Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Control of developmental timing in animals

Nature Reviews Genetics volume 2, pages 690–701 (2001)Cite this article

Key Points

  • The heterochronic genes of Caenorhabditis elegans control the timing and sequence of several post-embryonic developmental events, including the terminal differentiation of the hypodermis.

  • Mutations in heterochronic genes cause hypodermal-cell terminal differentiation to occur too early (precocious phenotype) or too late (retarded phenotype) relative to other unaffected events.

  • The 22-nucleotide lin-4 RNA molecule downregulates lin-14 and lin-28 expression at a step subsequent to translation initiation by interacting with antisense complementary sites in the 3′ untranslated regions of their mRNAs.

  • Temporal downregulation of LIN-14 and LIN-28 guides development from the first to the third larval stage.

  • The let-7 RNA molecule begins to accumulate in the late third larval stage and downregulates lin-41, and possibly other genes, freeing lin-29 to trigger the switch to the terminally differentiated adult stage.

  • let-7 is evolutionarily conserved from worms to humans and is developmentally regulated in some organisms, including flies, indicating a temporal regulatory function might also be conserved.

  • The production of the small lin-4 and let-7 RNAs uses components required to generate the small double-stranded RNAs involved in the mechanism of RNA interference.

  • Hormonal inputs are a common theme in the control of developmental time in diverse animals.

Abstract

The molecular mechanisms that time development are now being deciphered in various organisms, particularly in Caenorhabditis elegans. Key recent findings indicate that certain C. elegans timekeeping genes are conserved across phyla, and their developmental expression patterns indicate that a timing function might also be conserved. Small regulatory RNAs have crucial roles in the timing mechanism, and the cellular machinery required for production of these RNAs intersects with that used to process double-stranded RNAs during RNA interference.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The hypodermal seam-cell lineage programmes.
Figure 2: Terminal differentiation of the lateral hypodermis.
Figure 3: Predicted gene regulatory interactions and temporal accumulation of gene products.
Figure 4: let-7 sequences and predicted RNA duplexes.
Figure 5: Phylogenetic comparison of let-7 expression.
Figure 6: Developmental timing of scale maturation in butterflies.

Similar content being viewed by others

References

  1. Gellon, G. & McGinnis, W. Shaping animal body plans in development and evolution by modulation of Hox expression patterns. Bioessays 20, 116–125 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Zarkower, D. Establishing sexual dimorphism: conservation amidst diversity? Nature Rev. Genet. 2, 175–185 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Ferrier, D. E. & Holland, P. W. Ancient origin of the Hox gene cluster. Nature Rev. Genet. 2, 33–38 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Simon, M.-N., Pelegrini, O., Vernon, M. & Kay, R. R. Mutation of protein kinase A causes heterochronic development of Dictyostelium. Nature 356, 171–172 (1992).

    Article  CAS  PubMed  Google Scholar 

  5. Ebens, A. J., Garren, H., Cheyette, B. N. R. & Zipursky, S. L. The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74, 15–27 (1993).

    Article  CAS  PubMed  Google Scholar 

  6. Ambros, V. & Horvitz, H. R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416 (1984).

    Article  CAS  PubMed  Google Scholar 

  7. Evans, M. M. S., Passas, H. J. & Poethig, R. S. Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. Development 120, 1971–1981 (1994).

    CAS  PubMed  Google Scholar 

  8. Poethig, R. S. Heterochronic mutations affecting shoot development in maize. Genetics 119, 959–973 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Dudley, M. & Poethig, R. S. The heterochronic Teopod1 and Teopod2 mutations of maize are expressed non-cell-autonomously. Genetics 133, 389–399 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Dudley, M. & Poethig, R. S. The effect of a heterochronic mutation, Teopod2, on the cell lineage of the maize shoot. Development 111, 733–739 (1991).

    CAS  PubMed  Google Scholar 

  11. Telfer, A. & Poethig, R. S. HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development 125, 1889–1898 (1998).

    CAS  PubMed  Google Scholar 

  12. Berardini, T. Z., Bollman, K., Sun, H. & Poethig, R. S. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291, 2405–2407 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Itoh, J. I., Hasegawa, A., Kitano, H. & Nagato, Y. A recessive heterochronic mutation, plastochron1, shortens the plastochron and elongates the vegetative phase in rice. Plant Cell 10, 1511–1522 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Sulston, J. E. & Horvitz, H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110–156 (1977).

    Article  CAS  PubMed  Google Scholar 

  15. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119 (1983).

    Article  CAS  PubMed  Google Scholar 

  16. Hallam, S. J. & Jin, Y. lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans. Nature 395, 78–82 (1998).

    Article  CAS  PubMed  Google Scholar 

  17. Liu, Z. & Ambros, V. Heterochronic genes control the stage-specific initiation and expression of the dauer larva developmental program in Caenorhabditis elegans. Genes Dev. 3, 2039–2049 (1989).

    Article  CAS  PubMed  Google Scholar 

  18. Euling, S. & Ambros, V. Heterochronic genes control cell cycle progress and developmental competence of C. elegans vulva precursor cells. Cell 84, 667–676 (1996).

    Article  CAS  PubMed  Google Scholar 

  19. Ambros, V. A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 57, 49–57 (1989).lin-4, lin-14, lin-28 and lin-29 , first described as heterochronic genes in reference 6 , are masterfully ordered into a genetic regulatory hierarchy with respect to the control of seam-cell terminal differentiation.

    Article  CAS  PubMed  Google Scholar 

  20. Singh, R. N. & Sulston, J. E. Some observations on moulting in Caenorhabditis elegans. Nematologica 24, 63–71 (1978).

    Article  Google Scholar 

  21. Cox, G. N., Staprans, S. & Edgar, R. S. The cuticle of Caenorhabditis elegans. II. Stage-specific changes in ultrastructure and protein composition during postembryonic development. Dev. Biol. 86, 456–470 (1981).

    Article  CAS  PubMed  Google Scholar 

  22. Cox, G. N. & Hirsh, D. Stage-specific patterns of collagen gene expression during development of Caenorhabditis elegans. Mol. Cell. Biol. 5, 363–372 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Liu, Z., Kirch, S. & Ambros, V. The heterochronic gene pathway controls stage-specific transcription of C. elegans collagen genes. Development 121, 2471–2478 (1995).

    CAS  PubMed  Google Scholar 

  24. Ambros, V. Control of developmental timing in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 10, 428–433 (2000).

    Article  CAS  PubMed  Google Scholar 

  25. Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993).The cloning of lin-4 and the surprising finding that it encodes a small regulatory RNA molecule, and together with reference 36 , the identification of lin-14 as a target.

    Article  CAS  PubMed  Google Scholar 

  26. Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906 (2000).Identification of let-7 as the second, small regulatory RNA in the heterochronic gene pathway, and demonstration that lin-41 is downregulated during late post-embryonic development in a let-7 -dependent manner.

    Article  CAS  PubMed  Google Scholar 

  27. Pasquinelli, A. E. et al. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89 (2000).let-7 RNA is shown to be evolutionarily conserved from worms to humans, and intriguing patterns of developmentally regulated expression observed in some organisms, raises the possibility that a temporal-regulatory function has also been conserved.

    Article  CAS  PubMed  Google Scholar 

  28. Ambros, V. & Horvitz, H. R. The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev. 1, 398–414 (1987).

    Article  CAS  PubMed  Google Scholar 

  29. Ambros, V. & Moss, E. G. Heterochronic genes and the temporal control of C. elegans development. Trends Genet. 10, 123–127 (1994).

    Article  CAS  PubMed  Google Scholar 

  30. Reinhart, B. J. & Ruvkun, G. Isoform-specific mutations in the Caenorhabditis elegans heterochronic gene lin-14 affect stage-specific patterning. Genetics 157, 199–209 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Ruvkun, G. & Giusto, J. The Caenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature 338, 313–319 (1989).

    Article  CAS  PubMed  Google Scholar 

  32. Arasu, P. A., Wightman, B. & Ruvkun, G. Temporal regulation of lin-14 by the antagonistic action of two other heterochronic genes, lin-4 and lin-28. Genes Dev. 5, 1825–1833 (1991).

    Article  CAS  PubMed  Google Scholar 

  33. Moss, E. G., Lee, R. C. & Ambros, V. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88, 637–646 (1997).The identification of lin-28 as a probable RNA-binding protein and the demonstration of a second target of the lin-4 RNA.

    Article  CAS  PubMed  Google Scholar 

  34. Ruvkun, G. et al. Molecular genetics of the Caenorhabditis elegans heterochronic gene lin-14. Genetics 121, 501–516 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Hong, Y., Lee, R. C. & Ambros, V. Structure and function analysis of LIN-14, a temporal regulator of postembryonic developmental events in Caenorhabditis elegans. Mol. Cell. Biol. 20, 2285–2295 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862 (1993).

    Article  CAS  PubMed  Google Scholar 

  37. Feinbaum, R. & Ambros, V. The timing of lin-4 RNA accumulation controls the timing of postembryonic developmental events in Caenorhabditis elegans. Dev. Biol. 210, 87–95 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Olsen, P. H. & Ambros, V. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671–680 (1999).

    Article  CAS  PubMed  Google Scholar 

  39. Jeon, M., Gardner, H. F., Miller, E. A., Deshler, J. & Rougvie, A. E. Similarity of the C. elegans developmental timing protein LIN-42 to circadian rhythm proteins. Science 286, 1141–1146 (1999).Demonstration that lin-42 encodes a PAS-domain protein most similar to that of Drosophila Per, thereby providing a molecular link between the circadian and developmental timing pathways. Also, lin-42 mRNA levels are shown to oscillate relative to the molting cycles of post-embryonic development.

    Article  CAS  PubMed  Google Scholar 

  40. Liu, Z. Genetic Control of Stage-Specific Developmental Events in C. elegans. PhD thesis, Harvard Univ., Cambridge, Massachusets (1990).

    Google Scholar 

  41. Young, M. W. Life's 24-hour clock: molecular control of circadian rhythms in animal cells. Trends Biochem. Sci. 25, 601–606 (2000).

    Article  CAS  PubMed  Google Scholar 

  42. King, D. P. & Takahashi, J. S. Molecular genetics of circadian rhythms in mammals. Annu. Rev. Neurosci. 23, 713–742 (2000).

    Article  CAS  PubMed  Google Scholar 

  43. Konopka, R. J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112–2116 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hardin, P. E., Hall, J. C. & Rosbash, M. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343, 536–540 (1990).

    Article  CAS  PubMed  Google Scholar 

  45. Kyriacou, C. P., Oldroyd, M., Wood, J., Sharp, M. & Hill, M. Clock mutations alter developmental timing in Drosophila. Heredity 64, 395–401 (1990).

    Article  PubMed  Google Scholar 

  46. Clayton, J. D., Kyriacou, C. P. & Reppert, S. M. Keeping time with the human genome. Nature 409, 829–831 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Abrahante, J. E., Miller, E. A. & Rougvie, A. E. Identification of heterochronic mutants in Caenorhabditis elegans: temporal misexpression of a collagen::green fluorescent protein fusion gene. Genetics 149, 1335–1351 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Antebi, A., Culotti, J. G. & Hedgecock, E. M. daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 125, 1191–1205 (1998).

    CAS  PubMed  Google Scholar 

  49. Antebi, A., Yeh, W. H., Tait, D., Hedgecock, E. M. & Riddle, D. L. daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev. 14, 1512–1527 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Rougvie, A. E. & Ambros, V. The heterochronic gene lin-29 encodes a zinc finger protein that controls a terminal differentiation event in C. elegans. Development 121, 2491–2500 (1995).

    CAS  PubMed  Google Scholar 

  51. Slack, F. J. et al. The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5, 659–669 (2000).The demonstration that LIN-41 is probably an RNA-binding protein that might directly regulate lin-29 translation. let-7 -binding sites in the 3′ UTR are shown to be required for downregulation of lin-41 during late post-embryonic development.

    Article  CAS  PubMed  Google Scholar 

  52. Bettinger, J. C., Lee, K. & Rougvie, A. E. Stage-specific accumulation of the terminal differentiation factor LIN-29 during C. elegans development. Development 122, 2517–2527 (1996).

    CAS  PubMed  Google Scholar 

  53. Chan, E. K., Hamel, J. C., Buyon, J. P. & Tan, E. M. Molecular definition and sequence motifs of the 52-kD component of human SS-A/Ro autoantigen. J. Clin. Invest. 87, 68–76 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sonoda, J. & Wharton, R. P. Drosophila Brain tumor is a translational repressor. Genes Dev. 15, 762–773 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Riddle, D. L., Swanson, M. M. & Albert, P. S. Interacting genes in nematode dauer larva formation. Nature 290, 668–671 (1981).

    Article  CAS  PubMed  Google Scholar 

  56. Thomas, J. H. Chemosensory regulation of development in C. elegans. Bioessays 15, 791–797 (1993).

    Article  CAS  PubMed  Google Scholar 

  57. Sharp, P. A. RNA interference −2001. Genes Dev. 15, 485–490 (2001).

    Article  CAS  PubMed  Google Scholar 

  58. Grishok, A. et al. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23–34 (2001).This paper provides a link between RNA interference and the heterochronic gene pathway by showing that production of siRNAs and stRNAs use shared components.

    Article  CAS  PubMed  Google Scholar 

  59. Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366 (2001).

    Article  CAS  PubMed  Google Scholar 

  60. Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let–7 small temporal RNA. Science 293, 834–838 (2001).

    Article  CAS  PubMed  Google Scholar 

  61. Parrish, S., Fleenor, J., Xu, S., Mello, C. & Fire, A. Functional anatomy of a dsRNA trigger: differential requirement for the two trigger strands in RNA interference. Mol. Cell 6, 1077–1087 (2000).

    Article  CAS  PubMed  Google Scholar 

  62. Bettinger, J. C., Euling, S. & Rougvie, A. E. The terminal differentiation factor LIN-29 is required for proper vulval morphogenesis and egg laying in Caenorhabditis elegans. Development 124, 4333–4342 (1997).

    CAS  PubMed  Google Scholar 

  63. Newman, A. P., Inoue, T., Wang, M. & Sternberg, P. W. The Caenorhabditis elegans heterochronic gene lin-29 coordinates the vulval–uterine–epidermal connections. Curr. Biol. 10, 1479–1488 (2000).

    Article  CAS  PubMed  Google Scholar 

  64. Hodin, J. & Riddiford, L. M. Parallel alterations in the timing of ovarian Ecdysone receptor and Ultraspiracle expression characterize the independent evolution of larval reproduction in two species of gall midges (Diptera: Cecidomyiidae). Dev. Genes Evol. 210, 358–372 (2000).

    Article  CAS  PubMed  Google Scholar 

  65. Hodin, J. & Riddiford, L. M. The Ecdysone receptor and Ultraspiracle regulate the timing and progression of ovarian morphogenesis during Drosophila metamorphosis. Dev. Genes Evol. 208, 304–317 (1998).

    Article  CAS  PubMed  Google Scholar 

  66. Koch, P. B., Lorenz, U., Brakefield, P. M. & ffrench-Constant, R. H. Butterfly wing pattern mutants: developmental heterochrony and co-ordinately regulated phenotypes. Dev. Genes Evol. 210, 536–544 (2000).

    Article  CAS  PubMed  Google Scholar 

  67. Koch, P. B. Color pattern specific melanin synthesis is controlled by ecdysteroids via dopadecarboxylase in wings of Precis coenia. Eur. J. Entomol. 92, 161–167 (1995).

    CAS  Google Scholar 

  68. Huhtaniemi, I. The Parkes lecture. Mutations of gonadotrophin and gonadotrophin receptor genes: what do they teach us about reproductive physiology? J. Reprod. Fertil. 119, 173–186 (2000).

    Article  CAS  PubMed  Google Scholar 

  69. Weiss, J. et al. Hypogonadism caused by a single amino acid substitution in the β-subunit of luteinizing hormone. N. Engl. J. Med. 326, 179–183 (1992).

    Article  CAS  PubMed  Google Scholar 

  70. Gould, S. J. in Evolution and development (ed. Bonner, J. T.) (Springer, New York, 1982).

    Google Scholar 

  71. Fire, A. et al. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811 (1998).

    Article  CAS  PubMed  Google Scholar 

  72. Kennerdell, J. R. & Carthew, R. W. Heritable gene silencing in Drosophila using double-stranded RNA. Nature Biotechnol. 18, 896–898 (2000).

    Article  CAS  Google Scholar 

  73. Wianny, F. & Zernicka-Goetz, M. Specific interference with gene function by double-stranded RNA in early mouse development. Nature Cell Biol. 2, 70–75 (2000).

    Article  CAS  PubMed  Google Scholar 

  74. Hammond, S. M., Caudy, A. A. & Hannon, G. J. Post-transcriptional gene silencing by double-stranded RNA. Nature Rev. Genet. 2, 110–119 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Montgomery, M. K., Xu, S. & Fire, A. RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 95, 15502–15507 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hamilton, A. J. & Baulcombe, D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).

    Article  CAS  PubMed  Google Scholar 

  77. Hammond, S. M., Bernstein, E., Beach, D. & Hannon, G. J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 404, 293–296 (2000).

    Article  CAS  PubMed  Google Scholar 

  78. Zamore, P. D., Tuschl, T., Sharp, P. A. & Bartel, D. P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25–33 (2000).

    Article  CAS  PubMed  Google Scholar 

  79. Tabara, H. et al. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99, 123–132 (1999).

    Article  CAS  PubMed  Google Scholar 

  80. Ketting, R. F., Haverkamp, T. H., van Luenen, H. G. & Plasterk, R. H. mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99, 133–141 (1999).

    Article  CAS  PubMed  Google Scholar 

  81. Grishok, A., Tabara, H. & Mello, C. C. Genetic requirements for inheritance of RNAi in C. elegans. Science 287, 2494–2497 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Parrish, S. & Fire, A. Distinct roles for RDE-1 and RDE-4 during RNA interference in C. elegans. RNA (in the press).

  83. Fagard, M., Boutet, S., Morel, J. B., Bellini, C. & Vaucheret, H. AGO1, QDE-2, and RDE-1 are related proteins required for post-transcriptional gene silencing in plants, quelling in fungi, and RNA interference in animals. Proc. Natl Acad. Sci. USA 97, 11650–11654 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Bohmert, K. et al. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170–180 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I thank J. Simon, J. Shaw, M. Montgomery, H. Gardner and D. Zarkower for discussions and critical reading of the manuscript and C. Mello and A. Fire for sharing results before publication. My apologies to those whose work could not be cited owing to space constraints. The Rougvie laboratory is supported by the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Genetics, Cell Biology and Development, 250 BioScience Center, University of Minnesota, 1445 Gortner Avenue, St Paul, 55108, Minnesota, USA

    Ann E. Rougvie

Authors
  1. Ann E. Rougvie
    View author publications

    You can also search for this author in PubMed Google Scholar

Related links

Related links

DATABASE LINKS

alg-1

alg-2

anachronism

lin-28

lin-29

lin-4

let-7

lin-14

lin-46

lin-42

daf-12

col-19

lin-41

dcr-1

EcR

usp

FURTHER INFORMATION

CaenorhabditiselegansWWW.server

WormBase

Glossary

BILATERIAN

An animal that has bilateral symmetry — a form of symmetry in which the body axis can be divided by a sagittal plane into two mirror-image parts.

DIPLOBLAST

An animal with only two germ layers (ectoderm and endoderm), including the Cnidaria, Ctenophora and, according to some authors, Placozoa and Porifera.

HETEROCHRONIC MUTATION

A heterochronic mutation — from the Greek heteros, meaning other or different, and chronos, meaning time — alters the relative timing of developmental events as an organism grows.

BLAST CELL

An undifferentiated precursor cell.

DAUER LARVA

Juvenile nematode in which development is arrested during unsuiTable conditions and resumes when conditions improve.

ADHERENS JUNCTIONS

Cell–cell adhesive junctions that are linked to cytoskeletal filaments of the micro- filament type.

EPISTATIC

When one gene masks the expression of another. If mutant a gives phenotype A and mutant b gives phenotype B, and if the double mutant ab gives phenotype A and not B, then gene a is epistatic to gene b.

PENETRANCE

The proportion of genotypically mutant organisms that show the mutant phenotype. If all genotypically mutant individuals show the mutant phenotype, then the genotype is said to be completely penetrant.

ECDYSONE

Class of steroid hormones found in insects, crustaceans and some plants. In insects, ecdysone stimulates moulting and metamorphosis.

PAEDOGENETIC

A type of animal that shows precocious sexual mating in larval stage.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rougvie, A. Control of developmental timing in animals. Nat Rev Genet 2, 690–701 (2001). https://doi.org/10.1038/35088566

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35088566

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing