Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta
Open accessAbstract
It has been posited that animal development evolved from pre-existing mechanisms for regulating cell differentiation in the single celled and colonial ancestors of animals. Although the progenitors of animals cannot be studied directly, insights into their cell biology may be gleaned from comparisons between animals and their closest living relatives, the choanoflagellates. We report here on the life history, cell differentiation and intercellular interactions in the colony-forming choanoflagellate Salpingoeca rosetta. In response to diverse environmental cues, S. rosetta differentiates into at least five distinct cell types, including three solitary cell types (slow swimmers, fast swimmers, and thecate cells) and two colonial forms (rosettes and chains). Electron microscopy reveals that cells within colonies are held together by a combination of fine intercellular bridges, a shared extracellular matrix, and filopodia. In addition, we have discovered that the carbohydrate-binding protein wheat germ agglutinin specifically stains colonies and the slow swimmers from which they form, showing that molecular differentiation precedes multicellular development. Together, these results help establish S. rosetta as a model system for studying simple multicellularity in choanoflagellates and provide an experimental framework for investigating the origin of animal multicellularity and development.
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Cells in colonies of Salpingoeca rosetta can remain connected via the extracellular matrix, filopodia, and intercellular bridges.
“Cells in colonies of Salpingoeca rosetta (and other choanoflagellates) can remain connected in various ways including via the extracellular matrix, filopodia, and intercellular bridges (Dayel et al. , 2011).”
From The origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution (2017) · cites this paper as Dayel et al., 2011
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Cites
The Extracellular Matrix: Not Just Pretty Fibrils
Hynes, R. O. (2009) · Science · doi:10.1126/science.1176009 · Cited by 3,527 · see citing works
The Evolution of Individuality
Buss, L. W. (1988) · Princeton University Press eBooks · doi:10.1515/9781400858712 · Cited by 1,389 · see citing works
Cooperation and Competition in the Evolution of ATP-Producing Pathways
Pfeiffer, T., Schuster, S., & Bonhoeffer, S. (2001) · Science · doi:10.1126/science.1058079 · Cited by 1,365 · see citing works
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139 · see citing works
Self-citationFrom DNA to diversity: molecular genetics and the evolution of animal design
Carroll, S., Grenier, J., & Weatherbee, S. D. (2002) · Choice Reviews Online · doi:10.5860/choice.39-5182 · Cited by 986 · see citing works
The evolution of individuality
Raff, R. A. (1988) · Cell · doi:10.1016/0092-8674(88)90064-5 · Cited by 715 · see citing works
The Molecular Requirements for Cytokinesis
Glotzer, M. (2005) · Science · doi:10.1126/science.1096896 · Cited by 710 · see citing works
Ramı́rez-Weber, F.-A., & Kornberg, T. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80771-0 · Cited by 614 · see citing works
The Unicellular Ancestry of Animal Development
King, N. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.010 · Cited by 482 · see citing works
Self-citationThe evolution of signalling pathways in animal development
Pires-daSilva, A., & Sommer, R. J. (2003) · Nature Reviews Genetics · doi:10.1038/nrg977 · Cited by 466 · see citing works
Evolution of Key Cell Signaling and Adhesion Protein Families Predates Animal Origins
King, N., Hittinger, C. T., & Carroll, S. B. (2003) · Science · doi:10.1126/science.1083853 · Cited by 424 · see citing works
Self-citationLaubichler, M. D. (2003) · Max Planck Institute for Plasma Physics · Cited by 387 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · cited 6× · see citing works
“…choanocytes has long been interpreted as evidence of a close relationship between choanoflagellates and animals (James-Clark, 1867; Maldonado, 2004; Nielsen, 2008) and modern phylogenetic analyses now demonstrate that choanoflagellates are the closest known sister group of animals (Carr et al.,…”
BackgroundInfluentialGlotzer, M. (2001) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.17.1.351 · Cited by 342 · see citing works
Evo-Devo: Variations on Ancestral Themes
Robertis, E. M. D. (2008) · Cell · doi:10.1016/j.cell.2008.01.003 · Cited by 335 · see citing works
Evolution of individuality during the transition from unicellular to multicellular life
Michod, R. E. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701489104 · Cited by 334 · see citing works
The Protistan Origins of Animals and Fungi
Steenkamp, E. T., Wright, J., & Baldauf, S. L. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj011 · Cited by 307 · see citing works
A Phylogenomic Investigation into the Origin of Metazoa
Ruiz‐Trillo, I., Roger, A. J., Burger, G., Gray, M. W., & Lang, B. F. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn006 · Cited by 269 · see citing works
Ancient origin of the integrin-mediated adhesion and signaling machinery
Sebé-Pedrós, A., Roger, A. J., Lang, B. F., King, N., & Ruiz‐Trillo, I. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002257107 · Cited by 250 · see citing works
Self-citationSpecificity of Drosophila Cytonemes for Distinct Signaling Pathways
Roy, S., Hsiung, F., & Kornberg, T. B. (2011) · Science · doi:10.1126/science.1198949 · Cited by 241 · see citing works
The Premetazoan Ancestry of Cadherins
Sigg, M. A., & King, N. (2008) · Science · doi:10.1126/science.1151084 · Cited by 239 · see citing works
Self-citationHigh‐pressure freezing of cell suspensions in cellulose capillary tubes
Hohenberg, H., Mannweiler, K., & Müller, M. (1994) · Journal of Microscopy · doi:10.1111/j.1365-2818.1994.tb04785.x · Cited by 234 · see citing works
(2004) · Choice Reviews Online · doi:10.5860/choice.42-2217 · Cited by 214 · see citing works
Choanoflagellates, choanocytes, and animal multicellularity
Maldonado, M. (2004) · Invertebrate Biology · doi:10.1111/j.1744-7410.2004.tb00138.x · Cited by 207 · see citing works
The origins of multicellularity: a multi-taxon genome initiative
Ruiz‐Trillo, I., Burger, G., Holland, P. W. H., King, N., Lang, B. F., Roger, A. J., & Gray, M. W. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.01.005 · Cited by 206 · see citing works
Self-citationMolecular phylogeny of choanoflagellates, the sister group to Metazoa
Carr, M., Leadbeater, B. S. C., Hassan, R., Nelson, M., & Baldauf, S. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801667105 · Cited by 205 · see citing works
Haglund, K., Nezis, I. P., & Stenmark, H. (2011) · Communicative & Integrative Biology · doi:10.4161/cib.13550 · Cited by 203 · see citing works
Haglund, K., Nezis, I. P., & Stenmark, H. (2011) · PubMed · doi:10.4161/cib.4.1.13550 · Cited by 166 · see citing works
Multicellular development in a choanoflagellate
Fairclough, S. R., Dayel, M. J., & King, N. (2010) · Current Biology · doi:10.1016/j.cub.2010.09.014 · Cited by 163 · see citing works
Self-citationFalk, P., Roth, K. A., & Gordon, J. I. (1994) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1994.266.6.g987 · Cited by 152 · see citing works
The origin of Metazoa: a transition from temporal to spatial cell differentiation
Mikhailov, K. V., Константинова, А. В., Nikitin, M. A., Troshin, P. V., Rusin, L. Y., Lyubetsky, V., Panchin, Y. V., Mylnikov, A. P., Moroz, L. L., Kumar, S., et al. (2009) · BioEssays · doi:10.1002/bies.200800214 · Cited by 151 · see citing works
Conversion of midbodies into germ cell intercellular bridges
Greenbaum, M. P., Ma, L., & Matzuk, M. M. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.02.025 · Cited by 137 · see citing works
Theurkauf, W. E., & Hazelrigg, T. I. (1998) · Development · doi:10.1242/dev.125.18.3655 · Cited by 135 · see citing works
Midbodies and phragmoplasts: analogous structures involved in cytokinesis
Otegui, M. S., Verbrugghe, K. J. C., & Skop, A. R. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2005.06.003 · Cited by 127 · see citing works
Hibberd, D. J. (1975) · Journal of Cell Science · doi:10.1242/jcs.17.1.191 · Cited by 125 · see citing works
Chen, E. Y., Fujinaga, M., & Giaccia, A. J. (1999) · Teratology · doi:10.1002/(sici)1096-9926(199910)60:4 · Cited by 119 · see citing works
Life-history and ultrastructure of a new marine species of Proterospongia (Choanoflagellida)
Leadbeater, B. S. C. (1983) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315400049857 · Cited by 118 · see citing works
Isolation and initial characterization of the mammalian midbody.
Mullins, J. M., & McIntosh, J. R. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.94.3.654 · Cited by 113 · see citing works
Cytokinesis in HeLa: Post-telophase delay and microtubule-associated motility
Byers, B., & Abramson, D. H. (1968) · PROTOPLASMA · doi:10.1007/bf01255868 · Cited by 107 · see citing works
(2018) · CRC Press eBooks · doi:10.1201/9781351032742-11 · Cited by 104 · see citing works
The hydrodynamics of filter feeding in choanoflagellates
Pettitt, M. E., Orme, B., Blake, J. R., et al. (2002) · European Journal of Protistology · doi:10.1078/0932-4739-00854 · Cited by 74 · see citing works
Developmental studies on the loricate choanoflagellateStephanoeca diplocostata ellis
Leadbeater, B. S. C. (1979) · PROTOPLASMA · doi:10.1007/bf01281442 · Cited by 74 · see citing works
The Significance of Syncytial Tissues for the Position of the Hexactinellida in the Metazoa
Leys, S. P. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.19 · Cited by 71 · see citing works
Haeckel, E. (1874) · Journal of Cell Science · doi:10.1242/jcs.s2-14.54.142 · Cited by 70 · see citing works
Germline cyst formation and incomplete cytokinesis during Drosophila melanogaster oogenesis
Ong, S., & Tan, C. L. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.018 · Cited by 66 · see citing works
Baluška, F., Volkmann, D., & Barlow, P. W. (2007) · Cited by 64 · see citing works
Factors Influencing the Plate Method for Determining Abundance of Bacteria in Sea Water.
Carlucci, A. F., & Pramer, D. (1957) · Experimental Biology and Medicine · doi:10.3181/00379727-96-23487 · Cited by 58 · see citing works
James‐Clark, H. (1868) · Annals and Magazine of Natural History · doi:10.1080/00222936808695688 · Cited by 53 · see citing works
James‐Clark, H. (1868) · Annals and Magazine of Natural History · doi:10.1080/00222936808695657 · Cited by 42 · see citing works
Leadbeater, B. S. C. (1977) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315400021767 · Cited by 38 · see citing works
Cytoplasmic Bridges in Volvox and Its Relatives
Hoops, H. J., Nishii, I., & Kirk, D. L. (2007) · Springer eBooks · doi:10.1007/978-0-387-46957-7_4 · Cited by 35 · see citing works
Clark, H. J. (1866) · American Journal of Science · doi:10.2475/ajs.s2-42.126.320 · Cited by 34 · see citing works
Intercellular bridges and factors determining their patterns in the grasshopper testis
Carlson, J. G., & Handel, M. A. (1988) · Journal of Morphology · doi:10.1002/jmor.1051960206 · Cited by 26 · see citing works
Ramoino, P., Fronte, P., Fato, M., et al. (2001) · European Biophysics Journal · doi:10.1007/s002490100166 · Cited by 24 · see citing works
A Survey of Lectin Binding in Paramecium1
Allen, R. D., Ueno, M. S., & Fok, A. K. (1988) · The Journal of Protozoology · doi:10.1111/j.1550-7408.1988.tb04117.x · Cited by 24 · see citing works
Starting and Maintaining Monosiga brevicollis CulturesPreprint
King, N., Young, S. L., Sigg, M. A., Carr, M., & Leadbeater, B. S. C. (2009) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5148 · Cited by 21 · see citing works
Self-citationFollicle cell bridges in the mosquito ovary: syncytia formation and bridge morphology
Fiil, A. (1978) · Journal of Cell Science · doi:10.1242/jcs.31.1.137 · Cited by 21 · see citing works
James‐Clark, H. (1867) · Annals and Magazine of Natural History · doi:10.1080/00222936708679703 · Cited by 21 · see citing works
Developmental studies on the loricate choanoflagellateStephanoeca diplocostata ellis
Leadbeater, B. S. C. (1985) · PROTOPLASMA · doi:10.1007/bf01276261 · Cited by 18 · see citing works
Notes on the Choanoflagellate, Codosiga botrytis, Ehrbg
Lapage, G. (1925) · Journal of Cell Science · doi:10.1242/jcs.s2-69.275.471 · Cited by 16 · see citing works
LUEKKEN, W. W., Breer, H., & HARTKKEMEYER, M. (1981) · The Journal of Protozoology · doi:10.1111/j.1550-7408.1981.tb05312.x · Cited by 16 · see citing works
The immature part of the testis in Salamandra salamandra (L.) (amphibia, urodela).
Schindelmeiser, J., Greven, H., & Bergmann, M. (1983) · Archivum histologicum japonicum · doi:10.1679/aohc.46.159 · Cited by 13 · see citing works
Elastic Registration with Partial Data
Periaswamy, S., & Farid, H. (2003) · Lecture notes in computer science · doi:10.1007/978-3-540-39701-4_11 · Cited by 11 · see citing works
Lectin-binding glycoconjugates in Paramecium primaurelia : changes with cellular age and starvation
Ramoino, P. (1997) · Histochemistry and Cell Biology · doi:10.1007/s004180050117 · Cited by 11 · see citing works
Affolter, M., & Basler, K. (2011) · Science · doi:10.1126/science.1205971 · Cited by 8 · see citing works
Ultrastructure of Goat Testes: Intercellular Bridge between Germ Cells.
KOJIMA, Y. (1992) · Journal of Veterinary Medical Science · doi:10.1292/jvms.54.213 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- James-Clark H 1868 On the spongiae ciliatae as infusoria flagellata; or observations on the structure, animality, and relationship of Leucosolenia botryoides Annals and Magazine of Natural History 1 133 142 188 215 250 264
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Schuettengruber, B., Bourbon, H.-M., Di Croce, L., & Cavalli, G. (2017) · Cell · doi:10.1016/j.cell.2017.08.002 · Cited by 1,094 · see citing works
Alegado, R. A., Brown, L. W., Cao, S., Dermenjian, R. K., Zuzow, R., Fairclough, S. R., Clardy, J., & King, N. (2012) · eLife · doi:10.7554/elife.00013 · Cited by 249 · see citing works
Self-citationThe origin of the animals and a 'Savannah' hypothesis for early bilaterian evolution
Budd, G. E., & Jensen, S. (2017) · Biological Reviews · doi:10.1111/brv.12239 · Cited by 240 · see citing works
“However one good reason for concluding that stem-group animals were benthic is their large size: such benthic colonies – probably also with the ability to (at least facultatively) produce differentiated cells (as do choanoflagellates, albeit not in colonies; Dayel et al., 2011) – might best be considered as competitor…”
BackgroundThe Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196 · see citing works
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- Authors
- Dayel, M. J., Alegado, R. A., Fairclough, S. R., Levin, T. C., Nichols, S. A., McDonald, K., & King, N.
- Affiliations
- University of California, Berkeley (US)
- Corresponding author
- King, Nicole
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 357
- Issue
- 1
- Pages
- 73-82
- ISSN
- 0012-1606 (ISSN-L)
- PMC
- PMC3156392
- OpenAlex
- W2007399351
- Cited by
- 277
- References
- 66
- Citations by year
- 2026: 15 · 2025: 23 · 2024: 16 · 2023: 33 · 2022: 21 · 2021: 26 · 2020: 16 · 2019: 17 · 2018: 12 · 2017: 13 · 2016: 19 · 2015: 15 · 2014: 18 · 2013: 18 · 2012: 14
- FWCI
- 11.26
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIGMS/NIH (GM089977)
- Gordon and Betty Moore Foundation Marine Microbiology Initiative
- Miller Institute for Basic Research in Science
- NIH National Research Service Award and Fellowship (5F32GM086054)
- NIH Training (T32 HG00047)
- NSF Graduate Research Fellowship
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Salpingoeca rosetta, choanoflagellates, cell differentiation, morphogenesis, multicellularity, animal evolution, cell-cell interactions, rosettes, chains, extracellular matrix, filopodia, intercellular bridges, wheat germ agglutinin, life history
- MeSH terms
- Animals, Cell Differentiation, Microscopy, Electron, Scanning, Morphogenesis, Receptors, Cell Surface, Choanoflagellata
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