Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Two-step cell polarization in algal zygotes

A Corrigendum to this article was published on 13 February 2017

Abstract

In most complex eukaryotes, development starts with the establishment of cell polarity determining the first axis of the body plan. This polarity axis is established by the asymmetrical distribution of intrinsic factors13, which breaks the symmetry in a single step. Zygotes of the brown alga Fucus, which unlike land plant and animal zygotes4,5 do not possess a maternally predetermined polarity axis, serve as models to study polarity establishment6,7. Here, we studied this process in Dictyota, and concluded that sense and direction of the cell polarization vector are established in two mechanistically and temporally distinct phases that are under control of different life cycle stages. On egg activation, the zygote elongates rapidly according to a maternally predetermined direction expressing the first phase of cell polarization. Which of the two poles of the resulting prolate spheroidal zygote will acquire the basal cell fate is subsequently environmentally determined. The second phase is accompanied by and dependent on zygotic transcription instead of relying uniquely on maternal factors8. Cell polarization, whereby determination of direction and sense of the polarization vector are temporally and mechanistically uncoupled, is unique and represents a favourable system to gain insight into the processes underlying cell polarity establishment in general.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Elongation and polarization in the Dictyota dichotoma embryo.
Figure 2: Determination of direction of the polarization vector: elongation and chloroplast distribution.
Figure 3: Determination of sense of the polarization vector: timing, environmental cue and zygotic control.
Figure 4: One-step versus two-step zygote polarization.

Similar content being viewed by others

References

  1. Jan, Y. N. & Jan, L. Y. Asymmetric cell division. Nature 392, 775–778 (1998).

    Article  CAS  Google Scholar 

  2. Scheres, B. & Benfey, P. N. Asymmetric cell division in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 505–537 (1999).

    Article  CAS  Google Scholar 

  3. Abrash, E. B. & Bergmann, D. C. Asymmetric cell divisions: a view from plant development. Dev. Cell 16, 783–796 (2009).

    Article  CAS  Google Scholar 

  4. Nakajima, K., Uchiumi, T. & Okamoto, T. Positional relationship between the gamete fusion site and the first division plane in the rice zygote. J. Exp. Bot. 61, 3101–3105 (2010).

    Article  CAS  Google Scholar 

  5. Kumano, G. Polarizing animal cells via mRNA localization in oogenesis and early development. Dev. Growth Differ. 54, 1–18 (2012).

    Article  CAS  Google Scholar 

  6. De Smet, I. & Beeckman, T. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat. Rev. Mol. Cell Biol. 12, 177–188 (2011).

    Article  CAS  Google Scholar 

  7. Kropf, D. Induction of polarity in fucoid zygotes. Plant Cell 9, 1011–1020 (1997).

    Article  CAS  Google Scholar 

  8. Lee, M. T., Bonneau, A. R. & Giraldez, A. J. Zygotic genome activation during the maternal-to-zygotic transition. Annu. Rev. Cell Dev. Biol. 30, 581–613 (2014).

    Article  CAS  Google Scholar 

  9. Yang, Z. Cell polarity signaling in Arabidopsis. Annu. Rev. Cell Dev. Biol. 24, 551–575 (2008).

    Article  Google Scholar 

  10. Shaw, S. L. & Quatrano, R. S. Polar localization of a dihydropyridine receptor on living Fucus zygotes. J. Cell Sci. 109, 335–342 (1996).

    CAS  PubMed  Google Scholar 

  11. Dong, J. & MacAlister, C. A. & Bergmann, D. C. BASL controls asymmetric cell division in Arabidopsis. Cell 137, 1320–1330 (2009).

    Article  Google Scholar 

  12. Yamashita, Y. M., Mahowald, A. P., Perlin, J. R. & Fuller, M. T. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315, 518–521 (2007).

    Article  CAS  Google Scholar 

  13. Bogaert, K. A., Beeckman, T. & De Clerck, O. Photopolarization of Fucus zygotes is determined by time sensitive vectorial addition of environmental cues during axis amplification. Front. Plant Sci. 6, 1–8 (2015).

    Article  Google Scholar 

  14. Brawley, S. H., Wetherebee, R. & Quatrano, R. S. Fine-structural studies of the gametes and embryo of Fucus vesiculosus L. (Phaeophyta) II.: the cytoplasm of the egg and young zygote. J. Cell. Sci. 20, 255–271 (1976).

    CAS  PubMed  Google Scholar 

  15. Evans, L. V., Callow, J. A. & Callow, M. in Progress in Phycological Research (eds Round, F. E. & Chapman, D. J. ) 68–110 (Elsevier, 1982).

    Google Scholar 

  16. Novotny, A. M. & Forman, M. The relationship between changes in cell wall composition and the establishment of polarity in Fucus embryos. Dev. Bio. 173, 162–173 (1974).

    Article  Google Scholar 

  17. Samaj, J., Müller, J., Beck, M., Böhm, N. & Menzel, D. Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci. 11, 594–600 (2006).

    Article  CAS  Google Scholar 

  18. Weiner, O. D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196–202 (2002).

    Article  CAS  Google Scholar 

  19. Prodon, F., Dru, P., Roegiers, F. & Sardet, C. Polarity of the ascidian egg cortex and relocalization of cER and mRNAs in the early embryo. J. Cell Sci. 118, 2393–2404 (2005).

    Article  CAS  Google Scholar 

  20. Twell, D., Park, S. K. & Lalanne, E. Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci. 3, 305–310 (1998).

    Article  Google Scholar 

  21. Ueda, M. & Laux, T. The origin of the plant body axis. Curr. Opin. Plant Biol. 15, 578–584 (2012).

    Article  Google Scholar 

  22. Ueda, M., Zhang, Z. & Laux, T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell 20, 264–270 (2011).

    Article  CAS  Google Scholar 

  23. Ubbels, G. A. Establishment of polarities in the oocyte of Xenopus laevis: the provisional axial symmetry of the full-grown oocyte of Xenopus laevis. Cell. Mol. Life Sci. 53, 382–409 (1997).

    Article  CAS  Google Scholar 

  24. Schier, A. The maternal-zygotic transition: death and birth of RNAs. Science. 316, 406–408 (2007).

    Article  CAS  Google Scholar 

  25. Luo, A., Shi, C., Zhang, L. & Sun, M.-X. The expression and roles of parent-of-origin genes in early embryogenesis of angiosperms. Front. Plant Sci. 5, 729 (2014).

    PubMed  PubMed Central  Google Scholar 

  26. Nodine, M. D. & Bartel, D. P. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482, 94–97 (2012).

    Article  CAS  Google Scholar 

  27. Xin, H.-P., Zhao, J. & Sun, M.-X. The maternal-to-zygotic transition in higher plants. J. Integr. Plant Biol. 54, 610–615 (2012).

    Article  CAS  Google Scholar 

  28. Ning, J. et al. Differential gene expression in egg cells and zygotes suggests that the transcriptome is restructed before the first zygotic division in tobacco. FEBS Lett. 580, 1747–1752 (2006).

    Article  CAS  Google Scholar 

  29. Zhao, J. et al. Dynamic changes of transcript profiles after fertilization are associated with de novo transcription and maternal elimination in tobacco zygote, and mark the onset of the maternal-to-zygotic transition. Plant J. 65, 131–145 (2011).

    Article  CAS  Google Scholar 

  30. Ruttink, T. et al. Orthology guided assembly in highly heterozygous crops: creating a reference transcriptome to uncover genetic diversity in Lolium perenne. Plant Biotechnol. J. 11, 605–617 (2013).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are indebted to the Research Foundation Flanders (FWO) (PhD fellowship to K.A.B.) and ASSEMBLE (grant agreement no. 227799). We would like to thank S.M. Coelho, M. Claeys, K. Pauly, T. Motomura, J.H. Bothwell, C. Nagasato, A. Lipinska, F. Steen, G. Zuccarello and C. Katsaros for stimulating conversations and M. Claeys and S. D'hondt for practical assistance.

Author information

Authors and Affiliations

Authors

Contributions

K.A.B. conducted all experiments. K.A.B., T.B. and O.D.C. wrote the manuscript.

Corresponding author

Correspondence to Kenny A. Bogaert.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bogaert, K., Beeckman, T. & De Clerck, O. Two-step cell polarization in algal zygotes. Nature Plants 3, 16221 (2017). https://doi.org/10.1038/nplants.2016.221

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2016.221

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing