Advertisement
JOURNAL ARTICLES
Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration
R. Namba, T.M. Pazdera, R.L. Cerrone, J.S. Minden
Development 1997 124: 1393-1403;

Summary

The product of the maternal effect gene, bicoid (bcd), is a transcription factor that acts in a concentration-dependent fashion to direct the establishment of anterior fates in the Drosophila melanogaster embryo. Embryos laid by mothers with fewer or greater than the normal two copies of bcd show initial alterations in the expression of the gap, segmentation and segment polarity genes, as well as changes in early morphological markers. In the absence of a fate map repair system, one would predict that these initial changes would result in drastic changes in the shape and size of larval and adult structures. However, these embryos develop into relatively normal larvae and adults. This indicates that there is plasticity in Drosophila embryonic development along the anterior-posterior axis. Embryos laid by mothers with six copies of bcd have reduced viability, indicating a threshold for repairing anterior-posterior mispatterning. We show that cell death plays a major role in correcting expanded regions of the fate map. There is a concomitant decrease of cell death in compressed regions of the fate map. We also show that compression of the fate map does not appear to be repaired by the induction of new cell divisions. In addition, some tissues are more sensitive to fate map compression than others.

REFERENCES

    1. Berleth T.,
    2. Burri M.,
    3. Thoma G.,
    4. Bopp D.,
    5. Richstein S.,
    6. Frigerio G.,
    7. Noll M.,
    8. Nusslein-Volhard C.
    (1988) The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J 7, 1749–1756
    OpenUrlPubMedWeb of Science
    1. Bomze H. M.,
    2. Lopez A. J.
    (1994) Evolutionary conservation of the structure and expression of alternatively spliced ultrabithorax isoforms from Drosophila. Genetics 136, 965–977
    OpenUrlAbstract/FREE Full Text
    1. Bownes M.
    (1975) Adult deficiencies and duplication of head and thoracic structures resulting from microcautery of blastoderm stage Drosophila embryos. J. Embryol. Exp. Morph 34, 33–54
    OpenUrlPubMedWeb of Science
    1. Busturia A.,
    2. Lawrence P. A.
    (1994) Regulation of cell number in Drosophila. Nature 370, 561–563
    OpenUrlCrossRefPubMed
    1. Bryant S. V.,
    2. French V.,
    3. Bryant P. J.
    (1981) Distal regeneration and symmetry. Science 212, 993–1002
    OpenUrlAbstract/FREE Full Text
    1. Cagan R. L.,
    2. Ready D. F.
    (1989) The emergence of order in the Drosophila pupal retina. Dev. Biol 136, 346–262
    OpenUrlCrossRefPubMedWeb of Science
    1. Cohen S. M.,
    2. Jurgens G.
    (1990) Mediation of Drosophila head development by gap-like segmentation genes. Nature 346, 482–485
    OpenUrlCrossRefPubMedWeb of Science
    1. Davidson E. H.
    (1989) Lineage-specific gene expression and the regulative capacities of the sea urchin embryo: a proposed mechanism. Development 105, 421–45
    OpenUrlAbstract/FREE Full Text
    1. DiNardo S.,
    2. Kuner J. M.,
    3. Thies J.,
    4. O'Farrell P. H.
    (1985) Development of embryonic pattern in D. melanogaster as revealed by accumulation of the nuclear engrailed protein. Cell 40, 56–69
    OpenUrl
    1. Dohrmann C.,
    2. Azpiazu N.,
    3. Frasch M.
    (1990) A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev 4, 2098–2111
    OpenUrlAbstract/FREE Full Text
    1. Driever W.,
    2. Nusslein-Volhard C.
    (1988) The BICOIDprotein determines position in the Drosophila embryos in a concentration-dependent manner. Cell 54, 95–104
    OpenUrlCrossRefPubMedWeb of Science
    1. Eldon E. D.,
    2. Pirrotta V.
    (1991) Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes. Development 111, 367–378
    OpenUrlAbstract
    1. Foe V. E.,
    2. Odell G. M.
    (1989) Mitotic domains partition fly embryos, reflecting early biological consequences of determination in progress. American Zoologist 29, 617–652
    OpenUrl
    1. Frasch M.,
    2. Hoey T.,
    3. Rushlow C.,
    4. Doyle H.,
    5. Levine M.
    (1987) Characterization and localization of the EVEN-SKIPPEDprotein of Drosophila. EMBO J 6, 749–759
    OpenUrlPubMedWeb of Science
    1. French V.,
    2. Bryant S. V.,
    3. Bryant P. J.
    (1976) Pattern regulation in epimorphic fields. Science 193, 969–981
    OpenUrlAbstract/FREE Full Text
    1. Grether M. E.,
    2. Abrams J. M.,
    3. Agapite J.,
    4. White K.,
    5. Steller H.
    (1995) The head involution defective gene of Drosophilamelanogaster functions in programmed cell death. Genes Dev 9, 1694–1708
    OpenUrlAbstract/FREE Full Text
    1. Kam Z.,
    2. Minden J. S.,
    3. Agard D. A.,
    4. Sedat J. W.,
    5. Leptin M.
    (1991) Drosophila gastrulation: analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy. Development 112, 365–370
    OpenUrlAbstract
    1. King B. H.,
    2. Bryant P. J.
    (1982) Developmental responses of the Drosophila melanogaster embryo to localized X irradiation. Rad. Res 89, 590–606
    OpenUrlCrossRefPubMed
    1. Kraut R.,
    2. Levine M.
    (1991) Spatial regulation of the gap gene giant during Drosophila development. Development 111, 601–609
    OpenUrlAbstract
    1. Lamka M. L.,
    2. Boulet A. M.,
    3. Sakonju S.
    (1992) Ectopic expression of UBX and ABD-B proteins during Drosophila embryogenesis: competition, not a functional hierarchy, explains phenotypic suppression. Development 116, 841–854
    OpenUrlAbstract/FREE Full Text
    1. Maggert K.,
    2. Levine M.,
    3. Frasch M.
    (1995) The somatic-visceral subdivision of the embryonic mesoderm is initiated by dorsal gradient thresholds in Drosophila. Development 121, 2107–2116
    OpenUrlAbstract
    1. Minden J. S.
    (1996) Synthesis of a new substrate for detection of lacZ gene expression in live Drosophila embryos. BioTechniques 20, 122–129
    OpenUrlPubMedWeb of Science
    1. Minden J. S.,
    2. Agard D. A.,
    3. Sedat J. W.,
    4. Alberts B. M.
    (1989) Direct cell lineage analysis in Drosophilamelanogaster by time-lapse, three-dimensional optical microscopy in living embryos. J. Cell Biol 109, 505–516
    OpenUrlAbstract/FREE Full Text
    1. Raff M. C.,
    2. Barres B. A.,
    3. Burne J. F.,
    4. Coles H. S.,
    5. Ishizaki Y.,
    6. Jacobson M. D.
    (1993) Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 262, 695–700
    OpenUrlAbstract/FREE Full Text
    1. Robinow S.,
    2. White K.
    (1991) Characterization and spatial distribution of ELAV protein during Drosophila Melanogaster development. J. Neurobiol 22, 443–461
    OpenUrlCrossRefPubMedWeb of Science
    1. Rykowski M. C.
    (1991) Optical sectioning and three-dimensional reconstruction of diploid and polytene nuclei. Methods Cell Biol 35, 253–286
    OpenUrlPubMed
    1. Schubiger G.
    (1976) Adult differentiation and partial Drosophila embryos after ligation during stages of nuclear multiplication and cellular blastoderm. Dev. Biol 50, 476–488
    OpenUrlCrossRefPubMed
    1. Skeath J. B.,
    2. Carroll S.
    (1992) Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo. Development 114, 939–946
    OpenUrlAbstract
    1. Struhl G.
    (1989) Differing strategies for organizing anterior body pattern in Drosophila embryos. Nature 338, 741–744
    OpenUrlCrossRefPubMed
    1. Struhl G.,
    2. Struhl K.,
    3. Macdonald P. M.
    (1989) The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259–1273
    OpenUrlCrossRefPubMedWeb of Science
    1. Tautz D.,
    2. Lehmann R.,
    3. Schnurch H.,
    4. Schuh R.,
    5. Seifert E.,
    6. Keinlin A.,
    7. Jones K.,
    8. Jäckle J.
    (1987) Finger protein of novel structure encoded by hunchback, a second member of the gap class of Drosophila segmentation genes. Nature 327, 383–389
    OpenUrlCrossRef
    1. Tautz D.,
    2. Pfeifle C.
    (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Truman J. W.,
    2. Thorn R. S.,
    3. Robinow S.
    (1992) Programmed neuronal death in insect development. J. Neurobiol 23, 1295–1311
    OpenUrlCrossRefPubMedWeb of Science
    1. Warn R. M.,
    2. Magrath R.
    (1986) Observations by novel method of surface changes during the syncytial blastoderm stage of the Drosophila embryo. Dev. Biol 89, 540–548
    1. Wolff T.,
    2. Ready D. F.
    (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113, 825–839
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Drosophila embryonic pattern repair: how embryos respond to bicoid dosage alteration
R. Namba, T.M. Pazdera, R.L. Cerrone, J.S. Minden
Development 1997 124: 1393-1403;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

Kathryn Virginia Anderson (1952-2020)

Developmental geneticist Kathryn Anderson passed away at home on 30 November 2020. Tamara Caspary, a former postdoc and friend, remembers Kathryn and her remarkable contribution to developmental biology.

Zooming into 2021

In a new Editorial, Editor-in-Chief James Briscoe and Executive Editor Katherine Brown reflect on the triumphs and tribulations of the last 12 months, and look towards a hopefully calmer and more predictable year.

Read & Publish participation extends worldwide

Over 60 institutions in 12 countries are now participating in our Read & Publish initiative. Here, James Briscoe explains what this means for his institution, The Francis Crick Institute. Find out more and view our full list of participating institutions.

Upcoming special issues

Imaging Development, Stem Cells and Regeneration
Submission deadline: 30 March 2021
Publication: mid-2021

The Immune System in Development and Regeneration
Guest editors: Florent Ginhoux and Paul Martin
Submission deadline: 1 September 2021
Publication: Spring 2022

Both special issues welcome Review articles as well as Research articles, and will be widely promoted online and at key global conferences.

Development presents...

Our successful webinar series continues into 2021, with early-career researchers presenting their papers and a chance to virtually network with the developmental biology community afterwards. Sign up to join our next session:

10 February
Time: 13:00 (GMT)
Chaired by: preLights