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Post-Embryonic Cell Lineages of the Nematode, Caenorhabditis Elegans

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Post-Embryonic Cell Lineages of the Nematode, Caenorhabditis Elegans DEVELOPMENTAL BIOLOGY 56, 110-156 (1977) Post-embryonic Cell Lineages of the Nematode, Caenorhabditis elegans J. E. SULSTON AND H. R. HORVITZ Medical Research Council Laboratory of Molecular Biology, Hills Road, Cambridge, CB2 2QH, England Received August 23,1976; accepted November 4, 1976 The number of nongonadal nuclei in the free-living soil nematode Caenorhabditis elegans increases from about 550 in the newly hatched larva to about 810 in the mature hermaphrodite and to about 970 in the mature male. The pattern of cell divisions which leads to this increase is essentially invariant among individuals; rigidly determined cell lineages generate a fixed number of progeny cells of strictly specified fates. These lineages range in length from one to eight sequential divisions and lead to significant developmental changes in the neuronal, muscular, hypodermal, and digestive systems. Frequently, several blast cells follow the same asymmetric program of divisions; lineally equivalent progeny of such cells generally differen- tiate into functionally equivalent cells. We have determined these cell lineages by direct observation of the divisions, migrations, and deaths of individual cells in living nematodes. Many of the cell lineages are involved in sexual maturation. At hatching, the hermaphrodite and male are almost identical morphologically; by the adult stage, gross anatomical differences are obvious. Some of these sexual differences arise from blast cells whose division patterns are initially identical in the male and in the hermaphrodite but later diverge. In the hermaphro- dite, these cells produce structures used in egg-laying and mating, whereas, in the male, they produce morphologically different structures which function before and during copulation. In addition, development of the male involves a number of lineages derived from cells which do not divide in the hermaphrodite. Similar postembryonic developmental events occur in other nematode species. INTRODUCTION after hatching. As in embryogenesis, the The development of a multicellular or- pattern of these divisions is rigidly deter- ganism from a unicellular egg involves a mined; essentially invariant postembry- complex pattern of repeated cell divisions. onic cell lineages generate fixed numbers Classical observations of nematode embry- of neurons, glial cells, muscles, and hypo- ogenesis (reviewed by Chitwood and Chit- dermal cells of rigidly specified fates. wood, 1974) revealed that in these orga- These lineages reveal the ancestral rela- nisms early development follows a rigidly tionships among specific cells of known fixed program, i.e., an invariant pattern of structure and function; they thus comple- cell divisions produces specific progeny ment the classical embryology, which de- cells which, in turn, give rise to particular fined the ancestral relationships among parts of the organism. These and similar different organs. We have determined the studies led to the concept of “cell lineages,” postembryonic cell lineages by direct ob- in which the ancestry of different organs servation of living nematodes. can be traced back to specific progenitor C. elegans is an excellent organism for cells and, ultimately, to the egg (e.g., Wil- the study of cell lineages. It is small, easily son, 1925). cultured, and readily amenable to genetic In this paper, we extend these observa- manipulations (Brenner, 1973, 1974). Like tions from the embryonic to the postem- other nematodes (e.g., Chitwood and Chit- bryonic period. Many cell divisions occur wood, 1974), C. elegans is anatomically in the nematode Caenorhabditis elegans simple (Fig. 1). Its tubular body, consist- 110 Copyright 0 1977 by Academic Press, Inc. All rights of reproduction in any form reserved. ISSN 0012-1606 SULSTON AND HORVITZ Cell Lineages of a Nematode 111 112 DEVELOPMENTAL BIOLOGY VOLUME 56, 1977 ing of a hypodermal wall and an underly- ing larval development, we begin with a ing musculature, encloses its digestive and detailed account of the cellular anatomy of reproductive systems. Although it has the young nematode. This anatomy has most major differentiated tissue types been determined by a combination of No- (nerve, muscle, hypodermis, intestine, marski and electron microscopy. and gonad), C. elegans consists of rela- Readers who do not wish to become sub- tively few cells; as we show below, the merged in the detailed descriptions under adult contains fewer than 1000 nongonadal Materials and Methods and Results will nuclei. find a summary of our observations and The life cycle of C. elegans is rapid; in conclusions under Discussion. 3.5 days (at 20°C) it develops from a fertil- MATERIALS AND METHODS ized egg through four larval stages to a mature adult. Superficially, the newly (A) Nematode Strains hatched larva appears to be quite similar Caenorhabditis elegans var. Bristol to the adult. The most obvious develop- (strain N2) was obtained from Sydney mental change is in the size and complex- Brenner and grown on Escherichia coli ity of the gonad, which contains 4 nuclei in OP50 on petri dishes at 2O”C, as described the young larva and increases to about previously (Brenner, 1974). Hermaphro- 2500 in the mature adult (Hirsh et al., dite stocks were propagated by self-ferti- 1976). Gross morphological differences are lization; male stocks were propagated by also apparent in the nongonadal sexual crossing with hermaphrodites. structures of the hermaphrodite and male; Aphelencoides blastophthorus, Longido- these structures are not present in young rus macrosoma, Panagrellus redivivus larvae (Figs. 1 and 2). (Panagrellus silusiae), and Turbatrix Recently, one of us (Sulston, 1976) de- aceti were obtained from David J. Hooper, scribed a technique with which it is possi- Rothamsted Experimental Station, Har- ble to determine cell lineages by observing penden, Hertfordshire, England. Ascaris living nematodes. When appropriately lumbricoides var. suis was obtained from mounted on a thin block of agar on a mi- the local slaughterhouse; eggs were croscope slide, a nematode proceeds squeezed out of adult uteri and develop- through its normal life cycle. Observation ment was initiated by incubation in 0.1 M of such animals under Nomarski differen- sulfuric acid at 25°C (Rogers, 1960); at ap- tial interference contrast optics in the propriate intervals, samples were washed light microscope allows one to directly fol- with insect tissue culture medium (Shields low the migrations, divisions, and deaths et al., 1975) and larvae were released from of individual cells. the eggs by gently rolling the tip of a Pas- Using this technique, we have extended teur pipet over them. the earlier study (Sulston, 1976) of devel- (B) Techniques opment in the ventral nervous system of C. elegans. In this paper, we report the (1) Study of Living Specimens complete postembryonic nongonadal cell (a) Mounting. An agar slab about 0.5 lineages of C. elegans. These lineages pro- mm thick was prepared by flattening a duce the accessory sexual structures of the drop of 5% agar on a microscope slide with hermaphrodite and male and lead to other a second, siliconized slide placed across it; significant developmental changes in the the siliconized slide was supported by neuronal, muscular, hypodermal, and “spacer” slides raised by one or two thick- digestive systems. nessesof adhesive tape. After the agar had To provide a framework for describing hardened, the siliconized slide was re- the anatomical changes which occur dur- moved and a small drop (about 2 ~1) of 10% .%.u%oN AND HORVITZ Cell Lineages of a Nematode 113 114 DEVELOPMENTAL BIOLOG Y VOLUME 56, 1977 polyvinylpyrrolidone (molecular weight Nuclei and large nucleoli were clearly re- 44,000; BDH Chemicals, Ltd., Poole, Eng- solved by Nomarski optics, which permits land) in S medium (Sulston and Brenner, visualization of changes in refractive in- 1974) was placed on the agar, care being dex and has a very shallow depth of field taken not to break its surface. A selected (e.g., Fig. 2). Cell boundaries, however, nematode was transferred to this drop, us- were not always visible. The nuclei of dif- ing either a sharpened wooden stick or a ferent types of cells were generally dis- human eyelash attached with Plasticine to tinguishable and are described under Re- a stick. An animal successfully transferred sults. would thrash wildly. The center of a 12 x This technique is nondestructive and al- 12-mm coverslip was very thinly coated lows the nematode to live under reasona- with E. coli OP50 scraped from a petri dish bly natural conditions. While mounted for with a wire loop. The coverslip was low- observation, the nematode moved freely ered gently onto the agar, care again being between the coverslip and the surface of taken not to break the agar surface. The the agar block. Attracted by the bacterial volume of liquid was such that the pres- lawn, it generally stayed near the middle sure of the coverslip prevented the worm of the coverslip. If the nematode strayed from thrashing without excessively in- out from under the coverslip, it could be hibiting its movement. All of these opera- transferred to a petri dish and remounted. tions were performed at a room tempera- C. elegans can only flex in a dorso-ven- ture of about 20°C. tral direction. Hence, because it was re- Excess agar protruding beyond the cov- stricted to the plane between the agar and erslip was removed with a razor blade. The the coverslip, the nematode was observed edges of the remaining agar block were lying on its side. A properly mounted ani- sealed with silicone grease or Vaseline to mal usually remained lying on the same prevent dehydration. Air bubbles which side. However, for a period just before formed when the coverslip was positioned molting, nematodes actively and repeat- were gradually absorbed by the agar. edly invert their positions with a rapid After a period of quiescence (less than 1 twisting movement. On occasion, such hr), the nematode generally moved into “flips” proved very inconvenient, as they the bacterial lawn and started to feed.
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