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Caenorhabditis Elegans (Nematode) Provided for non-commercial research and educational use. Not for reproduction, distribution or commercial use. This article was originally published in Brenner’s Encyclopedia of Genetics, 2nd edition, published by Elsevier, and the attached copy is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier’s permissions site at: http://www.elsevier.com/locate/permissionusematerial Palikaras K and Tavernarakis N, Caenorhabditis elegans (Nematode). In: Stanley Maloy and Kelly Hughes, editors. Brenner’s Encyclopedia of Genetics 2nd edition, Vol 1. San Diego: Academic Press; 2013. p. 404–408. Author's personal copy Caenorhabditis elegans (Nematode) K Palikaras and N Tavernarakis, Foundation for Research and Technology – Hellas, Crete, Greece; University of Crete, Crete, Greece © 2013 Elsevier Inc. All rights reserved. This article is a revision of the previous edition article by J Hodgkin, volume 1, pp 251–256, © 2001, Elsevier Inc. Glossary Molting The end of each larval stage of C. elegans is Dauer An alternative larval form that Caenorhabditis marked with a molt where new cuticle is synthesized and elegans animals enter under conditions of environmental the old one is shed. Before molting, the animal enters a stress, nutrient deprivation, and/or overcrowding. brief lethargus stage. Diapause A stage of arrested development or quiescence. Nictation A dauer larva-specific behavioral pattern, where Differential interference contrast (DIC) microscopy Also animals crawl up on the substrate and wave back and forth known as Nomarski microscopy; a phase-contrast while standing on their tail (dispersal behavior). approach taking advantage of different refractive indexes Polycistronic mRNA Encodes several different proteins. within the sample to visualize transparent structures. These proteins are usually functionally related and are Gonochorism Method of reproduction in which male and coregulated in an operon. female germ cells are provided by two sexes and fertilized RNA interference (RNAi) A gene silencing phenomenon, within the female; the opposite of hermaphroditism. whereby double-stranded RNA fragments elicit Inbreeding depression The reduced fitness of individual degradation of cognate mRNAs. RNAi provides an progeny within a population, resulting from breeding of effective approach for gene knockdown and assessment of genetically related parents. loss-of-function phenotypes. Lethargus Animal behavioral state in which nematodes Transgenesis A process of introducing exogenous genes become generally inactive for a period of time, usually (transgenes) into a living organism. Transgenes are prior to shedding of the cuticle. typically transmitted to the offspring. Introduction Cross-fertilization of hermaphrodites with males allows the gen­ eration of double or multiple mutants, facilitating genetic Caenorhabditis elegans is a small, soil dwelling, and free-living analysis. Reproduction of C. elegans by self-fertilization allows (nonparasitic) nematode worm (phylum Nematoda, com­ the generation of genetically identical populations that do not monly known as roundworms). In the wild, C. elegans and undergo inbreeding depression. other Caenorhabditis species are found on most continents and Although C. elegans is a relatively modern addition to the many isolated territories. Animals of the Caenorhabditis genus arsenal of model organisms, its biology has already been inves­ preferentially colonize various microbe-rich habitats, such tigated to an exceptional level. The simple body plan, the as rotting plant material. More than 25 species of the transparent egg and cuticle, and the nearly invariant develop­ Caenorhabditis genus have been characterized up to date. mental plan of this nematode have facilitated exceptionally Although, Caenorhabditis species exhibit many morphological detailed developmental and anatomical characterization of similarities, they are highly divergent at the genetic level. the animal (detailed information is available online at the Genetic divergence reflects ecological specialization and terri­ WormAtlas website). The complete sequence of cell divisions torial distribution of different species. (the cell lineage) and the normal pattern of programmed cell The C. elegans adult reaches a length of about 1 mm and a deaths that occur as the fertilized egg develops into the adult diameter of 80 µm. In the laboratory, animals can be grown in have been elaborated. Wild-type hermaphrodites consist of 959 liquid medium or on agar plates seeded with Escherichia coli and somatic cells, 302 of which are neurons. The transparency of can be easily cultivated in large numbers. C. elegans has five the animal body allows easy visualization and monitoring of pairs of autosomes and one pair of sex chromosomes (XX). cellular processes and has permitted recording and determina­ Most species of the phylum Nematoda are gonochoristic, with tion of the complete pattern of cell divisions that generate the separate female and male sexes that reproduce through 959 somatic cells of the adult (the cell lineage). Cells can be cross-fertilization. Hermaphroditic species also exist, which easily followed during development using differential interfer­ reproduce by self-fertilization. C. elegans is primarily a hermaph­ ence contrast (DIC) light microscopy. Despite its apparent roditic species but males also exist (Figures 1 and 2, respectively). simplicity, there is a high degree of differentiation; worms The ratio of sex chromosomes to autosomes determines sex. have muscle cells, hypodermis, a nervous system, intestine, Hermaphrodites, the dominant sexual form, are diploid for the gonads, glands, and an excretory system. The nematode is one sex chromosome (XX), whereas males, which arise sporadically at of the few multicellular organisms for which routine cryo­ a frequency of 0.1%, have only one X chromosome (XO). Male preservation has been made possible. C. elegans strains can be population can be easily maintained through mating with her­ stored indefinitely in liquid nitrogen, making the maintenance maphrodites. A single hermaphrodite produces about 300 and distribution of large collections of mutants feasible and progeny by self-fertilization and more if it mates with males. cost-effective. 404 Brenner’s Encyclopedia of Genetics, 2nd Edition, Volume 1 doi:10.1016/B978-0-12-374984-0.00186-8 Author's personal copy Caenorhabditis elegans (Nematode) 405 (a) (b) 2B 2C 2D Distal gonad 2E 2F Pharynx Intestine Anus Uterus Proximal gonad Figure 1 Anatomy of the adult C. elegans hermaphrodite. (a) DIC image of an adult C. elegans hermaphrodite. Scale = 100 µm. (b) Anatomical features of the C. elegans hermaphrodite. Dotted lines and number-letter combinations signify individual EM cross-sections shown in WormAtlas. Courtesy of WormAtlas (http://www.wormatlas.org/hermaphrodite/introduction/IMAGES/introfig1.jpg). (a) Proctodeum Gonad Vas deferens Seminal vesicle (b) (c) (e) (d) Figure 2 Anatomy of the adult male. (a) Anatomical features of C. elegans males. (b) DIC image of an adult C. elegans male. Scale = 100 µm. (c) Enlarged image of the unilobed distal gonad of the adult male that is shown in (b). (d) Tail of the adult C. elegans male. The cloaca and the fan are indicated by the arrow and the arrowhead, respectively. (e) The C. elegans male tail is starting to bugle at the L3 larva stage (bottom). At L4 larva stage, the tail hypodermis has retracted (arrowhead, top). Courtesy of WormAtlas (http://www.wormatlas.org/hermaphrodite/introduction/IMAGES/introfig5.jpg). Life Cycle (Figure 3). After fertilization of oocytes, embryonic develop­ ment takes 14 h to complete. Eggs then hatch into L1 larvae. C. elegans completes a reproductive life cycle in 2.5 days at The next 50 h, larval development proceeds through three addi­ 25 °C (or in 3.5 days at 20 °C), progressing from fertilized tional developmental stages L2, L3, and L4. All these juvenile embryos through four larval stages (L1–L4), to become stages are separated by a short phase of lethargus and molting. egg-laying adults, which then live for about 2–3 weeks C. elegans develops and reproduces within a wide range of Author's personal copy 406 Caenorhabditis elegans (Nematode) Adult (1110–1150 μm) (capable of egg laying) 8 h In utero development Young adult (150 min) Eggs laid at gastrula First cleavage (40 min) (∼30-cell) (900–940 μm) L4/adult molt Comma 10 h E 1.5-fold x ut L4 (620–650 μm) er o de ve lo p e m t L3/L4 molt ( 6 h Twofold up to 4 months ) 8 h Dauer (400 μm) L3 (490–510 μm) 13 h Threefold Predauer (L2d) Arrest if no food L1/L2 molt L2/L3 molt Crowding L1 (250 μm) 8 h Starvation μ L2 (360–380 m) High temp. Hatching 12 h L1/L2 molt Figure 3 The life cycle of C. elegans. Numbers in blue indicate the approximate time spent at each developmental stage (22 °C). The first cleavage takes places at about 140 min postfertilization. Eggs are laid at about 150 min postfertilization. The length of the animal in micrometers at each
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