:e1001306. https://doi.org/10.1371/journal.pbio.1001306.
Albert, PS, Riddle, DL. Mutants of Caenorhabditis elegans that form dauer‐like larvae. Dev Biol 1988, 126:270–293. https://doi.org/10.1016/0012‐1606(88)90138‐8.
Antebi, A, Culotti, JG, Hedgecock, EM. daf‐12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 1998, 125:1191–1205.
Ohkura, K, Suzuki, N, Ishihara, T, Katsura, I. SDF‐9, a protein tyrosine phosphatase‐like molecule, regulates the L3/dauer developmental decision through hormonal signaling in C. elegans. Development 2003, 130:3237–3248. https://doi.org/10.1242/dev.00540.
Li, J, Brown, G, Ailion, M, Lee, S, Thomas, JH. 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 2004, 131:5741–5752. https://doi.org/10.1242/dev.01408.
Chitwood, DJ, Lusby, WR, Lozano, R, Thompson, MJ, Svoboda, JA. Sterol metabolism in the nematode Caenorhabditis elegans. Lipids 1984, 19:500–506. https://doi.org/10.1007/BF02534482.
Matyash, V, Entchev, EV, Mende, F, Wilsch‐Bräuninger, M, Thiele, C, Schmidt, AW, Knölker, H‐J, Ward, S, Kurzchalia, TV. Sterol‐derived hormone(s) controls entry into diapause in Caenorhabditis elegans by consecutive activation of DAF‐12 and DAF‐16. PLoS Biol 2004, 2:e280. https://doi.org/10.1371/journal.pbio.0020280.
Kenyon, C, Chang, J, Gensch, E, Rudner, A, Tabtiang, R. A C. elegans mutant that lives twice as long as wild type. Nature 1993, 366:461–464. https://doi.org/10.1038/366461a0.
Gottlieb, S, Ruvkun, G. daf‐2, daf‐16 and daf‐23: genetically interacting genes controlling dauer formation in Caenorhabditis elegans. Genetics 1994, 137:107–120.
Vowels, JJ, Thomas, JH. Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 1992, 130:105–123.
Jia, K, Chen, D, Riddle, DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development 2004, 131:3897–3906. https://doi.org/10.1242/dev.01255.
Narbonne, P, Roy, R. Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long‐term survival. Nature 2009, 457:210–214. https://doi.org/10.1038/nature07536.
Cunningham, KA, Bouagnon, AD, Barros, AG, Lin, L, Malard, L, Romano‐Silva, MA, Ashrafi, K. Loss of a neural AMP‐activated kinase mimics the effects of elevated serotonin on fat, movement, and hormonal secretions. PLoS Genet 2014, 10:17–20. https://doi.org/10.1371/journal.pgen.1004394.
Ailion, M, Thomas, JH. Isolation and characterization of high‐temperature‐induced dauer formation mutants in Caenorhabditis elegans. Genetics 2003, 165:127–144.
West‐Eberhard, MJ. Developmental plasticity and the origin of species differences. Proc Natl Acad Sci 2005, 102:6543–6549.
Viney, ME, Gardner, MP, Jackson, JA. Variation in Caenorhabditis elegans dauer larva formation. Dev Growth Differ 2003, 45:389–396. https://doi.org/10.1046/j.1440‐169X.2003.00703.x.

Society Partners

	Free online access to WIREs Developmental Biology is a member benefit. Learn More
	SDB Collaborative Resources
	Society for Developmental Biology Homepage

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

The latest WIREs articles in your inbox

Sign Up for Article Alerts