Worm Development

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Introduction

C.Elegans

Initially used in the 1960's by Sydney Brenner to study the genetics of development and neurobiology. Early embryological studies of the nematode worm (roundworm) Caenorhabditis elegans (C.Elegans, so called because of its "elegant" curving movement) characterized the fate of each and every cell in the worm through all stages of development. This worm was the first to have its entire genome sequenced and also used recently in space experiments (see below).

  • Sydney Brenner died on April 5, 2019, at age 92.[1]

The USA space shuttle Atlantis in November 2009 launched Caenorhabditis elegans into space as part of an experiment to study RNA interference and protein phosphorylation in a space environment.

"RNA interference and protein phosphorylation in space environment using the nematode Caenorhabditis elegans (CERISE) is an experiment that addresses two scientific objectives. The first is to evaluate the effect of microgravity on ribonucleic acid (RNA) interference. The second is to study how the space environment effects protein phosphorylation (addition of a phosphate molecule) and signal transduction in the muscle fibers of gene knock-downed Caenorhabditis elegans."
Animal Development: axolotl | bat | cat | chicken | cow | dog | dolphin | echidna | fly | frog | goat | grasshopper | guinea pig | hamster | horse | kangaroo | koala | lizard | medaka | mouse | opossum | pig | platypus | rabbit | rat | salamander | sea squirt | sea urchin | sheep | worm | zebrafish | life cycles | development timetable | development models | K12
Historic Embryology  
1897 Pig | 1900 Chicken | 1901 Lungfish | 1904 Sand Lizard | 1905 Rabbit | 1906 Deer | 1907 Tarsiers | 1908 Human | 1909 Northern Lapwing | 1909 South American and African Lungfish | 1910 Salamander | 1951 Frog | Embryology History | Historic Disclaimer

Some Recent Findings

Proposed Hox protein classification
Hox species expression.[2]
  • Unique homeobox codes delineate all the neuron classes of C. elegans[3] "It is not known at present whether neuronal cell-type diversity-defined by cell-type-specific anatomical, biophysical, functional and molecular signatures-can be reduced to relatively simple molecular descriptors of neuronal identity1. Here we show, through examination of the expression of all of the conserved homeodomain proteins encoded by the Caenorhabditis elegans genome2, that the complete set of 118 neuron classes of C. elegans can be described individually by unique combinations of the expression of homeodomain proteins, thereby providing-to our knowledge-the simplest currently known descriptor of neuronal diversity. Computational and genetic loss-of-function analyses corroborate the notion that homeodomain proteins not only provide unique descriptors of neuron type, but also have a critical role in specifying neuronal identity. We speculate that the pervasive use of homeobox genes in defining unique neuronal identities reflects the evolutionary history of neuronal cell-type specification." Hox
  • The Hox Gene egl-5 Acts as a Terminal Selector for VD13 Development via Wnt Signaling[4] "Nervous systems are comprised of diverse cell types that differ functionally and morphologically. During development, extrinsic signals, e.g., growth factors, can activate intrinsic programs, usually orchestrated by networks of transcription factors. Within that network, transcription factors that drive the specification of features specific to a limited number of cells are often referred to as terminal selectors. While we still have an incomplete view of how individual neurons within organisms become specified, reporters limited to a subset of neurons in a nervous system can facilitate the discovery of cell specification programs. We have identified a fluorescent reporter that labels VD13, the most posterior of the 19 inhibitory GABA (γ-amino butyric acid)-ergic motorneurons, and two additional neurons, LUAL and LUAR. Loss of function in multiple Wnt signaling genes resulted in an incompletely penetrant loss of the marker, selectively in VD13, but not the LUAs, even though other aspects of GABAergic specification in VD13 were normal. The posterior Hox gene, egl-5, was necessary for expression of our marker in VD13, and ectopic expression of egl-5 in more anterior GABAergic neurons induced expression of the marker. These results suggest egl-5 is a terminal selector of VD13, subsequent to GABAergic specification." Hox neural
More recent papers 
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More? References | Discussion Page | Journal Searches | 2019 References | 2020 References

Search term: Caenorhabditis elegans Development | Worm Development | Worm Embryology

Older papers 
These papers originally appeared in the Some Recent Findings table, but as that list grew in length have now been shuffled down to this collapsible table.

See also the Discussion Page for other references listed by year and References on this current page.

  • Homeobox Genes of Caenorhabditis elegans and Spatio-Temporal Expression[5] "We show that, out of 103 homeobox genes, 70 are co-orthologous to human homeobox genes. 14 are highly divergent, lacking an obvious ortholog even in other Caenorhabditis species. One of these homeobox genes encodes 12 homeodomains, while three other highly divergent homeobox genes encode a novel type of double homeodomain, termed HOCHOB. To understand how transcription factors regulate cell fate during development, precise spatio-temporal expression data need to be obtained. Using a new imaging framework that we developed, Endrov, we have generated spatio-temporal expression profiles during embryogenesis of over 60 homeobox genes, as well as a number of other developmental control genes using GFP reporters." Hox
  • Basic Caenorhabditis elegans Methods: Synchronization and Observation[6] "Research into the molecular and developmental biology of the nematode Caenorhabditis elegans was begun in the early seventies by Sydney Brenner and it has since been used extensively as a model organism (1). C. elegans possesses key attributes such as simplicity, transparency and short life cycle that have made it a suitable experimental system for fundamental biological studies for many years (2). ...Because of its transparency, C. elegans structures can be distinguished under the microscope using Differential Interference Contrast microscopy, also known as Nomarski microscopy. The use of a fluorescent DNA binder, DAPI (4',6-diamidino-2-phenylindole), for instance, can lead to the specific identification and localization of individual cells, as well as subcellular structures/defects associated to them."
  • Small RNAs and temporal control in Caenorhabditis elegans.[7] "Developmental timing studies in C. elegans led to the landmark discovery of miRNAs and continue to enhance our understanding of the regulation and activity of these small regulatory molecules. Current views of the heterochronic gene pathway are summarized here, with a focus on the ways in which miRNAs contribute to temporal control and how miRNAs themselves are regulated. Finally, the conservation of heterochronic genes and their functions in timing, as well as their related roles in stem cells and cancer, are highlighted."

Adult Anatomy

C elegans cartoon.jpg

Adult Hermaphrodite Gonad

Adult hermaphrodite gonad arm.jpg

Adult hermaphrodite gonad arm[8] - A drawing representation of an adult hermaphrodite gonad arm. The progression of germ cell proliferation and meiosis are indicated by the arrows starting from the distal tip region of the gonad arm.

Male Development

Worm - male development.jpg

The features that differentiate the C. elegans male from the hermaphrodite arise during postembryonic development.[9]

RNA interference

The two researchers, Andrew Z. Fire and Craig C. Mello[10], were investigating how gene expression is regulated in C. elegans and identified the novel regulation method of RNA interference (RNAi), gene silencing by double-stranded RNA. This discovery was awarded the 2006 Nobel Prize in Physiology or Medicine.

Links: 2006 Nobel Press Release


Embryonic Cell Lineages

Worm - embryonic cell lineage 02.jpg

The overview diagram above shows the fate of each individual cell in the developing c. elegans.

  • Zygote (P0 cell) divides into two daughter cells (AB and P1 cells).
  • These two daughter cells then divide into the next generation.
  • the "X" indicates cells that die by apoptosis during development.

Note the above image is not at a readable resolution, to view see large readable version (10,389 × 1,336 pixels). Embryonic cell lineage developed by J .E. Sulston, E. Schierenberg, J. G. White, J. N. Thomson.


Links: Apoptosis | Worm Atlas - Cell Lineages

Gastrointestinal Tract

The worm digestive tract consists of a pharynx (80-cell), intestine, and rectum and contains only about 100 cells. Development is regulated by similar transcription factors found for other species (FoxA and GATA factors).[11] There are also 20 neurons located within the pharynx.{#pmid:15780187|PMID15780187}}

Developmental Genes

  • pha-4 (Drosophila forkhead and vertebrate FoxA) - pharynx and rectum
  • ceh-22 (Drosophila tinman and vertebrate Template:Nkx2.5) - pharynx
  • pha-2 (vertebrate Hex) - pharynx
  • GATA - intestine


References

  1. Pederson T. (2019). The sui generis Sydney Brenner. Proc. Natl. Acad. Sci. U.S.A. , 116, 13155-13157. PMID: 31182578 DOI.
  2. Hueber SD, Weiller GF, Djordjevic MA & Frickey T. (2010). Improving Hox protein classification across the major model organisms. PLoS ONE , 5, e10820. PMID: 20520839 DOI.
  3. Reilly MB, Cros C, Varol E, Yemini E & Hobert O. (2020). Unique homeobox codes delineate all the neuron classes of C. elegans. Nature , , . PMID: 32814896 DOI.
  4. Kurland M, O'Meara B, Tucker DK & Ackley BD. (2020). The Hox Gene egl-5 Acts as a Terminal Selector for VD13 Development via Wnt Signaling. J Dev Biol , 8, . PMID: 32138237 DOI.
  5. Hench J, Henriksson J, Abou-Zied AM, Lüppert M, Dethlefsen J, Mukherjee K, Tong YG, Tang L, Gangishetti U, Baillie DL & Bürglin TR. (2015). The Homeobox Genes of Caenorhabditis elegans and Insights into Their Spatio-Temporal Expression Dynamics during Embryogenesis. PLoS ONE , 10, e0126947. PMID: 26024448 DOI.
  6. Porta-de-la-Riva M, Fontrodona L, Villanueva A & Cerón J. (2012). Basic Caenorhabditis elegans methods: synchronization and observation. J Vis Exp , , e4019. PMID: 22710399 DOI.
  7. Resnick TD, McCulloch KA & Rougvie AE. (2010). miRNAs give worms the time of their lives: small RNAs and temporal control in Caenorhabditis elegans. Dev. Dyn. , 239, 1477-89. PMID: 20232378 DOI.
  8. Bickel JS, Chen L, Hayward J, Yeap SL, Alkers AE & Chan RC. (2010). Structural maintenance of chromosomes (SMC) proteins promote homolog-independent recombination repair in meiosis crucial for germ cell genomic stability. PLoS Genet. , 6, e1001028. PMID: 20661436 DOI.
  9. Emmons SW. (2005). Male development. WormBook , , 1-22. PMID: 18050419 DOI.
  10. Timmons L, Tabara H, Mello CC & Fire AZ. (2003). Inducible systemic RNA silencing in Caenorhabditis elegans. Mol. Biol. Cell , 14, 2972-83. PMID: 12857879 DOI.
  11. Kormish JD, Gaudet J & McGhee JD. (2010). Development of the C. elegans digestive tract. Curr. Opin. Genet. Dev. , 20, 346-54. PMID: 20570129 DOI.

Books

WormBook - a comprehensive, open-access collection of original, peer-reviewed chapters covering topics related to the biology of Caenorhabditis elegans and other nematodes.

Nigon VM & Félix MA. (2017). History of research on C. elegans and other free-living nematodes as model organisms. WormBook , 2017, 1-84. PMID: 28326696 DOI.

Gieseler K, Qadota H & Benian GM. (2017). Development, structure, and maintenance of C. elegans body wall muscle. WormBook , 2017, 1-59. PMID: 27555356 DOI.

Hillers KJ, Jantsch V, Martinez-Perez E & Yanowitz JL. (2017). Meiosis. WormBook , 2017, 1-43. PMID: 26694509 DOI.


Links: Search WormBook by date

Reviews

Liang JJH, McKinnon IA & Rankin CH. (2020). The contribution of C. elegans neurogenetics to understanding neurodegenerative diseases. J. Neurogenet. , , 1-22. PMID: 32772603 DOI.

Rothman J & Jarriault S. (2019). Developmental Plasticity and Cellular Reprogramming in Caenorhabditis elegans. Genetics , 213, 723-757. PMID: 31685551 DOI.

Dimov I & Maduro MF. (2019). The C. elegans intestine: organogenesis, digestion, and physiology. Cell Tissue Res. , 377, 383-396. PMID: 31065800 DOI.

Pintard L & Bowerman B. (2019). Mitotic Cell Division in Caenorhabditis elegans. Genetics , 211, 35-73. PMID: 30626640 DOI.

Murray JI. (2018). Systems biology of embryonic development: Prospects for a complete understanding of the Caenorhabditis elegans embryo. Wiley Interdiscip Rev Dev Biol , 7, e314. PMID: 29369536 DOI.

Maduro MF. (2017). Gut development in C. elegans. Semin. Cell Dev. Biol. , 66, 3-11. PMID: 28065852 DOI.

Articles

Rödelsperger C, Ebbing A, Sharma DR, Okumura M, Sommer RJ & Korswagen HC. (2020). Spatial transcriptomics of nematodes identifies sperm cells as a source of genomic novelty and rapid evolution. Mol. Biol. Evol. , , . PMID: 32785688 DOI.

Search Pubmed

July 2010 "c elegans Development" All (5126) Review (898) Free Full Text (2363)


Search Pubmed: Worm Development | Caenorhabditis elegans Development | c elegans Development

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Animal Development: axolotl | bat | cat | chicken | cow | dog | dolphin | echidna | fly | frog | goat | grasshopper | guinea pig | hamster | horse | kangaroo | koala | lizard | medaka | mouse | opossum | pig | platypus | rabbit | rat | salamander | sea squirt | sea urchin | sheep | worm | zebrafish | life cycles | development timetable | development models | K12
Historic Embryology  
1897 Pig | 1900 Chicken | 1901 Lungfish | 1904 Sand Lizard | 1905 Rabbit | 1906 Deer | 1907 Tarsiers | 1908 Human | 1909 Northern Lapwing | 1909 South American and African Lungfish | 1910 Salamander | 1951 Frog | Embryology History | Historic Disclaimer

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Cite this page: Hill, M.A. (2024, March 19) Embryology Worm Development. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Worm_Development

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