Determinative Developmental Cell Lineages Are Robust to Cell Deaths
It is widely believed that development plays an important role in the phenotypic robustness of organisms to environmental and genetic perturbations. But, the developmental process and cell fate are largely predetermined and fixed in some species, including for example mollusks, annelids, tunicates, and nematodes. How these organisms deal with perturbations that cause cell deaths in ontogenesis has been a long-standing puzzle. We propose and demonstrate that the developmental cell lineages of these species are structured such that the resulting cellular compositions of the organisms are only moderately affected by cell deaths. A series of highly nonrandom features of the cell lineages underlie their developmental robustness and these features likely originated as adaptations in the face of various disturbances during development. Our findings reveal important organizing principles of determinative developmental cell lineages and a conceptually new mechanism of phenotypic robustness, which have broad implications for development and evolution.
Vyšlo v časopise:
Determinative Developmental Cell Lineages Are Robust to Cell Deaths. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004501
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004501
Souhrn
It is widely believed that development plays an important role in the phenotypic robustness of organisms to environmental and genetic perturbations. But, the developmental process and cell fate are largely predetermined and fixed in some species, including for example mollusks, annelids, tunicates, and nematodes. How these organisms deal with perturbations that cause cell deaths in ontogenesis has been a long-standing puzzle. We propose and demonstrate that the developmental cell lineages of these species are structured such that the resulting cellular compositions of the organisms are only moderately affected by cell deaths. A series of highly nonrandom features of the cell lineages underlie their developmental robustness and these features likely originated as adaptations in the face of various disturbances during development. Our findings reveal important organizing principles of determinative developmental cell lineages and a conceptually new mechanism of phenotypic robustness, which have broad implications for development and evolution.
Zdroje
1. WaddingtonCH (1942) Canalization of development and the inheritance of acquired characters. Nature 150: 563–565.
2. MaselJ, SiegalML (2009) Robustness: mechanisms and consequences. Trends Genet 25: 395–403.
3. FlattT (2005) The evolutionary genetics of canalization. Q Rev Biol 80: 287–316.
4. ScharlooW (1991) Canalization: genetic and developmental aspects. Annu Rev Ecol Syst 22: 65–93.
5. Wagner A (2005) Robustness and Evolvability in Living Systems. Princeton, NJ: Princeton University Press.
6. Alon U (2007) An Introduction to Systems Biology: Design Principles of Biological Circuits London: Chapman & Hall.
7. HoWC, ZhangJ (2014) The genotype-phenotype map of yeast complex traits: basic parameters and the role of natural selection. Mol Biol Evol 31(6): 1568–80.
8. DraghiJA, ParsonsTL, WagnerGP, PlotkinJB (2010) Mutational robustness can facilitate adaptation. Nature 463: 353–355.
9. LevySF, SiegalML (2008) Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol 6: e264.
10. RutherfordSL, LindquistS (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336–342.
11. Zhang J (2012) Genetic redundancies and their evolutionary maintenance. In: Soyer O, editor. Evolutionary Systems Biology. New York, NY: Springer.
12. WangZ, ZhangJ (2009) Abundant indispensable redundancies in cellular metabolic networks. Genome Biol Evol 1: 23–33.
13. NowakMA, BoerlijstMC, CookeJ, SmithJM (1997) Evolution of genetic redundancy. Nature 388: 167–171.
14. QianW, LiaoBY, ChangAY, ZhangJ (2010) Maintenance of duplicate genes and their functional redundancy by reduced expression. Trends Genet 26: 425–430.
15. VavouriT, SempleJI, LehnerB (2008) Widespread conservation of genetic redundancy during a billion years of eukaryotic evolution. Trends Genet 24: 485–488.
16. SiegalML, BergmanA (2002) Waddington's canalization revisited: developmental stability and evolution. Proc Natl Acad Sci U S A 99: 10528–10532.
17. HornsteinE, ShomronN (2006) Canalization of development by microRNAs. Nat Genet 38 Suppl: S20–24.
18. WuCI, ShenY, TangT (2009) Evolution under canalization and the dual roles of microRNAs: a hypothesis. Genome Res 19: 734–743.
19. PrillRJ, IglesiasPA, LevchenkoA (2005) Dynamic properties of network motifs contribute to biological network organization. PLoS Biol 3: e343.
20. Gilbert SF (2000) Developmental Biology. Sunderland, Mass.: Sinauer Associates.
21. DictusWJ, DamenP (1997) Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (mollusca). Mech Dev 62: 213–226.
22. LambertJD (2010) Developmental patterns in spiralian embryos. Curr Biol 20: R72–77.
23. NodaT, HamadaM, HamaguchiM, FujieM, SatohN (2009) Early zygotic expression of transcription factors and signal molecules in fully dissociated embryonic cells of Ciona intestinalis: A microarray analysis. Dev Growth Differ 51: 639–655.
24. HouthoofdW, JacobsenK, MertensC, VangestelS, CoomansA, et al. (2003) Embryonic cell lineage of the marine nematode Pellioditis marina. Dev Biol 258: 57–69.
25. SulstonJE, SchierenbergE, WhiteJG, ThomsonJN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64–119.
26. AzevedoRB, LohausR, BraunV, GumbelM, UmamaheshwarM, et al. (2005) The simplicity of metazoan cell lineages. Nature 433: 152–156.
27. VlachosM, TavernarakisN (2010) Non-apoptotic cell death in Caenorhabditis elegans. Dev Dyn 239: 1337–1351.
28. LiuX, LongF, PengH, AerniSJ, JiangM, et al. (2009) Analysis of cell fate from single-cell gene expression profiles in C. elegans. Cell 139: 623–633.
29. Altun ZF, Herndon L.A., Crocker C., Lints R. and Hall D.H. (2010) WormAtlas. http://www.wormatlas.org/.
30. NishidaH (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol 121: 526–541.
31. AveryL, HorvitzHR (1987) A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 51: 1071–1078.
32. StentGS (1998) Developmental cell lineage. Int J Dev Biol 42: 237–241.
33. Slack JMW (1983) From Egg to Embryo. Cambridge: Cambridge University Press
34. LawsonKA, MenesesJJ, PedersenRA (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113: 891–911.
35. HeldeKA, WilsonET, CretekosCJ, GrunwaldDJ (1994) Contribution of early cells to the fate map of the zebrafish gastrula. Science 265: 517–520.
36. DormannD, WeijerCJ (2006) Imaging of cell migration. EMBO J 25: 3480–3493.
37. ZamirEA, CzirokA, CuiC, LittleCD, RongishBJ (2006) Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc Natl Acad Sci U S A 103: 19806–19811.
38. WasserstromA, AdarR, SheferG, FrumkinD, ItzkovitzS, et al. (2008) Reconstruction of cell lineage trees in mice. PLoS One 3: e1939.
39. SalipanteSJ, KasA, McMonagleE, HorwitzMS (2010) Phylogenetic analysis of developmental and postnatal mouse cell lineages. Evol Dev 12: 84–94.
40. ReizelY, ItzkovitzS, AdarR, ElbazJ, JinichA, et al. (2012) Cell lineage analysis of the mammalian female germline. PLoS Genet 8: e1002477.
41. KimmelCB, WargaRM, SchillingTF (1990) Origin and organization of the zebrafish fate map. Development 108: 581–594.
42. StentGS (1985) The role of cell lineage in development. Philos Trans R Soc Lond B Biol Sci 312: 3–19.
43. LongF, PengH, LiuX, KimSK, MyersE (2009) A 3D digital atlas of C. elegans and its application to single-cell analyses. Nat Methods 6: 667–672.
44. FelixMA, BarkoulasM (2012) Robustness and flexibility in nematode vulva development. Trends Genet 28: 185–195.
45. ShostakS (2008) Speculation on the evolution of stem cells. Breast Dis 29: 3–13.
46. ZhangJ, JeradiS, StrahleU, AkimenkoMA (2012) Laser ablation of the sonic hedgehog-a-expressing cells during fin regeneration affects ray branching morphogenesis. Dev Biol 365: 424–433.
47. WangZ, ZhangJ (2011) Impact of gene expression noise on organismal fitness and the efficacy of natural selection. Proc Natl Acad Sci U S A 108: E67–76.
48. WagnerG, BoothG, Bagheri-ChaichianH (1997) A population genetic theory of canalization. Evolution 51: 329–347.
49. LohausR, GeardNL, WilesJ, AzevedoRB (2007) A generative bias towards average complexity in artificial cell lineages. Proc Biol Sci 274: 1741–1750.
50. ItzkovitzS, BlatIC, JacksT, CleversH, van OudenaardenA (2012) Optimality in the development of intestinal crypts. Cell 148: 608–619.
51. HouthoofdW, WillemsM, JacobsenK, CoomansA, BorgonieG (2008) The embryonic cell lineage of the nematode Rhabditophanes sp. Int J Dev Biol 52: 963–967.
52. HouthoofdW, BorgonieG (2007) The embryonic cell lineage of the nematode Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea). Nematology 9: 573–584.
53. GaoJJ, PanXR, HuJ, MaL, WuJM, et al. (2011) Highly variable recessive lethal or nearly lethal mutation rates during germ-line development of male Drosophila melanogaster. Proc Natl Acad Sci U S A 108: 15914–15919.
54. EllisHM, HorvitzHR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817–829.
55. Starz-GaianoM, LehmannR (2001) Moving towards the next generation. Mech Dev 105: 5–18.
56. McLarenA (2003) Primordial germ cells in the mouse. Dev Biol 262: 1–15.
57. KellySJ (1977) Studies of the developmental potential of 4- and 8-cell stage mouse blastomeres. J Exp Zool 200: 365–376.
58. CarlsonCA, KasA, KirkwoodR, HaysLE, PrestonBD, et al. (2012) Decoding cell lineage from acquired mutations using arbitrary deep sequencing. Nat Methods 9: 78–80.
59. ZongC, LuS, ChapmanAR, XieXS (2012) Genome-wide detection of single-nucleotide and copy-number variations of a single human cell. Science 338: 1622–1626.
60. HouY, SongL, ZhuP, ZhangB, TaoY, et al. (2012) Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell 148: 873–885.
61. XuX, HouY, YinX, BaoL, TangA, et al. (2012) Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 148: 886–895.
62. SalipanteSJ, HorwitzMS (2006) Phylogenetic fate mapping. Proc Natl Acad Sci U S A 103: 5448–5453.
63. FrumkinD, WasserstromA, KaplanS, FeigeU, ShapiroE (2005) Genomic variability within an organism exposes its cell lineage tree. PLoS Comput Biol 1: e50.
64. SulstonJE, HorvitzHR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56: 110–156.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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