The somatic lineage of the hermaphroditic nematode Caenorhabditis elegans has been mapped and is largely invariant, whereas germ cells proliferate continuously in a stem cell niche during larval and adult stages.
Early embryonic cell divisions are rapid and lack G1 (gap 1) and G2 (gap 2) phases. The introduction of a G2 phase is first observed at gastrulation, and the available evidence indicates that G1 phase is only present late in embryogenesis in a small minority of actively dividing cells.
Variations in early embryonic cell-cycle timing between lineages are due to different rates of DNA replication, which are attributable, in part, to the differential activation of the DNA-replication checkpoint.
Post-embryonic cell lineages are tightly regulated, with rounds of cell divisions beginning and ending at specific points during larval development. The extrinsic or intrinsic signals that determine the timing of initial cell-cycle entry are not known, although alterations in the heterochronic pathway, which specifies the order of larval programmes, can indirectly alter the timing of cell divisions.
The effectors of cell-cycle entry and exit are conserved cell-cycle regulators and include: G1 cyclin–CDK complexes, which are required for cell-cycle entry; and a CDK inhibitor, an Rb homologue and an SCF ubiquitin ligase complex, which mediate cell-cycle exit.
Cell-cycle perturbations usually do not block differentiation, although the failure to produce adequate cell numbers can alter differentiation choices.
Endoreplication (which is a cell cycle that lacks mitosis) occurs in the intestine and hypodermis, and is apparently used to increase the genome ploidy without the disruption of organ structure that would occur as a result of mitotic division.
Germ cell proliferation is dependent on the Delta homologue LAG-2 signal that is provided by the distal tip cell and is recognized by the GLP-1/Notch receptor on germ cells. In the absence of GLP-1 signalling, germ cells enter meiosis. In L3/L4 larval-stage hermaphrodites, proximal germ cells, which lack the LAG-2 signal, enter meiosis to create sperm, whereas in adults, germ cells enter meiosis to generate oocytes.
GLP-1 signalling maintains mitotic proliferation of germ cells by inhibiting a translational inhibitor (GLD-1) and a cytoplasmic poly(A) polymerase complex (GLD-2–GLD-3) that function in parallel pathways. GLD-1 and GLD-3 expression is inhibited in proliferating germ cells by translational repression through the PUF family members FBF-1 and FBF-2.
Cell-cycle regulators that mediate cell-cycle exit in somatic cells are not required for the negative regulation of germ cell proliferation, except in cases in which germ cell proliferation is halted in response to extrinsic signals (for example, lack of food).
The adult Caenorhabditis elegans nematode, a small roundworm, has a precisely defined number of somatic cells that create organs that are also found in larger animals, including intestine, muscles, skin, an excretory system and a primitive brain. Every cell has a defined role in this sophisticated, but tiny animal. Therefore, stringent control of the cell cycle is required to produce the almost invariant cell lineage that generates the C. elegans somatic body plan. The proliferation of germ cells is regulated differently, and occurs within a stem cell niche.
Subscribe to Journal
Get full journal access for 1 year
only $4.92 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Ankeny, R. A. The natural history of Caenorhabditis elegans research. Nature Rev. Genetics 2, 474–479 (2001).
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). A landmark paper that describes the full embryonic cell lineage and provides an account of all somatic cells generated during embryonic and larval development.
Edgar, L. G. & McGhee, J. D. DNA synthesis and the control of embryonic gene expression in C. elegans. Cell 53, 589–599 (1988).
Park, M. & Krause, M. W. Regulation of postembryonic G1 cell cycle progression in Caenorhabditis elegans by a cyclin D/CDK-like complex. Development 126, 4849–4860 (1999).
Boxem, M. & van den Heuvel, S. lin-35 Rb and cki-1 Cip/Kip cooperate in developmental regulation of G1 progression in C. elegans. Development 128, 4349–4359 (2001). Shows that the C. elegans Rb homologue inhibits cell-cycle progression and that loss of CKI-1 and Rb can suppress the G1-phase arrest of cyd-1 or cdk-4 mutants.
Yanowitz, J. & Fire, A. Cyclin D involvement demarcates a late transition in C. elegans embryogenesis. Dev. Biol. 279, 244–251 (2005).
van den Heuvel, S. The C. elegans cell cycle: overview of molecules and mechanisms. Methods Mol. Biol. 296, 51–67 (2005).
Raff, J. W. & Glover, D. M. Nuclear and cytoplasmic mitotic cycles continue in Drosophila embryos in which DNA synthesis is inhibited with aphidicolin. J. Cell Biol. 107, 2009–2019 (1988).
Kimelman, D., Kirschner, M. & Scherson, T. The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48, 399–407 (1987).
Encalada, S. E. et al. DNA replication defects delay cell division and disrupt cell polarity in early Caenorhabditis elegans embryos. Dev. Biol. 228, 225–238 (2000).
Gonczy, P. et al. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408, 331–336 (2000).
Zhong, W., Feng, H., Santiago, F. E. & Kipreos, E. T. CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 423, 885–889 (2003). Shows that the CUL-4 ubiquitin ligase prevents re-replication of genomic DNA by promoting the degradation of the replication licensing factor CDT-1.
Brauchle, M., Baumer, K. & Gonczy, P. Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos. Curr. Biol. 13, 819–827 (2003).
Sulston, J. E. & Horvitz, H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110–156 (1977). A landmark paper that describes the larval cell lineages of both hermaphrodites and males.
Kimble, J. & Hirsh, D. The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev. Biol. 70, 396–417 (1979). A landmark paper that provides the lineage of the somatic gonad, the one class of tissue that was not included in the analysis in reference 14.
Knight, C. G., Patel, M. N., Azevedo, R. B. & Leroi, A. M. A novel mode of ecdysozoan growth in Caenorhabditis elegans. Evol. Dev. 4, 16–27 (2002).
Euling, S. & Ambros, V. Heterochronic genes control cell cycle progress and developmental competence of C. elegans vulva precursor cells. Cell 84, 667–676 (1996).
Hedgecock, E. M. & White, J. G. Polyploid tissues in the nematode Caenorhabditis elegans. Dev. Biol. 107, 128–133 (1985).
Blow, J. J. & Hodgson, B. Replication licensing — defining the proliferative state? Trends Cell Biol. 12, 72–78 (2002).
Blagosklonny, M. V. & Pardee, A. B. The restriction point of the cell cycle. Cell Cycle 1, 103–110 (2002).
Pasquinelli, A. E. & Ruvkun, G. Control of developmental timing by microRNAs and their targets. Annu. Rev. Cell Dev. Biol. 18, 495–513 (2002).
Ambros, V. & Horvitz, H. R. Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416 (1984).
Riddle, D. L. in The Nematode Caenorhabditis Elegans (ed. Wood, W. B.) 393–412 (Cold Spring Harbor Laboratory Press, New York, 1988).
Hong, Y., Roy, R. & Ambros, V. Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125, 3585–3597 (1998). Shows that CKI-1 regulates cell-cycle exit and entry during larval stages.
Morgan, D. O. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261 (1997).
Liu, J. & Kipreos, E. T. Evolution of cyclin-dependent kinases (CDKs) and CDK-activating kinases (CAKs): differential conservation of CAKs in yeast and metazoa. Mol. Biol. Evol. 17, 1061–1074 (2000).
Boxem, M., Srinivasan, D. G. & van den Heuvel, S. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126, 2227–2239 (1999).
Richardson, H. E., Wittenberg, C., Cross, F. & Reed, S. I. An essential G1 function for cyclin-like proteins in yeast. Cell 59, 1127–1133 (1989).
Knoblich, J. A. et al. Cyclin E controls S phase progression and its downregulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77, 107–120 (1994).
Meyer, C. A. et al. Drosophila Cdk4 is required for normal growth and is dispensable for cell cycle progression. EMBO J. 19, 4533–4542 (2000).
Emmerich, J., Meyer, C. A., de la Cruz, A. F., Edgar, B. A. & Lehner, C. F. Cyclin D does not provide essential Cdk4-independent functions in Drosophila. Genetics 168, 867–875 (2004).
Sherr, C. J. & Roberts, J. M. Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18, 2699–2711 (2004).
Fay, D. S. & Han, M. Mutations in cye-1, a Caenorhabditis elegans cyclin E homolog, reveal coordination between cell-cycle control and vulval development. Development 127, 4049–4060 (2000).
Frolov, M. V. & Dyson, N. J. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 117, 2173–2181 (2004).
Lu, X. & Horvitz, H. R. lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95, 981–991 (1998).
Myers, T. R. & Greenwald, I. lin-35 Rb acts in the major hypodermis to oppose Ras-mediated vulval induction in C. elegans. Dev. Cell 8, 117–123 (2005).
Ceol, C. J. & Horvitz, H. R. dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signalling in C. elegans vulval development. Mol. Cell 7, 461–473 (2001).
Boxem, M. & van den Heuvel, S. C. elegans class B synthetic multivulva genes act in G1 regulation. Curr. Biol. 12, 906–911 (2002). Discusses the contributions of E2F and DP homologues to S-phase entry, as well as the identification of new G1-to-S-phase cell-cycle regulators.
Brodigan, T. M., Liu, J., Park, M., Kipreos, E. T. & Krause, M. Cyclin E expression during development in Caenorhabditis elegans. Dev. Biol. 254, 102–115 (2003).
Petroski, M. D. & Deshaies, R. J. Function and regulation of cullin-RING ubiquitin ligases. Nature Rev. Mol. Cell Biol. 6, 9–20 (2005).
Fukuyama, M., Gendreau, S. B., Derry, W. B. & Rothman, J. H. Essential embryonic roles of the CKI-1 cyclin-dependent kinase inhibitor in cell-cycle exit and morphogenesis in C. elegans. Dev. Biol. 260, 273–286 (2003).
Feng, H. et al. CUL-2 is required for the G1-to-S-phase transition and mitotic chromosome condensation in Caenorhabditis elegans. Nature Cell Biol. 1, 486–492 (1999).
Saito, R. M., Perreault, A., Peach, B., Satterlee, J. S. & van den Heuvel, S. The CDC-14 phosphatase controls developmental cell-cycle arrest in C. elegans. Nature Cell Biol. 6, 777–783 (2004).
Coqueret, O. New roles for p21 and p27 cell-cycle inhibitors: a function for each cell compartment? Trends Cell Biol. 13, 65–70 (2003).
Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W. & Hedgecock, E. M. cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829–839 (1996).
Kipreos, E. T., Gohel, S. P. & Hedgecock, E. M. The C. elegans F-box/WD-repeat protein LIN-23 functions to limit cell division during development. Development 127, 5071–5082 (2000).
Nayak, S. et al. The Caenorhabditis elegans Skp1-related gene family: diverse functions in cell proliferation, morphogenesis, and meiosis. Curr. Biol. 12, 277–287 (2002).
Yamanaka, A. et al. Multiple Skp1-related proteins in Caenorhabditis elegans: diverse patterns of interaction with Cullins and F-box proteins. Curr. Biol. 12, 267–275 (2002).
Ambros, V. The temporal control of cell cycle and cell fate in Caenorhabditis elegans. Novartis Found. Symp. 237, 203–214; discussion 214–220 (2001).
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).
Fay, D. S., Keenan, S. & Han, M. fzr-1 and lin-35/Rb function redundantly to control cell proliferation in C. elegans as revealed by a nonbiased synthetic screen. Genes Dev. 16, 503–517 (2002).
Harper, J. W., Burton, J. L. & Solomon, M. J. The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16, 2179–2206 (2002).
White, J. in The Nematode Caenorhabditis Elegans (ed. Wood, W. B.) 81–122 (Cold Spring Harbor Laboratory Press, New York, 1988).
Flemming, A. J., Shen, Z. Z., Cunha, A., Emmons, S. W. & Leroi, A. M. Somatic polyploidization and cellular proliferation drive body size evolution in nematodes. Proc. Natl Acad. Sci. USA 97, 5285–5290 (2000).
Nystrom, J. et al. Increased or decreased levels of Caenorhabditis elegans lon-3, a gene encoding a collagen, cause reciprocal changes in body length. Genetics 161, 83–97 (2002).
Morita, K. et al. A Caenorhabditis elegans TGF-β, DBL-1, controls the expression of LON-1, a PR-related protein, that regulates polyploidization and body length. EMBO J. 21, 1063–1073 (2002).
Kostic, I., Li, S. & Roy, R. cki-1 links cell division and cell fate acquisition in the C. elegans somatic gonad. Dev. Biol. 263, 242–252 (2003).
Lorson, M. A., Horvitz, H. R. & van den Heuvel, S. LIN-5 is a novel component of the spindle apparatus required for chromosome segregation and cleavage plane specification in Caenorhabditis elegans. J. Cell Biol. 148, 73–86 (2000).
Nguyen, T. Q., Sawa, H., Okano, H. & White, J. G. The C. elegans septin genes, unc-59 and unc-61, are required for normal postembryonic cytokineses and morphogenesis but have no essential function in embryogenesis. J. Cell Sci. 113, 3825–3837 (2000).
Albertson, D. G., Sulston, J. E. & White, J. G. Cell cycling and DNA replication in a mutant blocked in cell division in the nematode Caenorhabditis elegans. Dev. Biol. 63, 165–178 (1978).
White, J. G., Horvitz, H. R. & Sulston, J. E. Neuron differentiation in cell lineage mutants of Caenorhabditis elegans. Nature 297, 584–587 (1982).
Sundaram, M. V. Vulval development: the battle between Ras and Notch. Curr. Biol. 14, R311–R313 (2004).
Chen, N. & Greenwald, I. The lateral signal for LIN-12/Notch in C. elegans vulval development comprises redundant secreted and transmembrane DSL proteins. Dev. Cell 6, 183–192 (2004).
Ambros, V. Cell cycle-dependent sequencing of cell fate decisions in Caenorhabditis elegans vulva precursor cells. Development 126, 1947–1956 (1999).
Seydoux, G. & Schedl, T. The germline in C. elegans: origins, proliferation, and silencing. Int. Rev. Cytol. 203, 139–185 (2001).
Hall, D. H. et al. Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 212, 101–123 (1999).
Kimble, J. E. & White, J. G. On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81, 208–219 (1981).
Nurse, P. Ordering S phase and M phase in the cell cycle. Cell 79, 547–550 (1994).
Austin, J. & Kimble, J. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis. Cell 51, 589–599 (1987).
Lambie, E. J. & Kimble, J. Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 112, 231–240 (1991).
Berry, L. W., Westlund, B. & Schedl, T. Germ-line tumour formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development 124, 925–936 (1997).
Pepper, A. S., Killian, D. J. & Hubbard, E. J. Genetic analysis of Caenorhabditis elegans glp-1 mutants suggests receptor interaction or competition. Genetics 163, 115–132 (2003).
Petcherski, A. G. & Kimble, J. LAG-3 is a putative transcriptional activator in the C. elegans Notch pathway. Nature 405, 364–368 (2000).
Francis, R., Maine, E. & Schedl, T. Analysis of the multiple roles of gld-1 in germline development: interactions with the sex determination cascade and the glp-1 signalling pathway. Genetics 139, 607–630 (1995).
Jones, A. R. & Schedl, T. Mutations in gld-1, a female germ cell-specific tumour suppressor gene in Caenorhabditis elegans, affect a conserved domain also found in Src-associated protein Sam68. Genes Dev. 9, 1491–1504 (1995).
Jan, E., Motzny, C. K., Graves, L. E. & Goodwin, E. B. The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J. 18, 258–269 (1999).
Wang, L., Eckmann, C. R., Kadyk, L. C., Wickens, M. & Kimble, J. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419, 312–316 (2002).
Eckmann, C. R., Kraemer, B., Wickens, M. & Kimble, J. GLD-3, a bicaudal-C homologue that inhibits FBF to control germline sex determination in C. elegans. Dev. Cell 3, 697–710 (2002).
Eckmann, C. R., Crittenden, S. L., Suh, N. & Kimble, J. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168, 147–160 (2004).
Kadyk, L. C. & Kimble, J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125, 1803–1813 (1998).
Crittenden, S. L. et al. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417, 660–663 (2002).
Hansen, D., Wilson-Berry, L., Dang, T. & Schedl, T. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131, 93–104 (2004). References 79, 81 and 82 provide important insights into meiotic entry by describing pathways that regulate GLD-1 and GLD-2–GLD-3 in the germ line.
Lamont, L. B., Crittenden, S. L., Bernstein, D., Wickens, M. & Kimble, J. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev. Cell 7, 697–707 (2004). Shows that the interplay between FBF-1 and FBF-2 regulates the size of the germ stem-cell niche.
Wickens, M., Bernstein, D. S., Kimble, J. & Parker, R. A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet. 18, 150–157 (2002).
Deng, W. & Lin, H. Asymmetric germ cell division and oocyte determination during Drosophila oogenesis. Int. Rev. Cytol. 203, 93–138 (2001).
McCarter, J., Bartlett, B., Dang, T. & Schedl, T. Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev. Biol. 181, 121–143 (1997).
Killian, D. J. & Hubbard, E. J. Caenorhabditis elegans germline patterning requires coordinated development of the somatic gonadal sheath and the germ line. Dev. Biol. 279, 322–335 (2005).
Lamitina, S. T. & L'Hernault, S. W. Dominant mutations in the Caenorhabditis elegans Myt1 ortholog wee-1.3 reveal a novel domain that controls M-phase entry during spermatogenesis. Development 129, 5009–5018 (2002).
Ashcroft, N. & Golden, A. CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33, 1–7 (2002).
Subramaniam, K. & Seydoux, G. nos-1 and nos-2, two genes related to Drosophila nanos, regulate primordial germ cell development and survival in Caenorhabditis elegans. Development 126, 4861–4871 (1999).
Hansen, D., Hubbard, E. J. & Schedl, T. Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 268, 342–357 (2004).
I thank T. Schedl, D. Hansen, J. Gaertig and members of the Kipreos laboratory for critical reading of the manuscript, and B. Goldstein for the use of movie frames of a moving adult Caenorhabditis elegans that were used to create the image in Figure 1. Research in the Kipreos laboratory is supported by grants from the National Institutes of Health and the American Cancer Society.
The author declares no competing financial interests.
- DNA-REPLICATION CHECKPOINT
This cell-cycle checkpoint ensures that mitosis is not initiated when DNA replication is either blocked or ongoing.
- BLAST CELL
A cell that has not undergone terminal differentiation and that divides to produce cells of a committed cell lineage.
A common (shared) cytoplasm containing more than one nucleus.
- G0 PHASE
A 'resting' (quiescent) cell-cycle stage, in which a cell does not progress through the cell cycle. Cells enter G0 phase from G1 phase, and after receiving the proper stimulus they can return to G1 phase and continue cell-cycle progression.
- HETEROCHRONIC GENE
A gene that regulates the timing of developmental events. Mutations in heterochronic genes affect the timing of developmental programmes without overtly altering the programmes themselves.
- FOUNDER CELL
A C. elegans early embryonic blast cell, the descendants of which divide relatively synchronously and produce a defined subset of tissue types.
- CYCLIN-DEPENDENT KINASE
(CDK). A protein kinase that requires an associated cyclin protein for activity. Various CDK–cyclin complexes regulate different stages of the cell cycle or of the RNA polymerase II transcription cycle.
Genes in different species that have arisen directly from a single ancestral gene in the last common ancestor of the species. Orthologous genes often have similar cellular functions.
- SYNTHETIC MULTIVULVA (SYNMUV) PHENOTYPE
A mutant phenotype in which hermaphrodites have multiple vulvae that arises from combining class A mutant synMuv alleles with class B mutant synMuv alleles. Mutants of a single class do not have the multivulva phenotype.
- SCF UBIQUITIN LIGASE
A multi-subunit ubiquitin ligase (E3) that includes a cullin, CUL1 (for metazoa) or Cdc53 (for budding yeast), which is a scaffold for the complex; a RING-finger protein Rbx1/Roc1/Hrt1, which binds to the ubiquitin-conjugating enzyme (E2); an adaptor protein Skp1; and an F-box protein, which is the substrate-binding component that positions the substrate for ubiquitylation by E2.
- CIP/KIP FAMILY
(CDK-inhibitory protein/kinase-inhibitory protein). A family of CDK inhibitors that includes the mammalian p21Cip1, p27Kip1 and p57Kip2, and D. melanogaster Dacapo.
- ANAPHASE PROMOTING COMPLEX/CYCLOSOME
(APC/C). A multi-subunit E3 ubiquitin ligase that has an important role in the transition into anaphase, as well as the exit from mitosis and the maintenance of the G1 state.
- SEAM CELL
A hypodermal blast cell that produces lateral cuticular ridges (alae) during the L1 larval and adult stages. Seam cells divide during the larval stages to produce more seam cells, hyp7 cells — the main hypodermal (skin) cell for the body — and neurons (in a subset of seam cell lineages).
About this article
Cite this article
Kipreos, E. C. elegans cell cycles: invariance and stem cell divisions. Nat Rev Mol Cell Biol 6, 766–776 (2005). https://doi.org/10.1038/nrm1738
Antifungal Metabolite p-Aminobenzoic Acid (pABA): Mechanism of Action and Efficacy for the Biocontrol of Pear Bitter Rot Disease
Journal of Agricultural and Food Chemistry (2019)
Embryo timelapses can be compiled and quantified to understand canonical histone dynamics across multiple cell cycles
A simple answer to complex questions: Caenorhabditis elegans as an experimental model for examining the DNA damage response and disease genes
Journal of Cellular Physiology (2018)
Journal of Cell Science (2018)