Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Höhn S, Hallmann A (2016)
BMC Developmental Biology 16(1): 35.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 7.56 MB
Abstract / Bemerkung
Background The multicellular volvocine alga Pleodorina is intermediate in organismal complexity between its unicellular relative, Chlamydomonas, and its multicellular relative, Volvox, which shows complete division of labor between different cell types. The volvocine green microalgae form a group of genera closely related to the genus Volvox within the order Volvocales (Chlorophyta). Embryos of multicellular volvocine algae consist of a cellular monolayer that, depending on the species, is either bowl-shaped or comprises a sphere. During embryogenesis, multicellular volvocine embryos turn their cellular monolayer right-side out to expose their flagella. This process is called ‘inversion’ and serves as simple model for epithelial folding in metazoa. While the development of spherical Volvox embryos has been the subject of detailed studies, the inversion process of bowl-shaped embryos is less well understood. Therefore, it has been unclear how the inversion of a sphere might have evolved from less complicated processes. Results In this study we characterized the inversion of initially bowl-shaped embryos of the 64- to 128-celled volvocine species Pleodorina californica. We focused on the movement patterns of the cell sheet, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. The development of living embryos was recorded using time-lapse light microscopy. Moreover, fixed and sectioned embryos throughout inversion and at successive stages of development were analyzed by light and transmission electron microscopy. We generated three-dimensional models of the identified cell shapes including the localization of CBs. Conclusions In contrast to descriptions concerning volvocine embryos with lower cell numbers, the embryonic cells of P. californica undergo non-simultaneous and non-uniform cell shape changes. In P. californica, cell wedging in combination with a relocation of the CBs to the basal cell tips explains the curling of the cell sheet during inversion. In volvocine genera with lower organismal complexity, the cell shape changes and relocation of CBs are less pronounced in comparison to P. californica, while they are more pronounced in all members of the genus Volvox. This finding supports an increasing significance of the temporal and spatial regulation of cell shape changes and CB relocations with both increasing cell number and organismal complexity during evolution of differentiated multicellularity.
Cell-cell connections Cell sheet bending Cell sheet folding Cytoplasmic bridges Evolution Green algae Inversion Morphogenesis Multicellularity Volvocales
BMC Developmental Biology
Page URI


Höhn S, Hallmann A. Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina. BMC Developmental Biology. 2016;16(1): 35.
Höhn, S., & Hallmann, A. (2016). Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina. BMC Developmental Biology, 16(1), 35. doi:10.1186/s12861-016-0134-9
Höhn, Stephanie, and Hallmann, Armin. 2016. “Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina”. BMC Developmental Biology 16 (1): 35.
Höhn, S., and Hallmann, A. (2016). Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina. BMC Developmental Biology 16:35.
Höhn, S., & Hallmann, A., 2016. Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina. BMC Developmental Biology, 16(1): 35.
S. Höhn and A. Hallmann, “Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina”, BMC Developmental Biology, vol. 16, 2016, : 35.
Höhn, S., Hallmann, A.: Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina. BMC Developmental Biology. 16, : 35 (2016).
Höhn, Stephanie, and Hallmann, Armin. “Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina”. BMC Developmental Biology 16.1 (2016): 35.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
Dieses Objekt ist durch das Urheberrecht und/oder verwandte Schutzrechte geschützt. [...]
Access Level
OA Open Access
Zuletzt Hochgeladen
MD5 Prüfsumme

4 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
The Origin of Animal Multicellularity and Cell Differentiation.
Brunet T, King N., Dev Cell 43(2), 2017
PMID: 29065305

108 References

Daten bereitgestellt von Europe PubMed Central.

Timing the origins of multicellular eukaryotes through phylogenomics and relaxed molecular clock analyses
Sharpe SC, Eme L, Brown MW, Roger AJ., 2015
Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago.
El Albani A, Bengtson S, Canfield DE, Bekker A, Macchiarelli R, Mazurier A, Hammarlund EU, Boulvais P, Dupuy JJ, Fontaine C, Fursich FT, Gauthier-Lafaye F, Janvier P, Javaux E, Ossa FO, Pierson-Wickmann AC, Riboulleau A, Sardini P, Vachard D, Whitehouse M, Meunier A., Nature 466(7302), 2010
PMID: 20596019
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

Kirk DL., 1998
Volvox as a model system for studying the ontogeny and phylogeny of multicellularity and cellular differentiation
Kirk DL., 2000
Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri.
Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, Ferris P, Kuo A, Mitros T, Fritz-Laylin LK, Hellsten U, Chapman J, Simakov O, Rensing SA, Terry A, Pangilinan J, Kapitonov V, Jurka J, Salamov A, Shapiro H, Schmutz J, Grimwood J, Lindquist E, Lucas S, Grigoriev IV, Schmitt R, Kirk D, Rokhsar DS., Science 329(5988), 2010
PMID: 20616280
Evolution of reproductive development in the volvocine algae.
Hallmann A., Sex. Plant Reprod. 24(2), 2010
PMID: 21174128

Sleigh MA., 1989
A review on the evolution of development in Volvox: Morphological and physiological aspects
Desnitski AG., 1995
Die Zelldifferenzierung bei Pleodorina californica Shaw und die Organisation der Phytomonadinenkolonien
Gerisch G., 1959
The development of cytoplasmic bridges in Volvox aureus
Bisalputra T, Stein JR., 1966
Colony development in Eudorina elegans (Chlorophyta, Volvocales)
Gottlieb B, Goldstein ME., 1977
Plasmodesmata in algae and fungi
Marchant HJ., 1976
Colony formation and inversion in the green alga Eudorina elegans
Marchant HJ., 1977

Pleodorina, a new genus of the Volvocinae
Shaw WR., 1894
Cellular differentiation in Pleodorina californica
Kikuchi K., 1978
Ultrastructure of the extracellular matrix and taxonomy of Eudorina, Pleodorina and Yamagishiella gen. nov. (Volvocaceae, Chlorophyta)
Nozaki H, Kuroiwa T., 1992

Kofoid CA., 1899
Embryogenesis and cell positioning in Platydorina caudata (Volvocaceae, Chlorophyta)
Iida H, Nishii I, Inouye I., 2011

Müller OF., 1774
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)
Hartmann M., 1924
A morphologic and genetic study of Gonium pectorale
Stein JR., 1958
On cytoplasmic strands in Gonium pectorale (Volvocales)
Stein JR., 1965

Lamouroux JV, Bory JBGM, Deslongschamps E., 1824
Freshwater algae of the Lismore district: with an appendix on the algal fungi and Schizomycetes
Playfair GI., 1915
Volvulina compacta sp. nov. (Volvocaceae, Chlorophyta) from Nepal
Nozaki H, Kuroiwa T., 1990

Differentiation of reproductive cells in Volvox carteri.
Kochert G., J. Protozool. 15(3), 1968
PMID: 5703076
Control of differentiation in Volvox
Starr RC., 1970
Germ-soma differentiation in volvox.
Kirk DL., Dev. Biol. 238(2), 2001
PMID: 11784005
Evolution of developmental programs in volvox (chlorophyta)
Herron MD, Desnitskiy AG, Michod RE., J. Phycol. 46(2), 2010
PMID: IND44348078
Inversion of the developing coenobium in Pandorina morum Bory
Taft CE., 1941
Cell shape changes and the mechanism of inversion in Volvox.
Viamontes GI, Kirk DL., J. Cell Biol. 75(3), 1977
PMID: 925078
Two multicellular motile green algae, Volvulina Playfair and Astrephomene, a new genus
Pocock MA., 1953
Mitosis, cytokinesis and colony formation in the colonial green algae Astrephomene gubernaculifera
Hoops HJ, Floyd GL., 1982
Morphology and taxonomy of two species of Astrephomene (Chlorophyta, Volvocales) in Japan
Nozaki H., 1983
Volvox and associated algae from Kimberley
Pocock MA., 1933
Volvox in South Africa
Pocock MA., 1933
Inversion in Volvox (Chlorophyceae)
Kelland JL., 1977
Morphogenesis in Volvox: analysis of critical variables.
Viamontes GI, Fochtmann LJ, Kirk DL., Cell 17(3), 1979
PMID: 476832
Integrated morphogenetic behavior of cell sheets: Volvox as a model
Kirk DL, Viamontes GI, Green KJ, Bryant JL., 1982
A kinesin, invA, plays an essential role in volvox morphogenesis.
Nishii I, Ogihara S, Kirk DL., Cell 113(6), 2003
PMID: 12809605
Dynamics of a Volvox embryo turning itself inside out.
Hohn S, Honerkamp-Smith AR, Haas PA, Trong PK, Goldstein RE., Phys. Rev. Lett. 114(17), 2015
PMID: 25978266
Resolving the first steps to multicellularity.
Sachs JL., Trends Ecol. Evol. (Amst.) 23(5), 2008
PMID: 18375012
Stable nuclear transformation of Gonium pectorale.
Lerche K, Hallmann A., BMC Biotechnol. 9(), 2009
PMID: 19591675
The bending of cell sheets--from folding to rolling.
Keller R, Shook D., BMC Biol. 9(), 2011
PMID: 22206439
How we are shaped: the biomechanics of gastrulation.
Keller R, Davidson LA, Shook DR., Differentiation 71(3), 2003
PMID: 12694202

Stern CD., 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.
Zartman JJ, Shvartsman SY., Annu Rev Chem Biomol Eng 1(), 2010
PMID: 22432580
Apical constriction: a cell shape change that can drive morphogenesis.
Sawyer JM, Harrell JR, Shemer G, Sullivan-Brown J, Roh-Johnson M, Goldstein B., Dev. Biol. 341(1), 2009
PMID: 19751720
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
Zur Kenntnis der Entwicklungsgeschichte von Volvox
Kuschakewitsch S., 1931
Zur Kenntnis der Entwicklungsgeschichte von Volvox
Kuschakewitsch S., 1922
A morphological and cytological study of a new form of Volvox-I
Metzner J., 1945
Cytoplasmic bridges in Volvox and its relatives
Hoops HJ, Nishii I, Kirk DL., 2005
Extracellular matrix and sex-inducing pheromone in Volvox.
Hallmann A., Int. Rev. Cytol. 227(), 2003
PMID: 14518551
Induction and development of reproductive cells in the K-32 strains of Volvox rousseletii
McCracken MD, Starr RC., 1970
The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity.
Hanschen ER, Marriage TN, Ferris PJ, Hamaji T, Toyoda A, Fujiyama A, Neme R, Noguchi H, Minakuchi Y, Suzuki M, Kawai-Toyooka H, Smith DR, Sparks H, Anderson J, Bakaric R, Luria V, Karger A, Kirschner MW, Durand PM, Michod RE, Nozaki H, Olson BJ., Nat Commun 7(), 2016
PMID: 27102219
The Chlamydomonas genome reveals the evolution of key animal and plant functions.
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR., Science 318(5848), 2007
PMID: 17932292
The simplest integrated multicellular organism unveiled.
Arakaki Y, Kawai-Toyooka H, Hamamura Y, Higashiyama T, Noga A, Hirono M, Olson BJ, Nozaki H., PLoS ONE 8(12), 2013
PMID: 24349103

Oltmanns F., 1904

West GS, Fritsch FE., 1927
Chlorophyta I: Phytomonadina (Band 9)
Ettl H., 1983
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
Nozaki H, Itoh M, Sano R, Uchida H, Watanabe MM, Kuroiwa T., 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
Nozaki H, Ohta N, Takano H, Watanabe MM., 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
SAG-Sammlung von Algenkulturen at the University of Göttingen, Catalogue of Strains 1994
Schlösser UG., 1994
Sammlung von Algenkulturen
Schlösser UG., 1982

Andersen RA., 2005
Selection of some native microalgal strains for possibility of bio - oil production in Thailand
Janta K, Pekkoh J, Tongsiri S, Pumas C, Peerapornpisal Y., 2013
Phylogenetic analysis of Eudorina species (Volvocaceae, Chlorophyta) based on rbcL gene sequences
Nozaki H, Ito M, Uchida H, Watanabe MM, Kuroiwa T., 1997
Origin and evolution of the genera Pleodorina and Volvox (Volvocales)
Nozaki H., 2003

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 27733125
PubMed | Europe PMC

Suchen in

Google Scholar