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The role of GlsA in the evolution of asymmetric cell division in the green alga Volvox carteri

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Abstract

Volvox carteri, a green alga in the order Volvocales, contains two completely differentiated cell types, small motile somatic cells and large reproductive cells called gonidia, that are set apart from each other during embryogenesis by a series of visibly asymmetric cell divisions. Mutational analysis has revealed a class of genes (gonidialess, gls) that are required specifically for asymmetric divisions in V. carteri, but that are dispensable for symmetric divisions. Previously we cloned one of these genes, glsA, and showed that it encodes a chaperone-like protein (GlsA) that has close orthologs in a diverse set of eukaryotes, ranging from fungi to vertebrates and higher plants. In the present study we set out to explore the role of glsA in the evolution of asymmetric division in the volvocine algae by cloning and characterizing a glsA ortholog from one of the simplest members of the group, Chlamydomonas reinhardtii, which does not undergo asymmetric divisions. This ortholog (which we have named gar1, for glsA related) is predicted to encode a protein that is 70% identical to GlsA overall, and that is most closely related to GlsA in the same domains that are most highly conserved between GlsA and its other known orthologs. We report that a gar1 transgene fully complements the glsA mutation in V. carteri, a result that suggests that asymmetric division probably arose through the modification of a gene whose product interacts with GlsA, but not through a modification of glsA itself.

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Acknowledgements

We thank Valeria Pappas and Cynthia Wagner for helpful discussions and/or comments on an earlier version of the manuscript, and two anonymous reviewers for insightful suggestions for improving the submitted manuscript. We thank Cristina Caplinger for technical assistance, Patrick Ferris for providing the Chlamydomonas genomic library, and James Umen for Chlamydomonas strain c3. We are especially grateful to David Kirk, who inspired us to undertake this project, and in whose laboratory it was initiated. This work was supported by research grants from the USDA (no. 95-37304-2229) and from the NSF (no. 0077535) to S.M.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Maryland, 1000 Hilltop Circle, Baltimore County, Baltimore, MD 21250, USA

    Qian Cheng, Lisseth Edwards & Stephen M. Miller

  2. Department of Biology, Washington University, St. Louis, MO 68130, USA

    Rachel Fowler

  3. Department of Plant Biology, University of Minnesota, St. Paul, MN 55108, USA

    Lai-wa Tam

Authors
  1. Qian Cheng
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  2. Rachel Fowler
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  3. Lai-wa Tam
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  4. Lisseth Edwards
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  5. Stephen M. Miller
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Correspondence to Stephen M. Miller.

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Edited by G. Jürgens

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Cheng, Q., Fowler, R., Tam, Lw. et al. The role of GlsA in the evolution of asymmetric cell division in the green alga Volvox carteri . Dev Genes Evol 213, 328–335 (2003). https://doi.org/10.1007/s00427-003-0332-x

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  • DOI: https://doi.org/10.1007/s00427-003-0332-x

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