Developmental robustness in the Caenorhabditis elegans embryo

Molecular Reproduction and Development

Volumn 82, Issue 12, 2015, Pages 918-931

  Maduro, Morris F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL SPECIFICITY; CONCEPTUAL FRAMEWORK; DEVELOPMENTAL GENE; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; ENDODERM; GENE DUPLICATION; GENE REGULATORY NETWORK; GENETIC BACKGROUND; GENETIC REGULATION; INTESTINE; MOLECULAR EVOLUTION; MUTANT; NONHUMAN; ORGANOGENESIS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; STEM CELL; ANIMAL; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; NONMAMMALIAN EMBRYO; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENOME-WIDE ASSOCIATION STUDY;

EID: 84983094869     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22582     Document Type: Article

References (89)

1. Bao Z, Murray JI, Boyle T, Ooi SL, Sandel MJ, Waterston RH. 2006. Automated cell lineage tracing in Caenorhabditis elegans. Pro Nat Acad Sci USA 103:2707-2712.
2. Baugh LR, Wen JC, Hill AA, Slonim DK, Brown EL, Hunter CP. 2005. Synthetic lethal analysis of Caenorhabditis elegans posterior embryonic patterning genes identifies conserved genetic interactions. Genome Biol 6:R45.
3. Bei Y, Hogan J, Berkowitz LA, Soto M, Rocheleau CE, Pang KM, Collins J, Mello CC. 2002. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev Cell 3:113-125.
4. Blackwell TK, Bowerman B, Priess JR, Weintraub H. 1994. Formation of a monomeric DNA binding domain by Skn-1 bZIP and homeodomain elements. Science 266:621-628.
5. Boeck ME, Boyle T, Bao Z, Murray J, Mericle B, Waterston R. 2011. Specific roles for the GATA transcription factors end-1 and end-3 during C. elegans E-lineage development. Dev Biol 358:345-355.
6. Bowerman B. 1998. Maternal control of pattern formation in early Caenorhabditis elegans embryos. Curr Top Dev Biol 39:73-117.
7. Bowerman B, Draper BW, Mello CC, Priess JR. 1993. The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74:443-452.
8. Bowerman B, Eaton BA, Priess JR. 1992. Skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68:1061-1075.
9. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
10. Broitman-Maduro G, Maduro MF, Rothman JH. 2005. The noncanonical binding site of the MED-1 GATA factor defines differentially regulated target genes in the C. elegans mesendoderm. Dev Cell 8:427-433.
11. Broitman-Maduro G, Owraghi M, Hung W, Kuntz S, Sternberg PW, Maduro M. 2009. The NK-2 class homeodomain factor CEH-51 and the T-box factor TBX-35 have overlapping function in C. elegans mesoderm development. Development 176:2735-2746.
12. Burga A, Casanueva MO, Lehner B. 2011. Predicting mutation outcome from early stochastic variation in genetic interaction partners. Nature 480:250-253.
13. Burke SL, Hammell M, Ambros V. 2015. Robust distal tip cell pathfinding in the face of temperature stress is ensured by two conserved microRNAS in caenorhabditis elegans. Genetics 200:1201-1218.
14. Chalancon G, Ravarani CN, Balaji S, Martinez-Arias A, Aravind L, Jothi R, Babu MM. 2012. Interplay between gene expression noise and regulatory network architecture. Trends Genet: TIG 28:221-232.
15. Clucas C, Cabello J, Bussing I, Schnabel R, Johnstone IL. 2002. Oncogenic potential of a C. elegans cdc25 gene is demonstrated by a gain-of-function allele. EMBO J 21:665-674.
16. Coroian C, Broitman-Maduro G, Maduro MF. 2005. Med-type GATA factors and the evolution of mesendoderm specification in nematodes. Dev Biol 289:444-455.
17. Cutter AD. 2008. Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. Mol Biol Evol 25:778-786.
18. Davidson EH. 2010. Emerging properties of animal gene regulatory networks. Nature 468:911-920.
19. Ellis RE, Lin SY. 2014. The evolutionary origins and consequences of self-fertility in nematodes. F1000 Prime Rep 6:62.
20. Felix MA, Barkoulas M. 2012. Robustness and flexibility in nematode vulva development. Trends Genet: TIG 28:185-195.
21. Felix MA, Wagner A. 2008. Robustness and evolution: Concepts, insights and challenges from a developmental model system. Heredity 100:132-140.
22. Francesconi M, Lehner B. 2014. The effects of genetic variation on gene expression dynamics during development. Nature 505:208-211.
23. Fukushige T, Brodigan TM, Schriefer LA, Waterston RH, Krause M. 2006. Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: Evidence for a unified theory of animal muscle development. Genes Dev 20:3395-3406.
24. Fukushige T, Goszczynski B, Tian H, McGhee JD. 2003. The evolutionary duplication and probable demise of an endodermal GATA factor in Caenorhabditis elegans. Genetics 165:575-588.
25. Fukushige T, Hawkins MG, McGhee JD. 1998. The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev Biol 198:286-302.
26. Fukushige T, Hendzel MJ, Bazett-Jones DP, McGhee JD. 1999. Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc Nat Acad Sci USA 96:11883-11888.
27. Good K, Ciosk R, Nance J, Neves A, Hill RJ, Priess JR. 2004. The T-box transcription factors TBX-37 and TBX-38 link GLP-1/Notch signaling to mesoderm induction in C. elegans embryos. Development 131:1967-1978.
28. Goszczynski B, McGhee JD. 2005. Re-evaluation of the role of the med-1 and med-2 genes in specifying the C. elegans endoderm. Genetics 171:545-555.
29. Gursky VV, Surkova SY, Samsonova MG. 2012. Mechanisms of developmental robustness. Bio Syst. Biosystems 109:329-335.
30. Hashimshony T, Wagner F, Sher N, Yanai I. 2012. CEL-Seq: Single-cell RNA-Seq by multiplexed linear amplification. Cell Rep 2:666-673.
31. Hawkins MG, McGhee JD. 1995. Elt-2, a second GATA factor from the nematode Caenorhabditis elegans. J Biol Chem 270:14666-14671.
32. Hebeisen M, Roy R. 2008. CDC-25.1 stability is regulated by distinct domains to restrict cell division during embryogenesis in C. elegans. Development 135:1259-1269.
33. Hunter CP, Kenyon C. 1996. Spatial and temporal controls target pal-1 blastomere-specification activity to a single blastomere lineage in C. elegans embryos. Cell 87:217-226.
34. Kellogg DR. 2003. Wee1-dependent mechanisms required for coordination of cell growth and cell division. J Cell Sci 116:4883-4890.
35. Kiontke KC, Felix MA, Ailion M, Rockman MV, Braendle C, Penigault JB, Fitch DH. 2011. A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol 11:339.
36. Kostic I, Roy R. 2002. Organ-specific cell division abnormalities caused by mutation in a general cell cycle regulator in C. elegans. Development 129:2155-2165.
37. Ladewig J, Koch P, Brustle O. 2013. Leveling Waddington: the emergence of direct programming and the loss of cell fate hierarchies. Nat Rev Mol Cell Biol 14:225-236.
38. Lee JH, Lee JB, Shapovalova Z, Fiebig-Comyn A, Mitchell RR, Laronde S, Szabo E, Benoit YD, Bhatia M. 2014. Somatic transcriptome priming gates lineage-specific differentiation potential of human-induced pluripotent stem cell states. Nat Commun 5:5605.
39. Leung B, Hermann GJ, Priess JR. 1999. Organogenesis of the Caenorhabditis elegans intestine. Dev Biol 216:114-134.
40. Lin KT, Broitman-Maduro G, Hung WW, Cervantes S, Maduro MF. 2009. Knockdown of SKN-1 and the Wnt effector TCF/POP-1 reveals differences in endomesoderm specification in C. briggsae as compared with C. elegans. Dev Biol 325:296-306.
41. Lin R, Hill RJ, Priess JR. 1998. POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 92:229-239.
42. Lin R, Thompson S, Priess JR. 1995. Pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 83:599-609.
43. Macneil LT, Walhout AJ. 2011. Gene regulatory networks and the role of robustness and stochasticity in the control of gene expression. Genome Res 21:645-657.
44. Maduro M, Hill RJ, Heid PJ, Newman-Smith ED, Zhu J, Priess J, Rothman J. 2005a. Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev Biol 284:509-522.
45. Maduro MF. 2006. Endomesoderm specification in Caenorhabditis elegans and other nematodes. Bioessays 28:1010-1022.
46. Maduro MF. 2009. Structure and evolution of the C. elegans embryonic endomesoderm network. Biochimica et Biophysica Acta 1789:250-260.
47. Maduro MF, Broitman-Maduro G, Choi H, Carranza F, Chia-Yi Wu A, Rifkin SA. 2015. MED GATA factors promote robust development of the C. elegans endoderm. Dev Biol 404:66-79.
48. Maduro MF, Broitman-Maduro G, Mengarelli I, Rothman JH. 2007. Maternal deployment of the embryonic SKN-1->MED-1, 2 cell specification pathway in C. elegans. Dev Biol 301:590-601.
49. Maduro MF, Kasmir JJ, Zhu J, Rothman JH. 2005b. The Wnt effector POP-1 and the PAL-1/Caudal homeoprotein collaborate with SKN-1 to activate C. elegans endoderm development. Dev Biol 285:510-523.
50. Maduro MF, Lin R, Rothman JH. 2002. Dynamics of a developmental switch: Recursive intracellular and intranuclear redistribution of Caenorhabditis elegans POP-1 parallels Wnt-inhibited transcriptional repression. Dev Biol 248:128-142.
51. Maduro MF, Meneghini MD, Bowerman B, Broitman-Maduro G, Rothman JH. 2001. Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3beta homolog is mediated by MED-1 and -2 in C. elegans. Mol Cell 7:475-485.
52. Maduro MF, Rothman JH. 2002. Making worm guts: The gene regulatory network of the Caenorhabditis elegans endoderm. Deve Biol 246:68-85.
53. Maeda YT, Sano M. 2006. Regulatory dynamics of synthetic gene networks with positive feedback. J Mol Biol 359:1107-1124.
54. McGhee JD, Fukushige T, Krause MW, Minnema SE, Goszczynski B, Gaudet J, Kohara Y, Bossinger O, Zhao Y, Khattra J, Hirst M, Jones SJ, Marra MA, Ruzanov P, Warner A, Zapf R, Moerman DG, Kalb JM. 2009. ELT-2 is the predominant transcription factor controlling differentiation and function of the C. elegans intestine, from embryo to adult. Dev Biol 327:551-565.
55. McGhee JD, Sleumer MC, Bilenky M, Wong K, McKay SJ, Goszczynski B, Tian H, Krich ND, Khattra J, Holt RA, Baillie DL, Kohara Y, Marra MA, Jones SJ, Moerman DG, Robertson AG. 2007. The ELT-2 GATA-factor and the global regulation of transcription in the C. elegans intestine. Deve Biol 302:627-645.
56. Mendenhall AR, Tedesco PM, Sands B, Johnson TE, Brent R. 2015. Single cell quantification of reporter gene expression in live adult Caenorhabditis elegans reveals reproducible cell-specific expression patterns and underlying biological variation. PLoS ONE 10:e0124289.
57. Murray JI, Bao Z, Boyle TJ, Boeck ME, Mericle BL, Nicholas TJ, Zhao Z, Sandel MJ, Waterston RH. 2008. Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nat Methods 5:703-709.
58. Neves A, Busso C, Gonczy P. 2015. Cellular hallmarks reveal restricted aerobic metabolism at thermal limits. eLife 4:e04810.
59. Olson SK, Greenan G, Desai A, Muller-Reichert T, Oegema K. 2012. Hierarchical assembly of the eggshell and permeability barrier in C. elegans. J Cell Biol 198:731-748.
60. Owraghi M, Broitman-Maduro G, Luu T, Roberson H, Maduro MF. 2010. Roles of the Wnt effector POP-1/TCF in the C. elegans endomesoderm specification gene network. Dev Biol 340:209-221.
61. Palgunow D, Klapper M, Doring F. 2012. Dietary restriction during development enlarges intestinal and hypodermal lipid droplets in Caenorhabditis elegans. PLoS ONE 7:e46198.
62. Pauli F, Liu Y, Kim YA, Chen PJ, Kim SK. 2006. Chromosomal clustering and GATA transcriptional regulation of intestine-expressed genes in C. elegans. Development 133:287-295.
63. Phillips BT, Kidd AR, King 3rd, Hardin R, Kimble J. 2007. Reciprocal asymmetry of SYS-1/beta-catenin and POP-1/TCF controls asymmetric divisions in Caenorhabditis elegans. Proc Nat Acad Sci USA 104:3231-3236.
64. Prasad A, Croydon-Sugarman MJ, Murray RL, Cutter AD. 2011. Temperature-dependent fecundity associates with latitude in Caenorhabditis briggsae. Evol Int J Org Evol 65:52-63.
65. Priess JR, Thomson JN. 1987. Cellular interactions in early C. elegans embryos. Cell 48:241-250.
66. Raj A, Rifkin SA, Andersen E, van Oudenaarden A. 2010. Variability in gene expression underlies incomplete penetrance. Nature 463:913-918.
67. Robertson SM, Medina J, Lin R. 2014. Uncoupling different characteristics of the C. elegans E lineage from differentiation of intestinal markers. PLoS ONE 9:e106309.
68. Robertson SM, Shetty P, Lin R. 2004. Identification of lineage-specific zygotic transcripts in early Caenorhabditis elegans embryos. Dev Biol 276:493-507.
69. Rocheleau CE, Downs WD, Lin R, Wittmann C, Bei Y, Cha YH, Ali M, Priess JR, Mello CC. 1997. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90:707-716.
70. Rocheleau CE, Yasuda J, Shin TH, Lin R, Sawa H, Okano H, Priess JR, Davis RJ, Mello CC. 1999. WRM-1 activates the LIT-1 protein kinase to transduce anterior/posterior polarity signals in C. elegans. Cell 97:717-726.
71. Schmiedel JM, Klemm SL, Zheng Y, Sahay A, Bluthgen N, Marks DS, van Oudenaarden A. 2015. Gene expression. MicroRNA control of protein expression noise. Science 348:128-132.
72. Schnabel R, Hutter H, Moerman D, Schnabel H. 1997. Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: Variability of development and regional specification. Dev Biol 184:234-265.
73. Segref A, Cabello J, Clucas C, Schnabel R, Johnstone IL. 2010. Fate specification and tissue-specific cell cycle control of the Caenorhabditis elegans intestine. Mol Biol Cell 21:725-738.
74. Shetty P, Lo MC, Robertson SM, Lin R. 2005. C. elegans TCF protein, POP-1, converts from repressor to activator as a result of Wnt-induced lowering of nuclear levels. Dev Biol 285:584-592.
75. Sommermann EM, Strohmaier KR, Maduro MF, Rothman JH. 2010. Endoderm development in Caenorhabditis elegans: The synergistic action of ELT-2 and -7 mediates the specification->differentiation transition. Dev Biol 347:154-166.
76. Staller MV, Fowlkes CC, Bragdon MD, Wunderlich Z, Estrada J, DePace AH. 2015. A gene expression atlas of a bicoid-depleted Drosophila embryo reveals early canalization of cell fate. Development 142:587-596.
77. Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D'Eustachio P, Fitch DH, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, Stajich JE, Wei C, Willey D, Wilson RK, Durbin R, Waterston RH. 2003. The genome sequence of Caenorhabditis briggsae: A platform for comparative genomics. PLoS Biol 1:E45.
78. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110-156.
79. Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64-119.
80. Tanenbaum ME, Gilbert LA, Qi LS, Weissman JS, Vale RD. 2014. A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159:635-646.
81. Thorpe CJ, Schlesinger A, Carter JC, Bowerman B. 1997. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90:695-705.
82. True JR, Haag ES. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3:109-119.
83. Vu V, Verster AJ, Schertzberg M, Chuluunbaatar T, Spensley M, Pajkic D, Hart GT, Moffat J, Fraser AG. 2015. Natural variation in gene expression modulates the severity of mutant phenotypes. Cell 162:391-402.
84. Waaijers S, Boxem M. 2014. Engineering the Caenorhabditis elegans genome with CRISPR/Cas9. Methods 68:381-388.
85. Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
86. Walton T, Preston E, Nair G, Zacharias AL, Raj A, Murray JI. 2015. The Bicoid class homeodomain factors ceh-36/OTX and unc-30/PITX cooperate in C. elegans embryonic progenitor cells to regulate robust development. PLoS Genet 11:e1005003.
87. Wilson MA, Hoch RV, Ashcroft NR, Kosinski ME, Golden A. 1999. A Caenorhabditis elegans wee1 homolog is expressed in a temporally and spatially restricted pattern during embryonic development. Biochimica et Biophysica Acta 1445:99-109.
88. Zhao Z, Boyle TJ, Bao Z, Murray JI, Mericle B, Waterston RH. 2008. Comparative analysis of embryonic cell lineage between Caenorhabditis briggsae and Caenorhabditis elegans. Dev Biol 314:93-99.
89. Zhu J, Hill RJ, Heid PJ, Fukuyama M, Sugimoto A, Priess JR, Rothman JH. 1997. End-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev 11:2883-2896.