The simplicity of metazoan cell lineages

Azevedo, Ricardo B. R.; Lohaus, Rolf; Braun, Volker; Gumbel, Markus; Umamaheshwar, Muralikrishna; Agapow, Paul‐Michael; Houthoofd, Wouter; Platzer, Ute; Borgonie, Gaëtan; Meinzer, Hans-Peter; Leroi, Armand M.

doi:10.1038/nature03178

Cited by 44 publications

(71 citation statements)

References 23 publications

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“…This finding is consistent with the hypothesis that selection for decreased cell lineage complexity played a major role in the evolution of metazoan ontogenies (17,37). Although Caenorhabditis elegans had been considered a prime example of mosaic development (38), modern investigations have demonstrated that its ontogeny is based on principles of regional specification rather than clonal organization of cell lineage (39,40).…”

Section: Resultssupporting

confidence: 82%

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Embryology of a planktonic tunicate reveals traces of sessility

Stach

Winter

Bouquet³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

100

102

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A key problem in understanding deuterostome evolution has been the origin of the chordate body plan. A biphasic life cycle with a sessile adult and a free-swimming larva is traditionally considered ancestral in chordates with subsequent neotenic loss of the sessile adult stage. Molecular phylogenies challenged this view, suggesting that the primitive life cycle in chordates was entirely free-living as in modern day larvaceans. Here, we report the precise cell lineage and fate map in the normal embryo of the larvacean Oikopleura dioica , using 4D microscopy technique and transmission electron microscopy. We document the extraordinary rapidity of cleavage and morphogenetic events until hatching and demonstrate that—compared with ascidians—fate restriction occurs considerably earlier in O. dioica and that clonal organization of the cell lineage is more tightly coupled to tissue fate. We show that epidermal cells in the trunk migrate through 90°, reminiscent of events in ascidian metamorphosis and that the axis of bilateral symmetry in the tail rotates in relation to the trunk. We argue that part of the tail muscle cells are ectomesodermal, because they are more closely associated with prospective epidermis than with other tissues in the cell lineage. Cladistic comparison with other deuterostomes suggests that these traits are derived within tunicates strengthening the hypothesis that the last common ancestor of tunicates had a sessile adult and thus support traditional morphology-derived scenarios. Our results allow hypothesizing that molecular developmental mechanisms known from ascidian models are restricted to fewer, yet identifiable, cells in O. dioica .

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Section: Resultssupporting

confidence: 82%

“…The present study reveals the simplest cell lineage (in the sense of ref. 17) known from metazoans and amounts to a major step forward in tracing evolutionary changes in cellular mechanisms that will ultimately facilitate understanding molecular mechanisms correlated with drastic changes in life history strategies.…”

mentioning

confidence: 99%

Embryology of a planktonic tunicate reveals traces of sessility

Stach

Winter

Bouquet³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

100

102

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“…We can test whether sequestered germlines reduce selfish cell lineages by drawing propagules from a pre-defined region near the centre of the plate. We might even test more complex body plans where different lineages grow to different degrees [20] by shifting from a circular plate to arenas where growth is channelled in desired directions and amounts.…”

Section: General Methodologymentioning

confidence: 99%

Experimental evolution of multicellularity using microbial pseudo-organisms

Queller

Strassmann

2013

Biol. Lett.

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In a major evolutionary transition to a new level of organization, internal conflicts must be controlled before the transition can truly be successful. One such transition is that from single cells to multicellularity. Conflicts among cells in multicellular organisms can be greatly reduced if they consist of genetically identical clones. However, mutations to cheaters that experience one round of within-individual selection could still be a problem, particularly for certain life cycles. We propose an experimental evolution method to investigate this issue, using micro-organisms to construct multicellular pseudo-organisms, which can be evolved under different artificial life cycles. These experiments can be used to test the importance of various life cycle features in maintaining cooperation. They include structured reproduction, in which small propagule size reduces within-individual genetic variation. They also include structured growth, which increases local relatedness within individual bodies. Our method provides a novel way to test how different life cycles favour cooperation, even for life cycles that do not exist.

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“…Our hypothesis is that, while a traditional Boolean model is general, our tweaked (meta-Boolean) model is biologically plausible, and has several features that makes it useful in the context of currently used models. In particular, it can be used to investigate whether the inclusion of cell-cell signaling reduces the complexity of the resulting lineage descriptions, which would enable a more detailed analysis of, e.g., the suggestion of Azevedo et al (2005).…”

Section: Modelling the Caenorhabditis Elegans Cell Lineagementioning

confidence: 99%

“…Finally, Azevedo et al (2005) use a Boolean rule-based model to measure cell lineage complexity. They compare the complexity of the C. elegans lineage and three other metazoan lineages, and also use the measure on random lineages.…”

Section: Modelling the Caenorhabditis Elegans Cell Lineagementioning

confidence: 99%

Modelling cell lineage using a meta-Boolean tree model with a relation to gene regulatory networks

Larsson

Wadströmer

Hermanson

et al. 2011

Journal of Theoretical Biology

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. Modelling cell lineage using a meta-Boolean tree model with a relation to Gene Regulatory Networks. Journal of Theoretical Biology, Elsevier, 2010, 268 (1) This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.Modelling cell lineage using a meta-Boolean tree model with a relation to Gene Regulatory Networks AbstractA cell lineage is the ancestral relationship between a group of cells that originate from a single founder cell. For example, in the embryo of the nematode Caenorhabditis elegans an invariant cell lineage has been traced, and with this information at hand it is possible to theoretically model the emergence of different cell types in the lineage, starting from the single fertilized egg. In this report we outline a modelling technique for cell lineage trees, which can be used for the C. elegans embryonic cell lineage but also extended to other lineages. The model takes into account both cell-intrinsic (transcription factor-based) and -extrinsic (extracellular) factors as well as synergies within and between these two types of factors. The model can faithfully recapitulate the entire C. elegans cell lineage, but is also general, i.e. it can be applied to describe any cell lineage. We show that synergy between factors, as well as the use of extrinsic factors, drastically reduce the number of regulatory factors needed for recapitulating the lineage. The model gives indications regarding co-variation of factors, number of involved genes and where in the cell lineage tree that asymmetry might be controlled by external influence. Furthermore, the model is able to emulate other (Boolean, discrete and differential-equation-based) models. As an example, we show that the model can be translated to the language of a previous linear sigmoid-limited concentration-based model (Geard and Wiles, 2005). This means that this latter model also can exhibit synergy effects, and also that the cumbersome iterative technique for parameter estimation previously used is no longer needed. In conclusion, the proposed model is general and simple to use, can be mapped onto other models to extend and simplify their use, and can also be used to indicate where synergy and external influence would reduce the complexity of the regulatory process.

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The simplicity of metazoan cell lineages

Cited by 44 publications

References 23 publications

Embryology of a planktonic tunicate reveals traces of sessility

Embryology of a planktonic tunicate reveals traces of sessility

Experimental evolution of multicellularity using microbial pseudo-organisms

Modelling cell lineage using a meta-Boolean tree model with a relation to gene regulatory networks

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