There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator

Höhn S, Hallmann A (2011)
BMC Biology 9(1): 89.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Abstract / Bemerkung
Background: Epithelial folding is a common morphogenetic process during the development of multicellular organisms. In metazoans, the biological and biomechanical processes that underlie such three-dimensional (3D) developmental events are usually complex and difficult to investigate. Spheroidal green algae of the genus Volvox are uniquely suited as model systems for studying the basic principles of epithelial folding. Volvox embryos begin life inside out and then must turn their spherical cell monolayer outside in to achieve their adult configuration; this process is called 'inversion.' There are two fundamentally different sequences of inversion processes in Volvocaceae: type A and type B. Type A inversion is well studied, but not much is known about type B inversion. How does the embryo of a typical type B inverter, V. globator, turn itself inside out? Results: In this study, we investigated the type B inversion of V. globator embryos and focused on the major movement patterns of the cellular monolayer, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. Isolated intact, sectioned and fragmented embryos were analyzed throughout the inversion process using light microscopy, confocal laser scanning microscopy, scanning electron microscopy and transmission electron microscopy techniques. We generated 3D models of the identified cell shapes, including the localizations of CBs. We show how concerted cell-shape changes and concerted changes in the position of cells relative to the CB system cause cell layer movements and turn the spherical cell monolayer inside out. The type B inversion of V. globator is compared to the type A inversion in V. carteri. Conclusions: Concerted, spatially and temporally coordinated changes in cellular shapes in conjunction with concerted migration of cells relative to the CB system are the causes of type B inversion in V. globator. Despite significant similarities between type A and type B inverters, differences exist in almost all details of the inversion process, suggesting analogous inversion processes that arose through parallel evolution. Based on our results and due to the cellular biomechanical implications of the involved tensile and compressive forces, we developed a global mechanistic scenario that predicts epithelial folding during embryonic inversion in V. globator.
Erscheinungsjahr
2011
Zeitschriftentitel
BMC Biology
Band
9
Ausgabe
1
Art.-Nr.
89
ISSN
1741-7007
Finanzierungs-Informationen
Open-Access-Publikationskosten wurden durch die Deutsche Forschungsgemeinschaft und die Universität Bielefeld gefördert.
Page URI
https://pub.uni-bielefeld.de/record/2454524

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Höhn S, Hallmann A. There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator. BMC Biology. 2011;9(1): 89.
Höhn, S., & Hallmann, A. (2011). There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator. BMC Biology, 9(1), 89. doi:10.1186/1741-7007-9-89
Höhn, Stephanie, and Hallmann, Armin. 2011. “There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator”. BMC Biology 9 (1): 89.
Höhn, S., and Hallmann, A. (2011). There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator. BMC Biology 9:89.
Höhn, S., & Hallmann, A., 2011. There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator. BMC Biology, 9(1): 89.
S. Höhn and A. Hallmann, “There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator”, BMC Biology, vol. 9, 2011, : 89.
Höhn, S., Hallmann, A.: There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator. BMC Biology. 9, : 89 (2011).
Höhn, Stephanie, and Hallmann, Armin. “There is more than one way to turn a spherical cellular monolayer inside out: type B embryo inversion in Volvox globator”. BMC Biology 9.1 (2011): 89.
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12 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The noisy basis of morphogenesis: Mechanisms and mechanics of cell sheet folding inferred from developmental variability.
Haas PA, Höhn SSMH, Honerkamp-Smith AR, Kirkegaard JB, Goldstein RE., PLoS Biol 16(7), 2018
PMID: 30001335
Cell shape change and invagination of the cephalic furrow involves reorganization of F-actin.
Spencer AK, Siddiqui BA, Thomas JH., Dev Biol 402(2), 2015
PMID: 25929228
Elasticity and glocality: initiation of embryonic inversion in Volvox.
Haas PA, Goldstein RE., J R Soc Interface 12(112), 2015
PMID: 26490631
Stable nuclear transformation of Pandorina morum.
Lerche K, Hallmann A., BMC Biotechnol 14(), 2014
PMID: 25031031
Green algae and the origins of multicellularity in the plant kingdom.
Umen JG., Cold Spring Harb Perspect Biol 6(11), 2014
PMID: 25324214
The bending of cell sheets--from folding to rolling.
Keller R, Shook D., BMC Biol 9(), 2011
PMID: 22206439

90 References

Daten bereitgestellt von Europe PubMed Central.


AUTHOR UNKNOWN, 2004
Conserved patterns of cell movements during vertebrate gastrulation.
Solnica-Krezel L., Curr. Biol. 15(6), 2005
PMID: 15797016
Biology and physics of cell shape changes in development.
Paluch E, Heisenberg CP., Curr. Biol. 19(17), 2009
PMID: 19906581
Tissue tectonics: morphogenetic strain rates, cell shape change and intercalation.
Blanchard GB, Kabla AJ, Schultz NL, Butler LC, Sanson B, Gorfinkiel N, Mahadevan L, Adams RJ., Nat. Methods 6(6), 2009
PMID: 19412170
Tissue morphogenesis coupled with cell shape changes.
Watanabe T, Takahashi Y., Curr. Opin. Genet. Dev. 20(4), 2010
PMID: 20677359
Unit operations of tissue development: epithelial folding
AUTHOR UNKNOWN, 2010
Primary invagination of the vegetal plate during sea urchin gastrulation
AUTHOR UNKNOWN, 1984
The cellular basis of epithelial morphogenesis. A review.
Fristrom D., Tissue Cell 20(5), 1988
PMID: 3068832
Epithelial morphogenesis in embryos: asymmetries, motors and brakes.
Quintin S, Gally C, Labouesse M., Trends Genet. 24(5), 2008
PMID: 18375008
Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension.
Butler LC, Blanchard GB, Kabla AJ, Lawrence NJ, Welchman DP, Mahadevan L, Adams RJ, Sanson B., Nat. Cell Biol. 11(7), 2009
PMID: 19503074
Molecular basis of morphogenesis during vertebrate gastrulation.
Wang Y, Steinbeisser H., Cell. Mol. Life Sci. 66(14), 2009
PMID: 19347571
Cortical forces in cell shape changes and tissue morphogenesis.
Rauzi M, Lenne PF., Curr. Top. Dev. Biol. 95(), 2011
PMID: 21501750
Tension and epithelial morphogenesis in Drosophila early embryos.
Lye CM, Sanson B., Curr. Top. Dev. Biol. 95(), 2011
PMID: 21501751
Epithelial polarity and morphogenesis.
St Johnston D, Sanson B., Curr. Opin. Cell Biol. 23(5), 2011
PMID: 21807488
Vertebrate intestinal endoderm development.
Spence JR, Lauf R, Shroyer NF., Dev. Dyn. 240(3), 2011
PMID: 21246663
Cell shape changes and the mechanism of inversion in Volvox.
Viamontes GI, Kirk DL., J. Cell Biol. 75(3), 1977
PMID: 925078
Integrated morphogenetic behavior of cell sheets Volvox as a model
AUTHOR UNKNOWN, 1982

AUTHOR UNKNOWN, 1998
A kinesin, invA, plays an essential role in volvox morphogenesis.
Nishii I, Ogihara S, Kirk DL., Cell 113(6), 2003
PMID: 12809605
Inversion in Volvox (Chlorophyceae)
AUTHOR UNKNOWN, 1977
Morphogenesis in Volvox: analysis of critical variables.
Viamontes GI, Fochtmann LJ, Kirk DL., Cell 17(3), 1979
PMID: 476832
Cytoplasmic bridges in Volvox and its relatives
AUTHOR UNKNOWN, 2005
Inversion in Volvox tertius: the effects of con A.
Ireland GW, Hawkins SE., J. Cell. Sci. 48(), 1981
PMID: 7276096
Some ultrastructural features of Volvox, with particular reference to the phenomenon of inversion
AUTHOR UNKNOWN, 1970
Volvox tertius Meyer. With notes on the two other British species of Volvox
AUTHOR UNKNOWN, 1938
Sexual and asexual differentiation in Volvox obversus (Shaw) Printz, strains Wd3 and Wd7
AUTHOR UNKNOWN, 1974
Sexual differentiation in Volvox aureus.
Darden WH Jr., J. Protozool. 13(2), 1966
PMID: 5953846
Le Volvox. Troisième Mémoire. Ontogénèse de la blastéa volvocéenne
AUTHOR UNKNOWN, 1923
Die ungeschlechtliche Entwicklung von Volvox
AUTHOR UNKNOWN, 1925
Volvox in South Africa
AUTHOR UNKNOWN, 1933
Induction and development of reproductive cells in the K-32 strains of Volvox rousseletii
AUTHOR UNKNOWN, 1970
Differentiation in Volvox
AUTHOR UNKNOWN, 1970
Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred from cladistic analysis based on morphological data
AUTHOR UNKNOWN, 1994
Cellular differentiation in Pleodorina californica
AUTHOR UNKNOWN, 1978
Colony development in Eudorina elegans (Chlorophyta, Volvocales)
AUTHOR UNKNOWN, 1977
Über die Veränderung der Koloniebildung von Eudorina elegans und Gonium pectorale unter dem Einfluss äußerer Bedingungen. IV. Mitt. der Untersuchungen über die Morphologie und Physiologie des Formwechsels der Phytomonadinen (Volvocales)
AUTHOR UNKNOWN, 1924
Colony formation and inversion in the green alga Eudorina elegans
AUTHOR UNKNOWN, 1977
On the morphology and cytology of Eudorina indica Iyengar
AUTHOR UNKNOWN, 1940
Inversion of the developing coenobium in Pandorina morum Bory
AUTHOR UNKNOWN, 1941
Embryogenesis and cell positioning in Platydorina caudata (Volvocaceae, Chlorophyta)
AUTHOR UNKNOWN, 2011
A morphologic and genetic study of Gonium pectorale
AUTHOR UNKNOWN, 1958
On cytoplasmic strands in Gonium pectorale (Volvocales)
AUTHOR UNKNOWN, 1965
Further studies on Volvox, with description of three new species
AUTHOR UNKNOWN, 1908
Zur Kenntnis der Entwicklungsgeschichte von Volvox
AUTHOR UNKNOWN, 1931
Zur Kenntnis der Entwicklungsgeschichte von Volvox
AUTHOR UNKNOWN, 1922
Volvox and associated algae from Kimberley
AUTHOR UNKNOWN, 1933
A morphological and cytological study of a new form of Volvox-I
AUTHOR UNKNOWN, 1945
Differentiation of reproductive cells in Volvox carteri.
Kochert G., J. Protozool. 15(3), 1968
PMID: 5703076
Control of differentiation in Volvox.
Starr RC., Symp Soc Dev Biol 29(), 1970
PMID: 4950154
Origin and evolution of the genera Pleodorina and Volvox (Volvocales)
AUTHOR UNKNOWN, 2003
Triassic origin and early radiation of multicellular volvocine algae.
Herron MD, Hackett JD, Aylward FO, Michod RE., Proc. Natl. Acad. Sci. U.S.A. 106(9), 2009
PMID: 19223580
Molecular phylogeny of the volvocine flagellates.
Larson A, Kirk MM, Kirk DL., Mol. Biol. Evol. 9(1), 1992
PMID: 1552843
Phylogenetic relationships within the colonial Volvocales (Chlorophyta) inferred from rbcL gene sequence data
AUTHOR UNKNOWN, 1995
Phylogenetic analysis of "Volvocacae" for comparative genetic studies.
Coleman AW., Proc. Natl. Acad. Sci. U.S.A. 96(24), 1999
PMID: 10570169
Reexamination of phylogenetic relationships within the colonial Volvocales (Chlorophyta): an analysis of atpB and rbcL gene sequences
AUTHOR UNKNOWN, 1999
Evolution of rbcL group IA introns and intron open reading frames within the colonial Volvocales (Chlorophyceae).
Nozaki H, Takahara M, Nakazawa A, Kita Y, Yamada T, Takano H, Kawano S, Kato M., Mol. Phylogenet. Evol. 23(3), 2002
PMID: 12099791
Evolution of reproductive development in the volvocine algae.
Hallmann A., Sex. Plant Reprod. 24(2), 2010
PMID: 21174128
A comparative study of the species of Volvox
AUTHOR UNKNOWN, 1944
Phylogenetic analysis of Yamagishiella and Platydorina (Volvocaceae, Chlorophyta) based on rbcL gene sequences
AUTHOR UNKNOWN, 1997
Morphology, molecular phylogeny and taxonomy of two new species of Pleodorina (Volvoceae, Chlorophyceae)
AUTHOR UNKNOWN, 2006

AUTHOR UNKNOWN, 1914
Flagellar development and regeneration in Volvox carteri (Chlorophyta)
AUTHOR UNKNOWN, 1986
Extracellular matrix and sex-inducing pheromone in Volvox.
Hallmann A., Int. Rev. Cytol. 227(), 2003
PMID: 14518551
Phylogenetic analysis of Eudorina species (Volvocaceae, Chlorophyta) based on rbcL gene sequences
AUTHOR UNKNOWN, 1997
Resolving the first steps to multicellularity.
Sachs JL., Trends Ecol. Evol. (Amst.) 23(5), 2008
PMID: 18375012
Evolution of developmental programs in volvox (chlorophyta)
Herron MD, Desnitskiy AG, Michod RE., J. Phycol. 46(2), 2010
PMID: IND44348078
Stable nuclear transformation of Gonium pectorale.
Lerche K, Hallmann A., BMC Biotechnol. 9(), 2009
PMID: 19591675
THE FLAGELLAR PHOTORESPONSE IN VOLVOX SPECIES (VOLVOCACEAE, CHLOROPHYCEAE)1.
Solari CA, Drescher K, Goldstein RE., J. Phycol. 47(3), 2011
PMID: 27021987
How we are shaped: the biomechanics of gastrulation.
Keller R, Davidson LA, Shook DR., Differentiation 71(3), 2003
PMID: 12694202
Mesoderm migration in the Xenopus gastrula.
Winklbauer R, Nagel M, Selchow A, Wacker S., Int. J. Dev. Biol. 40(1), 1996
PMID: 8735942
SAG-Sammlung von Algenkulturen at the University of Göttingen, Catalogue of Strains 1994
AUTHOR UNKNOWN, 1994
Artificial media for fresh-water algae: problems and suggestions
AUTHOR UNKNOWN, 1959
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