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Annual Review of Genetics

Volume 55, 2021

Dissecting Organismal Morphogenesis by Bridging Genetics and Biophysics

Abstract

Multicellular organisms develop complex shapes from much simpler, single-celled zygotes through a process commonly called morphogenesis. Morphogenesis involves an interplay between several factors, ranging from the gene regulatory networks determining cell fate and differentiation to the mechanical processes underlying cell and tissue shape changes. Thus, the study of morphogenesis has historically been based on multidisciplinary approaches at the interface of biology with physics and mathematics. Recent technological advances have further improved our ability to study morphogenesis by bridging the gap between the genetic and biophysical factors through the development of new tools for visualizing, analyzing, and perturbing these factors and their biochemical intermediaries. Here, we review how a combination of genetic, microscopic, biophysical, and biochemical approaches has aided our attempts to understand morphogenesis and discuss potential approaches that may be beneficial to such an inquiry in the future.

Keyword(s): biochemistry, biophysics, forward genetics, high-resolution microscopy, morphogenesis, patterning
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2021-11-23
2024-04-19
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Literature Cited

  1. 1. 
    Adler PN, Charlton J, Liu J 1998. Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. Development 125:5959–68
     [Google Scholar]
  2. 2. 
    Aegerter-Wilmsen T, Smith AC, Christen AJ, Aegerter CM, Hafen E, Basler K 2010. Exploring the effects of mechanical feedback on epithelial topology. Development 137:3499–506
     [Google Scholar]
  3. 3. 
    Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ 2013. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10:5413–20
     [Google Scholar]
  4. 4. 
    Alt S, Ganguly P, Salbreux G. 2017. Vertex models: from cell mechanics to tissue morphogenesis. Philos. Trans. R. Soc. B 372:172020150520
     [Google Scholar]
  5. 5. 
    Amos LA, Hirose K 2007. Studying the structure of microtubules by electron microscopy. Microtubule Protocols J Zhou 65–91 Totowa, NJ: Humana Press
     [Google Scholar]
  6. 6. 
    An Y, Xue G, Shaobo Y, Mingxi D, Zhou X et al. 2017. Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts. Development 144:122153–64
     [Google Scholar]
  7. 7. 
    Avery L. 1993. The genetics of feeding in Caenorhabditis elegans. Genetics 133:4897–917
     [Google Scholar]
  8. 8. 
    Babb SG, Barnett J, Doedens AL, Cobb N, Liu Q et al. 2001. Zebrafish E-cadherin: expression during early embryogenesis and regulation during brain development. Dev. Dyn. 221:2231–37
     [Google Scholar]
  9. 9. 
    Babb SG, Marrs JA. 2004. E-cadherin regulates cell movements and tissue formation in early zebrafish embryos. Dev. Dyn. 230:2263–77
     [Google Scholar]
  10. 10. 
    Bai X, Huang L-J, Chen S-W, Nebenfuehr B, Wysolmerski B et al. 2020. Loss of the seipin gene perturbs eggshell formation in Caenorhabditis elegans. Development 147:20dev192997
     [Google Scholar]
  11. 11. 
    Besner S, Scarcelli G, Pineda R, Yun S-H. 2016. In vivo Brillouin analysis of the aging crystalline lens. Invest. Ophthalmol. Vis. Sci. 57:135093–100
     [Google Scholar]
  12. 12. 
    Bieling P, Kandels-Lewis S, Telley IA, van Dijk J, Janke C, Surrey T 2008. CLIP-170 tracks growing microtubule ends by dynamically recognizing composite EB1/tubulin-binding sites. J. Cell Biol. 183:71223–33
     [Google Scholar]
  13. 13. 
    Biryukova I, Heitzler P. 2005. The Drosophila LIM-homeodomain protein Islet antagonizes proneural cell specification in the peripheral nervous system. Dev. Biol. 288:2559–70
     [Google Scholar]
  14. 14. 
    Blake KJ, Myette G, Jack J 1998. The products of ribbon and raw are necessary for proper cell shape and cellular localization of nonmuscle myosin in Drosophila. Dev. Biol. 203:1177–88
     [Google Scholar]
  15. 15. 
    Blanchard GB, Kabla AJ, Schultz NL, Butler LC, Sanson B et al. 2009. Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation. Nat. Methods 6:6458–64
     [Google Scholar]
  16. 16. 
    Boulay JL, Dennefeld C, Alberga A. 1987. The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330:6146395–98
     [Google Scholar]
  17. 17. 
    Bradley PL, Andrew DJ. 2001. ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128:153001–15
     [Google Scholar]
  18. 18. 
    Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:171–94
     [Google Scholar]
  19. 19. 
    Brodland GW, Veldhuis JH, Kim S, Perrone M, Mashburn D, Hutson MS 2014. CellFIT: a cellular force-inference toolkit using curvilinear cell boundaries. PLOS ONE 9:6e99116
     [Google Scholar]
  20. 20. 
    Brown KS, Blower MD, Maresca TJ, Grammer TC, Harland RM, Heald R 2007. Xenopus tropicalis egg extracts provide insight into scaling of the mitotic spindle. J. Cell Biol. 176:6765–70
     [Google Scholar]
  21. 21. 
    Byars CL, Bates KL, Letsou A. 1999. The dorsal-open group gene raw is required for restricted DJNK signaling during closure. Dev. Camb. Engl. 126:214913–23
     [Google Scholar]
  22. 22. 
    Carvalho L, Heisenberg C-P 2009. Imaging zebrafish embryos by two-photon excitation time-lapse microscopy. Zebrafish: Methods and Protocols GJ Lieschke, AC Oates, K Kawakami 273–87 Totowa, NJ: Humana Press
     [Google Scholar]
  23. 23. 
    Chan CJ, Bevilacqua C, Prevedel R. 2021. Mechanical mapping of mammalian follicle development using Brillouin microscopy. bioRxiv 432113. https://doi.org/10.1101/2021.02.21.432113
    [Crossref]
  24. 24. 
    Chen CM, Struhl G. 1999. Wingless transduction by the Frizzled and Frizzled2 proteins of Drosophila. Development 126:235441–52
     [Google Scholar]
  25. 25. 
    Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 1997. Geometric control of cell life and death. Science 276:53171425–28
     [Google Scholar]
  26. 26. 
    Chen L, McCloskey T, Joshi PM, Rothman JH. 2008. ced-4 and proto-oncogene tfg-1 antagonistically regulate cell size and apoptosis in C. elegans. Curr. Biol. 18:141025–33
     [Google Scholar]
  27. 27. 
    Conradt B, Horvitz HR. 1998. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93:4519–29
     [Google Scholar]
  28. 28. 
    Cubadda Y, Heitzler P, Ray RP, Bourouis M, Ramain P et al. 1997. u-shaped encodes a zinc finger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila. Genes Dev 11:223083–95
     [Google Scholar]
  29. 29. 
    Denk W, Strickler JH, Webb WW. 1990. Two-photon laser scanning fluorescence microscopy. Science 248:495173–76
     [Google Scholar]
  30. 30. 
    Devenport D. 2014. The cell biology of planar cell polarity. J. Cell Biol. 207:2171–79
     [Google Scholar]
  31. 31. 
    Dil JG. 1982. Brillouin scattering in condensed matter. Rep. Prog. Phys. 45:3285–334
     [Google Scholar]
  32. 32. 
    Dogterom M, Kerssemakers JW, Romet-Lemonne G, Janson ME. 2005. Force generation by dynamic microtubules. Curr. Opin. Cell Biol. 17:167–74
     [Google Scholar]
  33. 33. 
    Doubrovinski K, Swan M, Polyakov O, Wieschaus EF 2017. Measurement of cortical elasticity in Drosophila melanogaster embryos using ferrofluids. PNAS 114:51051–56
     [Google Scholar]
  34. 34. 
    Doyle T, Botstein D 1996. Movement of yeast cortical actin cytoskeleton visualized in vivo. PNAS 93:93886–91
     [Google Scholar]
  35. 35. 
    Driever W, Solnica-Krezel L, Schier AF, Neuhauss SC, Malicki J et al. 1996. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123:37–46
     [Google Scholar]
  36. 36. 
    Dupont J-C. 2017. Wilhelm His and mechanistic approaches to development at the time of Entwicklungsmechanik. Hist. Philos. Life Sci. 39:321
     [Google Scholar]
  37. 37. 
    Ellis HM, Horvitz HR. 1986. Genetic control of programmed cell death in the nematode C. elegans. Cell 44:6817–29
     [Google Scholar]
  38. 38. 
    Erni R, Rossell MD, Kisielowski C, Dahmen U. 2009. Atomic-resolution imaging with a sub-50-pm electron probe. Phys. Rev. Lett. 102:9096101
     [Google Scholar]
  39. 39. 
    Farhadifar R, Röper J-C, Aigouy B, Eaton S, Jülicher F. 2007. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 17:242095–104
     [Google Scholar]
  40. 40. 
    Fletcher AG, Osterfield M, Baker RE, Shvartsman SY. 2014. Vertex models of epithelial morphogenesis. Biophys. J. 106:112291–304
     [Google Scholar]
  41. 41. 
    Fodor E, Zsigmond Á, Horváth B, Molnár J, Nagy I et al. 2013. Full transcriptome analysis of early dorsoventral patterning in zebrafish. PLOS ONE 8:7e70053
     [Google Scholar]
  42. 42. 
    Frohnhöfer HG, Nüsslein-Volhard C. 1986. Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324:6093120–25
     [Google Scholar]
  43. 43. 
    Frøkjær-Jensen C, Davis MW, Ailion M, Jorgensen EM 2012. Improved Mos1-mediated transgenesis in C. elegans. Nat. Methods 9:2117–18
     [Google Scholar]
  44. 44. 
    Frøkjær-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM et al. 2008. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40:111375–83
     [Google Scholar]
  45. 45. 
    Goldstein B, Hird SN. 1996. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122:51467–74
     [Google Scholar]
  46. 46. 
    Gönczy P, Echeverri C, Oegema K, Coulson A, Jones SJM et al. 2000. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408:6810331–36
     [Google Scholar]
  47. 47. 
    Gong L, Puri M, Ünlü M, Young M, Robertson K et al. 2004. Drosophila ventral furrow morphogenesis: a proteomic analysis. Development 131:3643–56
     [Google Scholar]
  48. 48. 
    Grau Y, Carteret C, Simpson P. 1984. Mutations and chromosomal rearrangements affecting the expression of snail, a gene involved in embryonic patterning in Drosophila melanogaster. Genetics 108:2347–60
     [Google Scholar]
  49. 49. 
    Grill SW, Gönczy P, Stelzer EHK, Hyman AA. 2001. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:6820630–33
     [Google Scholar]
  50. 50. 
    Haeckel E. 1866. Generelle Morphologie der Organismen. Allgemeine Grundzüge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin reformirte Descendenztheorie Berlin: G. Reimer
  51. 51. 
    Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M et al. 1996. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123:1–36
     [Google Scholar]
  52. 52. 
    Hammerschmidt M, Pelegri F, Mullins MC, Kane DA, Brand M et al. 1996. Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio. Development 123:143–51
     [Google Scholar]
  53. 53. 
    Hannak E, Heald R. 2006. Investigating mitotic spindle assembly and function in vitro using Xenopus laevis egg extracts. Nat. Protoc. 1:52305–14
     [Google Scholar]
  54. 54. 
    Harmansa S, Alborelli I, Bieli D, Caussinus E, Affolter M. 2017. A nanobody-based toolset to investigate the role of protein localization and dispersal in Drosophila. eLife 6:e22549
     [Google Scholar]
  55. 55. 
    Hedgecock E, Sulston J, Thomson J. 1983. Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220:46031277–79
     [Google Scholar]
  56. 56. 
    Heisenberg C-P, Brand M, Jiang Y-J, Warga RM, Beuchle D et al. 1996. Genes involved in forebrain development in the zebrafish, Danio rerio. Development 123:191–203
     [Google Scholar]
  57. 57. 
    Heisenberg C-P, Tada M, Rauch G-J, Saúde L, Concha ML et al. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405:678276–81
     [Google Scholar]
  58. 58. 
    Hemenway CS, Halligan BW, Levy LS. 1998. The Bmi-1 oncoprotein interacts with dinG and MPh2: the role of RING finger domains. Oncogene 16:192541–47
     [Google Scholar]
  59. 59. 
    Hengartner MO, Ellis R, Horvitz R 1992. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 356:6369494–99
     [Google Scholar]
  60. 60. 
    Hird SN, White JG. 1993. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol. 121:61343–55
     [Google Scholar]
  61. 61. 
    Hofer M, Lutolf MP. 2021. Engineering organoids. Nat. Rev. Mater. 6:402–20
     [Google Scholar]
  62. 62. 
    Honda H, Nagai T, Tanemura M. 2008. Two different mechanisms of planar cell intercalation leading to tissue elongation. Dev. Dyn. 237:71826–36
     [Google Scholar]
  63. 63. 
    Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS et al. 2009. An EB1-binding motif acts as a microtubule tip localization signal. Cell 138:2366–76
     [Google Scholar]
  64. 64. 
    Huisken J, Swoger J, Del Bene F, Wittbrodt J, Stelzer EHK 2004. Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305:56861007–9
     [Google Scholar]
  65. 65. 
    Ip YT, Park RE, Kosman D, Yazdanbakhsh K, Levine M 1992. dorsal–twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 6:81518–30
     [Google Scholar]
  66. 66. 
    Irvine KD, Wieschaus E. 1994. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120:4827–41
     [Google Scholar]
  67. 67. 
    Izquierdo E, Quinkler T, De Renzis S. 2018. Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis. Nat. Commun. 9:2366
     [Google Scholar]
  68. 68. 
    Jacinto A, Wood W, Balayo T, Turmaine M, Martinez-Arias A, Martin P. 2000. Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 10:221420–26
     [Google Scholar]
  69. 69. 
    Jambor H, Surendranath V, Kalinka AT, Mejstrik P, Saalfeld S, Tomancak P. Systematic imaging reveals features and changing localization of mRNAs in Drosophila development. eLife 4:e05003
     [Google Scholar]
  70. 70. 
    Jessen JR, Topczewski J, Bingham S, Sepich DS, Marlow F et al. 2002. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4:8610–15
     [Google Scholar]
  71. 71. 
    Jiang Y-J, Brand M, Heisenberg CP, Beuchle D, Furutani-Seiki M et al. 1996. Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123:205–16
     [Google Scholar]
  72. 72. 
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science 337:6096816–21
     [Google Scholar]
  73. 73. 
    Joanny J-F, Prost J. 2009. Active gels as a description of the actin-myosin cytoskeleton. HFSP J. 3:294–104
     [Google Scholar]
  74. 74. 
    Jülicher F, Kruse K, Prost J, Joanny J-F. 2007. Active behavior of the cytoskeleton. Phys. Rep. 449:1–33–28
     [Google Scholar]
  75. 75. 
    Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster: II. Zygotic loci on the third chromosome. Roux Arch. . Dev. Biol. 193:5283–95
     [Google Scholar]
  76. 76. 
    Kane DA, McFarland KN, Warga RM. 2005. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 132:51105–16
     [Google Scholar]
  77. 77. 
    Kane DA, Hammerschmidt M, Mullins MC, Maischein HM, Brand M et al. 1996. The zebrafish epiboly mutants. Development 123:47–55
     [Google Scholar]
  78. 78. 
    Karlstrom RO, Trowe T, Klostermann S, Baier H, Brand M et al. 1996. Zebrafish mutations affecting retinotectal axon pathfinding. Development 123:427–38
     [Google Scholar]
  79. 79. 
    Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK. 2008. Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:59041065–69
     [Google Scholar]
  80. 80. 
    Kelly C, Chin AJ, Leatherman JL, Kozlowski DJ, Weinberg ES. 2000. Maternally controlled β-catenin-mediated signaling is required for organizer formation in the zebrafish. Development 127:183899–911
     [Google Scholar]
  81. 81. 
    Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA. 2000. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149:2471–90
     [Google Scholar]
  82. 82. 
    Kieserman EK, Heald R. 2011. Mitotic chromosome size scaling in Xenopus. Cell Cycle 10:223863–70
     [Google Scholar]
  83. 83. 
    Kong D, Wolf F, Großhans J 2017. Forces directing germ-band extension in Drosophila embryos. Mech. Dev. 144:11–22
     [Google Scholar]
  84. 84. 
    Köppen M, García Fernández B, Carvalho L, Jacinto A, Heisenbert C-P 2006. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development 133:142671–81
     [Google Scholar]
  85. 85. 
    Koski KJ, Yarger JL. 2005. Brillouin imaging. Appl. Phys. Lett. 87:6061903
     [Google Scholar]
  86. 86. 
    Kosman D, Ip YT, Levine M, Arora K. 1991. Establishment of the mesoderm-neuroectoderm boundary in the Drosophila embryo. Science 254:5028118–22
     [Google Scholar]
  87. 87. 
    Krieg M, Arboleda-Estudillo Y, Puech P-H, Käfer J, Graner F et al. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10:4429–36
     [Google Scholar]
  88. 88. 
    Krishnamurthy VV, Khamo JS, Mei W, Turgeon AJ, Ashraf HM et al. 2016. Reversible optogenetic control of kinase activity during differentiation and embryonic development. Development 143:214085–94
     [Google Scholar]
  89. 89. 
    Krueger D, Izquierdo E, Viswanathan R, Hartmann J, Pallares Cartes C, De Renzis S. 2019. Principles and applications of optogenetics in developmental biology. Development 146:20dev175067
     [Google Scholar]
  90. 90. 
    Kumar A, Wu Y, Christensen R, Chandris P, Gandler W et al. 2014. Dual-view plane illumination microscopy for rapid and spatially isotropic imaging. Nat. Protoc. 9:112555–73
     [Google Scholar]
  91. 91. 
    Lecuit T, Lenne P-F, Munro E. 2011. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27:157–84
     [Google Scholar]
  92. 92. 
    Lele Z, Folchert A, Concha M, Rauch G-J, Geisler R et al. 2002. parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129:143281–94
     [Google Scholar]
  93. 93. 
    Leptin M. 1991. twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5:91568–76
     [Google Scholar]
  94. 94. 
    Li Q, Joshi HC 1995. γ-Tubulin is a minus end-specific microtubule binding protein. J. Cell Biol. 131:1207–14
     [Google Scholar]
  95. 95. 
    Liu Y, Dale S, Ball R, VanLeuven AJ, Sornborger A et al. 2019. Imaging neural events in zebrafish larvae with linear structured illumination light sheet fluorescence microscopy. Neurophotonics 6:1015009
     [Google Scholar]
  96. 96. 
    Loughlin R, Wilbur JD, McNally FJ, Nédélec FJ, Heald R. 2011. Katanin contributes to interspecies spindle length scaling in Xenopus. Cell 147:61397–407
     [Google Scholar]
  97. 97. 
    Maienschein J 1991. The origins of Entwicklungsmechanik. A Conceptual History of Modern Embryology SF Gilbert 43–61 Boston: Springer US
     [Google Scholar]
  98. 98. 
    Maître J-L, Berthoumieux H, Krens SFG, Salbreux G, Jülicher F et al. 2012. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338:6104253–56
     [Google Scholar]
  99. 99. 
    Maître J-L, Niwayama R, Turlier H, Nédélec F, Hiiragi T 2015. Pulsatile cell-autonomous contractility drives compaction in the mouse embryo. Nat. Cell Biol. 17:7849–55
     [Google Scholar]
  100. 100. 
    Mammoto A, Huang S, Moore K, Oh P, Ingber DE. 2004. Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J. Biol. Chem. 279:2526323–30
     [Google Scholar]
  101. 101. 
    Mammoto A, Ingber DE. 2009. Cytoskeletal control of growth and cell fate switching. . Curr. Opin. Cell Biol. 21:6864–70
     [Google Scholar]
  102. 102. 
    Marlow FL, Mullins MC. 2008. Bucky ball functions in Balbiani body assembly and animal–vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev. Biol. 321:140–50
     [Google Scholar]
  103. 103. 
    Matsuda M, Koga M, Woltjen K, Nishida E, Ebisuya M. 2015. Synthetic lateral inhibition governs cell-type bifurcation with robust ratios. Nat. Commun. 6:6195
     [Google Scholar]
  104. 104. 
    Mayer M, Depken M, Bois JS, Jülicher F, Grill SW 2010. Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467:7315617–21
     [Google Scholar]
  105. 105. 
    McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6:4483–95
     [Google Scholar]
  106. 106. 
    McMahon A, Supatto W, Fraser SE, Stathopoulos A 2008. Dynamic analyses of Drosophila gastrulation provide insights into collective cell migration. Science 322:59071546–50
     [Google Scholar]
  107. 107. 
    Millo H, Leaper K, Lazou V, Bownes M. 2004. Myosin VI plays a role in cell-cell adhesion during epithelial morphogenesis. Mech. Dev. 121:111335–51
     [Google Scholar]
  108. 108. 
    Mishra N, Wei H, Conradt B 2018. Caenorhabditis elegans ced-3 caspase is required for asymmetric divisions that generate cells programmed to die. Genetics 210:3983–98
     [Google Scholar]
  109. 109. 
    Montero J-A, Carvalho L, Wilsch-Bräuninger M, Kilian B, Mustafa C, Heisenberg C-P. 2005. Shield formation at the onset of zebrafish gastrulation. Development 132:61187–98
     [Google Scholar]
  110. 110. 
    Mortensen RD, Moore RP, Fogerson SM, Chiou HY, Obinero CV et al. 2018. Identifying genetic players in cell sheet morphogenesis using a Drosophila deficiency screen for genes on chromosome 2R involved in dorsal closure. G3 8:72361–87
     [Google Scholar]
  111. 111. 
    Munro E, Nance J, Priess JR 2004. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev. Cell 7:3413–24
     [Google Scholar]
  112. 112. 
    Murray AW, Kirschner MW. 1989. Cyclin synthesis drives the early embryonic cell cycle. Nature 339:6222275–80
     [Google Scholar]
  113. 113. 
    Numaguchi Y, Huang S, Polte TR, Eichler GS, Wang N, Ingber DE 2003. Caldesmon-dependent switching between capillary endothelial cell growth and apoptosis through modulation of cell shape and contractility. Angiogenesis 6:155–64
     [Google Scholar]
  114. 114. 
    Nüsslein-Volhard C. 2012. The zebrafish issue of Development. Development 139:224099–103
     [Google Scholar]
  115. 115. 
    Nüsslein-Volhard C, Frohnhofer H, Lehmann R 1987. Determination of anteroposterior polarity in Drosophila. Science 238:48341675–81
     [Google Scholar]
  116. 116. 
    Nüsslein-Volhard C, Wieschaus E. 1980. Mutations affecting segment number and polarity in Drosophila. Nature 287:5785795–801
     [Google Scholar]
  117. 117. 
    Nüsslein-Volhard C, Wieschaus E, Kluding H 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster: I. Zygotic loci on the second chromosome. Roux Arch. . Dev. Biol. 193:5267–82
     [Google Scholar]
  118. 118. 
    Odenthal J, Haffter P, Vogelsang E, Brand M, van Eeden FJ et al. 1996. Mutations affecting the formation of the notochord in the zebrafish, Danio rerio. Development 123:103–15
     [Google Scholar]
  119. 119. 
    Okuda S, Inoue Y, Adachi T. 2015. Three-dimensional vertex model for simulating multicellular morphogenesis. Biophys. Physicobiol. 12:13–20
     [Google Scholar]
  120. 120. 
    Olarte OE, Andilla J, Artigas D, Loza-Alvarez P. Decoupled illumination detection in light sheet microscopy for fast volumetric imaging. Optica 2:8702–5
     [Google Scholar]
  121. 121. 
    Olivier N, Luengo-Oroz MA, Duloquin L, Faure E, Savy T et al. 2010. Cell lineage reconstruction of early zebrafish embryos using label-free nonlinear microscopy. Science 329:5994967–71
     [Google Scholar]
  122. 122. 
    Olson SK, Greenan G, Desai A, Müller-Reichert T, Oegema K. 2012. Hierarchical assembly of the eggshell and permeability barrier in C. elegans. J. Cell Biol. 198:4731–48
     [Google Scholar]
  123. 123. 
    Ou G, Stuurman N, D'Ambrosio M, Vale RD 2010. Polarized myosin produces unequal-size daughters during asymmetric cell division. Science 330:6004677–80
     [Google Scholar]
  124. 124. 
    Ou G, Vale RD. 2009. Molecular signatures of cell migration in C. elegans Q neuroblasts. J. Cell Biol. 185:177–85
     [Google Scholar]
  125. 125. 
    Ozbay BN, Futia GL, Ma M, Bright VM, Gopinath JT et al. 2018. Three dimensional two-photon brain imaging in freely moving mice using a miniature fiber coupled microscope with active axial-scanning. Sci. Rep. 8:8108
     [Google Scholar]
  126. 126. 
    Park M, Moon RT 2002. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol. 4:20–25
     [Google Scholar]
  127. 127. 
    Parsons MJ, Pollard SM, Saúde L, Feldman B, Coutinho P et al. 2002. Zebrafish mutants identify an essential role for laminins in notochord formation. Development 129:133137–46
     [Google Scholar]
  128. 128. 
    Paulus JD, Halloran MC. 2006. Zebrafish bashful/laminin-α1 mutants exhibit multiple axon guidance defects. Dev. Dyn. 235:1213–24
     [Google Scholar]
  129. 129. 
    Peerani R, Rao BM, Bauwens C, Yin T, Wood GA et al. 2007. Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J 26:224744–55
     [Google Scholar]
  130. 130. 
    Perrimon N, Engstrom L, Mahowald AP. 1989. Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121:2333–52
     [Google Scholar]
  131. 131. 
    Perrimon N, Lanjuin A, Arnold C, Noll E 1996. Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics 144:41681–92
     [Google Scholar]
  132. 132. 
    Petridou NI, Grigolon S, Salbreux G, Hannezo E, Heisenberg C-P. 2019. Fluidization-mediated tissue spreading by mitotic cell rounding and non-canonical Wnt signalling. Nat. Cell Biol. 21:2169–78
     [Google Scholar]
  133. 133. 
    Piotrowski T, Schilling TF, Brand M, Jiang YJ, Heisenberg C-P et al. 1996. Jaw and branchial arch mutants in zebrafish II: anterior arches and cartilage differentiation. Development 123:345–56
     [Google Scholar]
  134. 134. 
    Prost J, Jülicher F, Joanny J-F. 2015. Active gel physics. Nat. Phys. 11:2111–17
     [Google Scholar]
  135. 135. 
    Puech P-H, Taubenberger A, Ulrich F, Krieg M, Muller DJ, Heisenberg C-P. 2005. Measuring cell adhesion forces of primary gastrulating cells from zebrafish using atomic force microscopy. J. Cell Sci. 118:184199–206
     [Google Scholar]
  136. 136. 
    Raghunathan R, Zhang J, Wu C, Rippy J, Singh M et al. 2017. Evaluating biomechanical properties of murine embryos using Brillouin microscopy and optical coherence tomography. J. Biomed. Opt. 22:8086013
     [Google Scholar]
  137. 137. 
    Rauch G-J, Hammerschmidt M, Blader P, Schauerte HE, Strähle U et al. 1997. WNT5 is required for tail formation in the zebrafish embryo. Cold Spring Harb. Symp. Quant. Biol. 62:227–34
     [Google Scholar]
  138. 138. 
    Rossi G, Manfrin A, Lutolf MP 2018. Progress and potential in organoid research. Nat. Rev. Genet. 19:11671–87
     [Google Scholar]
  139. 139. 
    Roth S, Stein D, Nüsslein-Volhard C. 1989. A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59:61189–202
     [Google Scholar]
  140. 140. 
    Sammak PJ, Borisy GG. 1988. Direct observation of microtubule dynamics in living cells. Nature 332:6166724–26
     [Google Scholar]
  141. 141. 
    Scarcelli G, Besner S, Pineda R, Kalout P, Yun SH 2015. In vivo biomechanical mapping of normal and keratoconus corneas. JAMA Ophthalmol 133:4480
     [Google Scholar]
  142. 142. 
    Scarcelli G, Yun SH. 2007. Confocal Brillouin microscopy for three-dimensional mechanical imaging. Nat. Photon. 2:39–43
     [Google Scholar]
  143. 143. 
    Schroeder TE. 1968. Cytokinesis: filaments in the cleavage furrow. Exp. Cell Res. 53:1272–76
     [Google Scholar]
  144. 144. 
    Schroeder TE. 1972. The contractile ring: II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J. Cell Biol. 53:2419–34
     [Google Scholar]
  145. 145. 
    Schulze C, Wetzel F, Kueper T, Malsen A, Muhr G et al. 2010. Stiffening of human skin fibroblasts with age. Biophys. J. 99:82434–42
     [Google Scholar]
  146. 146. 
    Schüpbach T, Wieschaus E. 1986. Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux Arch. . Dev. Biol. 195:5302–17
     [Google Scholar]
  147. 147. 
    Schutgens F, Clevers H. 2020. Human organoids: tools for understanding biology and treating diseases. Annu. Rev. Pathol. Mech. Dis. 15:211–34
     [Google Scholar]
  148. 148. 
    Selman K, Wallace RA, Sarka A, Qi X. 1993. Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphol. 218:2203–24
     [Google Scholar]
  149. 149. 
    Shamipour S, Kardos R, Xue S-L, Hof B, Hannezo E, Heisenberg C-P. 2019. Bulk actin dynamics drive phase segregation in zebrafish oocytes. Cell 177:61463–79.e18
     [Google Scholar]
  150. 150. 
    Shelden E, Wadsworth P 1993. Observation and quantification of individual microtubule behavior in vivo: microtubule dynamics are cell-type specific. J. Cell Biol. 120:4935–45
     [Google Scholar]
  151. 151. 
    Simpson P. 1983. Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105:3615–32
     [Google Scholar]
  152. 152. 
    Singh A, Saha T, Begemann I, Ricker A, Nüsse H et al. 2018. Polarized microtubule dynamics directs cell mechanics and coordinates forces during epithelial morphogenesis. Nat. Cell Biol. 20:101126–33
     [Google Scholar]
  153. 153. 
    Solini GE, Dong C, Saha M. 2017. Embryonic transplantation experiments: past, present, and future. Trends Dev. Biol. 10:13–30
     [Google Scholar]
  154. 154. 
    Solnica-Krezel L, Driever W. 1994. Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120:92443–55
     [Google Scholar]
  155. 155. 
    Solnica-Krezel L, Stemple DL, Mountcastle-Shah E, Rangini Z, Neuhauss SC et al. 1996. Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 123:67–80
     [Google Scholar]
  156. 156. 
    Spahn P, Reuter R. 2013. A vertex model of Drosophila ventral furrow formation. PLOS ONE 8:9e75051
     [Google Scholar]
  157. 157. 
    Spiess M, Hernandez-Varas P, Oddone A, Olofsson H, Blom H et al. 2018. Active and inactive β1 integrins segregate into distinct nanoclusters in focal adhesions. J. Cell Biol. 217:61929–40
     [Google Scholar]
  158. 158. 
    Staple DB, Farhadifar R, Röper J-C, Aigouy B, Eaton S, Jülicher F. 2010. Mechanics and remodelling of cell packings in epithelia. Eur. Phys. J. E 33:2117–27
     [Google Scholar]
  159. 159. 
    Steward R. 1987. Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238:4827692–94
     [Google Scholar]
  160. 160. 
    Straight AF, Marshall WF, Sedat JW, Murray AW. 1997. Mitosis in living budding yeast: anaphase A but no metaphase plate. Science 277:5325574–78
     [Google Scholar]
  161. 161. 
    Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56:1110–56
     [Google Scholar]
  162. 162. 
    Sulston JE, Horvitz HR. 1981. Abnormal cell lineages in mutants of the nematode Caenorhabditis elegans. Dev. Biol. 82:141–55
     [Google Scholar]
  163. 163. 
    Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100:164–119
     [Google Scholar]
  164. 164. 
    Taslimi A, Vrana JD, Chen D, Borinskaya S, Mayer BJ et al. 2014. An optimized optogenetic clustering tool for probing protein interaction and function. Nat. Commun. 5:4925
     [Google Scholar]
  165. 165. 
    Telley IA, Gáspár I, Ephrussi A, Surrey T 2012. Aster migration determines the length scale of nuclear separation in the Drosophila syncytial embryo. J. Cell Biol. 197:7887–95
     [Google Scholar]
  166. 166. 
    Thisse B, Stoetzel C, Gorostiza-Thisse C, Perrin-Schmitt F. 1988. Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7:72175–83
     [Google Scholar]
  167. 167. 
    Thompson DW. 1992. 1917. On Growth and Form Cambridge, UK: Cambridge Univ. Press
  168. 168. 
    Thorpe CJ, Schlesinger A, Carter JC, Bowerman B. 1997. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90:4695–705
     [Google Scholar]
  169. 169. 
    Tomer R, Khairy K, Amat F, Keller PJ 2012. Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nat. Methods 9:7755–63
     [Google Scholar]
  170. 170. 
    Topczewski J, Sepich DS, Myers DC, Walker C, Amores A et al. 2001. The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1:2251–64
     [Google Scholar]
  171. 171. 
    Truong TV, Supatto W, Koos DS, Choi JM, Fraser SE. 2011. Deep and fast live imaging with two-photon scanned light-sheet microscopy. Nat. Methods 8:9757–60
     [Google Scholar]
  172. 172. 
    Tsai TY-C, Sikora M, Xia P, Colak-Champollion T, Knaut H et al. 2020. An adhesion code ensures robust pattern formation during tissue morphogenesis. Science 370:6512113–16
     [Google Scholar]
  173. 173. 
    Verveer PJ, Swoger J, Pampaloni F, Greger K, Marcello M, Stelzer EHK 2007. High-resolution three-dimensional imaging of large specimens with light sheet-based microscopy. Nat. Methods 4:4311–13
     [Google Scholar]
  174. 174. 
    Voltes A, Hevia CF, Engel-Pizcueta C, Dingare C, Calzolari S et al. 2019. Yap/Taz-TEAD activity links mechanical cues to progenitor cell behavior during zebrafish hindbrain segmentation. Development 146:14dev176735
     [Google Scholar]
  175. 175. 
    Voncken JW, Roelen BAJ, Roefs M, de Vries S, Verhoeven E et al. 2003. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. PNAS 100:52468–73
     [Google Scholar]
  176. 176. 
    Weaver BP, Weaver YM, Mitani S, Han M. 2017. Coupled caspase and N-end rule ligase activities allow recognition and degradation of pluripotency factor LIN-28 during non-apoptotic development. Dev. Cell 41:6665–73.e6
     [Google Scholar]
  177. 177. 
    Wieschaus E, Nüsslein-Volhard C. 2016. The Heidelberg screen for pattern mutants of Drosophila: a personal account. Annu. Rev. Cell Dev. Biol. 32:1–46
     [Google Scholar]
  178. 178. 
    Wieschaus E, Nüsslein-Volhard C, Jürgens G. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster: III. Zygotic loci on the X-chromosome and fourth chromosome. Roux Arch. . Dev. Biol. 193:5296–307
     [Google Scholar]
  179. 179. 
    Williams AL, Bohnsack BL. 2017. Multi-photon time lapse imaging to visualize development in real-time: visualization of migrating neural crest cells in zebrafish embryos. J. Vis. Exp. 126:56214
     [Google Scholar]
  180. 180. 
    Xia P, Gütl D, Zheden V, Heisenberg C-P. 2019. Lateral inhibition in cell specification mediated by mechanical signals modulating TAZ activity. Cell 176:61379–92.e14
     [Google Scholar]
  181. 181. 
    Yang C, Axelrod JD, Simon MA. 2002. Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108:5675–88
     [Google Scholar]
  182. 182. 
    Yang Y, Mlodzik M 2015. Wnt-Frizzled/planar cell polarity signaling: cellular orientation by facing the wind (Wnt). Annu. Rev. Cell Dev. Biol. 31:623–46
     [Google Scholar]
  183. 183. 
    Yau KW, van Beuningen SFB, Cunha-Ferreira I, Cloin BMC, van Battum EY et al. 2014. Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82:51058–73
     [Google Scholar]
  184. 184. 
    Young PE, Richman AM, Ketchum AS, Kiehart DP. 1993. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7:29–41
     [Google Scholar]
  185. 185. 
    Zallen JA. 2007. Planar polarity and tissue morphogenesis. Cell 129:61051–63
     [Google Scholar]
  186. 186. 
    Zhang J, Raghunathan R, Rippy J, Wu C, Finnell RH et al. 2019. Tissue biomechanics during cranial neural tube closure measured by Brillouin microscopy and optical coherence tomography. Birth Defects Res 111:14991–98
     [Google Scholar]
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Dissecting Organismal Morphogenesis by Bridging Genetics and Biophysics
Annual Review of Genetics 55, 209 (2021); https://doi.org/10.1146/annurev-genet-071819-103748
/content/journals/10.1146/annurev-genet-071819-103748
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