Skip to main content

Thank you for visiting 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.

Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages


During development, different cell fates are generated by cell–cell interactions or by the asymmetric distribution of patterning molecules. Asymmetric inheritance is known to occur either through directed transport along actin microfilaments into one daughter cell1,2 or through capture of determinants by a region of the cortex inherited by one daughter3,4,5. Here we report a third mechanism of asymmetric inheritance in a mollusc embryo. Different messenger RNAs associate with centrosomes in different cells and are subsequently distributed asymmetrically during division. The segregated mRNAs are diffusely distributed in the cytoplasm and then localize, in a microtubule-dependent manner, to the pericentriolar matrix. During division, they dissociate from the core mitotic centrosome and move by means of actin filaments to the presumptive animal daughter cell cortex. In experimental cells with two interphase centrosomes, mRNAs accumulate on the correct centrosome, indicating that differences between centrosomes control mRNA targeting. Blocking the accumulation of mRNAs on the centrosome shows that this event is required for subsequent cortical localization. These events produce a complex pattern of mRNA localization, in which different messages distinguish groups of cells with the same birth order rank and similar developmental potentials.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Diagram of Ilyanassa cleavage and patterns of centrosomally localized mRNA.
Figure 2: Localization of mRNAs to the centrosome and mRNA dynamics during cleavage.
Figure 3: Cytoskeletal basis of mRNA localization.
Figure 4: mRNAs are localized to specific subsets of cells during cleavage, and mRNAs are specifically targeted to particular centrosomes.


  1. Takizawa, P. A., Sil, A., Swedlow, J. R., Herskowitz, I. & Vale, R. D. Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast. Nature 389, 90–93 (1997)

    Article  ADS  CAS  Google Scholar 

  2. Long, R. M. et al. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277, 383–387 (1997)

    Article  CAS  Google Scholar 

  3. Spana, E. P. & Doe, C. Q. The Prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 121, 3187–3195 (1995)

    CAS  PubMed  Google Scholar 

  4. Boyd, L., Guo, S., Levitan, D., Stinchcomb, D. T. & Kemphues, K. J. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075–3084 (1996)

    CAS  PubMed  Google Scholar 

  5. Lu, B. W., Ackerman, L., Jan, L. Y. & Jan, Y. N. Modes of protein movement that lead to the asymmetric localization of partner of numb during Drosophila neuroblast division. Mol. Cell 4, 883–891 (1999)

    Article  CAS  Google Scholar 

  6. Crampton, H. E. Experimental studies on gastropod development. Roux's Arch. EntwMech. Org. 3, 1–19 (1896)

    Google Scholar 

  7. Clement, A. C. Experimental studies on germinal localization in Ilyanassa. I. The role of the polar lobe in determination of the cleavage pattern and its influence in later development. J. Exp. Zool. 132, 427–446 (1952)

    Article  Google Scholar 

  8. Wilson, E. B. Experimental studies in germinal localization. II Experiments on the cleavage-mosaic in patella and dentalium. J. Exp. Zool. 1, 197–268 (1904)

    Article  Google Scholar 

  9. Clement, A. C. Development of Ilyanassa following the removal of the D macromere at successive cleavage stages. J. Exp. Zool. 149, 193–216 (1962)

    Article  Google Scholar 

  10. Macdonald, P. M., Ingham, P. & Struhl, G. Isolation, structure, and expression of even-skipped—a 2nd pair-rule gene of Drosophila containing a homeo box. Cell 47, 721–734 (1986)

    Article  CAS  Google Scholar 

  11. Wharton, K. A., Ray, R. P. & Gelbart, W. M. An activity gradient of Decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807–822 (1993)

    CAS  PubMed  Google Scholar 

  12. Holley, S. A. et al. A conserved system for dorsal–ventral patterning in insects and vertebrates involving Sog and Chordin. Nature 376, 249–253 (1995)

    Article  ADS  CAS  Google Scholar 

  13. Shimell, M. J., Ferguson, E. L., Childs, S. R. & Oconnor, M. B. The Drosophila dorsal–ventral patterning gene Tolloid is related to human bone morphogenetic protein-1. Cell 67, 469–481 (1991)

    Article  CAS  Google Scholar 

  14. Clement, A. C. Cell determination and organogenesis in molluscan development—reappraisal based on deletion experiments in Ilyanassa. Am. Zool. 16, 447–453 (1976)

    Article  Google Scholar 

  15. Render, J. Cell fate maps in the Ilyanassa obsoleta embryo beyond the third division. Dev. Biol. 189, 301–310 (1997)

    Article  CAS  Google Scholar 

  16. Sweet, H. C. Specification of first quartet micromeres in Ilyanassa involves inherited factors and position with respect to the inducing D macromere. Development 125, 4033–4044 (1998)

    CAS  PubMed  Google Scholar 

  17. Yoshida, S., Marikawa, Y. & Satoh, N. posterior end mark, a novel maternal gene encoding a localized factor in the ascidian embryo. Development 122, 2005–2012 (1996)

    CAS  PubMed  Google Scholar 

  18. Nishikata, T., Hibino, T. & Nishida, H. The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev. Biol. 209, 72–85 (1999)

    Article  CAS  Google Scholar 

  19. Mello, C. C. et al. The PIE-1 protein and germline specification in C. elegans embryos. Nature 382, 710–712 (1996)

    Article  ADS  CAS  Google Scholar 

  20. Reese, K. J., Dunn, M. A., Waddle, J. A. & Seydoux, G. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol. Cell 6, 445–455 (2000)

    Article  CAS  Google Scholar 

  21. Wu, X. Y. & Palazzo, R. E. Differential regulation of maternal vs. paternal centrosomes. Proc. Natl Acad. Sci. USA 96, 1397–1402 (1999)

    Article  ADS  CAS  Google Scholar 

  22. Bonaccorsi, S., Giansanti, M. G. & Gatti, M. Spindle assembly in Drosophila neuroblasts and ganglion mother cells. Nature Cell Biol. 2, 54–56 (2000)

    Article  CAS  Google Scholar 

  23. Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. & Bornens, M. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317–329 (2000)

    Article  CAS  Google Scholar 

  24. Conklin, E. G. Karyokinesis and cytokinesis in the maturation, fertilization and cleavage of Crepidula and other gasteropoda. J. Acad. Nat. Sci. Philadelphia Ser. 2 12, 1–21 (1902)

    Google Scholar 

  25. Goto, S. & Hayashi, S. Cell migration within the embryonic limb primordium of Drosophila as revealed by a novel fluorescence method to visualize mRNA and protein. Dev. Genes Evol. 207, 194–198 (1997)

    Article  CAS  Google Scholar 

  26. Sanders, M. A. & Salisbury, J. L. Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J. Cell Biol. 124, 795–805 (1994)

    Article  CAS  Google Scholar 

  27. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J. L. & Bornens, M. Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J. Cell Sci. 109, 3089–3102 (1996)

    CAS  PubMed  Google Scholar 

  28. Lambert, J. D. & Nagy, L. M. MAPK signaling by the D quadrant embryonic organizer of the mollusc Ilyanassa obsoleta. Development 128, 45–56 (2001)

    CAS  PubMed  Google Scholar 

Download references


We thank J. Cooley, D. Bentley and J. Wandelt for technical help; J. Salisbury and G. Hermann for antibodies; D. Brower, C. Gregorio and G. Von Dassow for critically reading the manuscript; and R. Palazzo, M. Goulding, G. Lambert, E. Wilk and M. Gibson for technical advice and discussions. This work was supported by an National Science Foundation (NSF) Graduate Research Fellowship and an NSF Doctoral Dissertation Improvement Grant to J.D.L., and a grant from the NSF to L.M.N.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Lisa M. Nagy.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lambert, J., Nagy, L. Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 420, 682–686 (2002).

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


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