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A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation

Nature Cell Biology volume 2, pages 458–460 (2000)Cite this article

In Drosophila melanogaster and Caenorhabditis elegans, development of the germ-line lineage depends upon cytoplasmic granules localized to the posterior pole of the zygote, which are present in germ-line cells throughout development1,2. In D. melanogaster, polar granules are components of the pole plasm assembled at the posterior pole during oogenesis, and in C. elegans P granules accumulate at the posterior pole of one-cell embryos. Mutations in D. melanogaster pole-plasm components such as OSKAR result in defects in embryonic patterning and germ-line specification2; mutations in C. elegans polarity proteins, such as the Ser/Thr kinase PAR-1, that result in mispositioning of P granules, cause defects in embryonic patterning and cell-fate determination3. Here we show that a D. melanogaster homologue of PAR-1 becomes asymmetrically localized as polarity is established, and that mutations affecting its expression perturb posterior patterning, germ-line development and posterior localization of pole-plasm components. We propose that par-1 has an important and conserved function in establishment of polarity and development of the germ-line lineage in both of these species.

Analysis of the distribution of Drosophila PAR-1 in ovaries revealed that it is present in the spectrosome and early fusome of the germarium (data not shown) and becomes enriched in the oocyte during early oogenesis (Fig. 1d, top). During stages 5–8 of oogenesis, the protein is uniformly distributed along the oocyte cortex (Fig. 1d, middle), and at stage 9, it is enriched at the posterior pole, although it can be detected at a low level throughout the oocyte cortex (Fig. 1d, bottom). PAR-1 is also expressed in follicle cells (Fig. 1d).

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Figure 1: Molecular analysis of D. melanogaster par-1.
Figure 2: Drosophila par-1 mutants exhibit defects in abdominal patterning, pole-cell formation and pole-plasm positioning.

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Acknowledgements

We thank N. Gunkel for help in screening cDNAs, A. Cyrklaff for salivary-gland chromosome squashes, A-M. Michon for immunohistochemistry, T. Vaccari for western blots, A. Spradling and P. Tolias for their gifts of cDNA libraries, D. St Johnston for anti-STAU antibody and J. Knoblich and H. Strober for anti- Drosophila PAR antibody. We also thank P. Gönczy and T. Vaccari for critical reading of the manuscript, and J. M. Schulman and D. St Johnston for sharing their observations concerning Drosophila par-1. Their analysis (Schulman et al., Cell 101, 377–388, 2000) was published while this paper was under review. P.T. was supported by an EMBL predoctoral fellowship, F.P. by a cancer centre research fund (DRG-1404) of the Damon Runyon-Walter Winchell Foundation Fellowship, and V.R. by an EMBO long-term fellowship. This work was supported by grants from the EMBL (to A.E.) and the NICHD (HD27689; to K.K.).

Correspondence and requests for materials should be addressed to A.E.

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Authors and Affiliations

  1. Developmental Biology Programme, European Molecular Biology Laboratory, Meyerhofstrasse 1, Heidelberg, 69117, Germany

    Pavel Tomancak, Veit Riechmann & Anne Ephrussi

  2. Department of Molecular Biology and Genetics, 107 Biotechnology Building, Cornell University, Ithaca, 14853, New York, USA

    Fabio Piano, Kristin C. Gunsalus, Kenneth J. Kemphues & Anne Ephrussi

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  1. Pavel Tomancak
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  6. Anne Ephrussi
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Correspondence to Anne Ephrussi.

Supplementary information

Figure 1S

Effect of the par-19A P element on par-1 expression. (PDF 17 kb)

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Tomancak, P., Piano, F., Riechmann, V. et al. A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat Cell Biol 2, 458–460 (2000). https://doi.org/10.1038/35017101

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