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JOURNAL ARTICLES
Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo
S.E. Mango, C.J. Thorpe, P.R. Martin, S.H. Chamberlain, B. Bowerman
Development 1994 120: 2305-2315;

Summary

In a 4-cell Caenorhabditis elegans embryo, two sister blastomeres called ABa and ABp are born with equivalent developmental potential, but eventually produce distinct patterns of cell fate. The different fates of ABa and ABp are specified at least in part by inductive interactions with neighboring blastomeres. Previous studies indicate that, at the 4-cell stage, a signal from the posterior-most blastomere, P2, is required for ABp to produce at least one of its unique cell types. This P2/ABp interaction depends on glp-1, a putative receptor for intercellular interactions. To investigate this early induction further, we isolated mutants in which ABp developed abnormally. We describe the effects of recessive mutations in apx-1, a maternal gene that appears to be required for P2 to signal ABp. In embryos from mothers homozygous for mutations in apx-1 (apx-1 embryos), ABp fails to produce its characteristic cell types. Instead, ABp from apx-1 embryos develops more like its sister ABa: it produces ABa-like pharyngeal cells and it recapitulates ABa-like cell lineages. Because mutations in apx-1 affect the development of only the ABp blastomere, we suggest that the wild-type gene encodes a component of the P2/ABp signalling pathway. To explain the observation that ABp in apx-1 embryos adopts an ABa-like fate, we propose a model in which the P2 signal is required to break the initial equivalence of ABa and ABp. We performed two independent tests of this model. First, we examined ABp development in pie-1 mutant embryos, in which P2 adopts the identity of another blastomere. We find that, in pie-1 embryos, APp fails to produce its characteristic cell types and instead adopts a fate similar to that of ABa. We conclude that the changed identity of P2 in pie-1 embryos prevents the P2/ABp interaction. As a second test, we examined ABp development in wild-type embryos after physically removing P2. These operated embryos produce extra pharyngeal cells, consistent with out proposal that a signal from P2 breaks the initially equivalent developmental state of ABa and ABp. We discuss the possibility that apx-1 acts as a ligand in this glp-1-dependent signalling pathway.

REFERENCES

    1. Artavanis-Tsakonas S.,
    2. Delidakis C.,
    3. Fehon R. G.
    (1991) The Notch locus and the cell biology of neuroblast segregation. Ann. Rev. Genet 7, 427–452
    OpenUrl
    1. Austin J.,
    2. Kimble J.
    (1987) glp-1 is required for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51, 589–599
    OpenUrlCrossRefPubMedWeb of Science
    1. Austin J.,
    2. Kimble J.
    (1989) Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58, 565–571
    OpenUrlCrossRefPubMedWeb of Science
    1. Bowerman B.,
    2. Tax F. E.,
    3. Thomas J. H.,
    4. Priess J. R.
    (1992) Cell interactions involved in development of the bilaterally symmetrical intestinal valve cells during embryogenesis in Caenorhabditis elegans. Development 116, 1113–1122
    OpenUrlAbstract/FREE Full Text
    1. Bowerman B.,
    2. Draper B. W.,
    3. Mello C. C.,
    4. Priess J. R.
    (1992) The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74, 443–452
    OpenUrl
    1. Brenner S.
    (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Chamberlin H. M.,
    2. Sternberg P. W.
    (1993) Multiple cell interactions are required for fate specification during male spicule development in Caenorhabditis elegans. Development 118, 297–324
    OpenUrlAbstract
    1. Doe C. Q.,
    2. Goodman C. S.
    (1985) Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev. Biol 111, 206–219
    OpenUrlCrossRefPubMedWeb of Science
    1. Eisen J. S.,
    2. Pike S. H.,
    3. Romancier B.
    (1990) An identified neuron with variable fates in embryonic zebrafish. J. Neurosci 10, 34–43
    OpenUrlAbstract
    1. Eisen J. S.
    (1992) The role of interactions in determining cell fate of two identified motoneurons in the embryonic zebrafish. Neuron 8, 231–240
    OpenUrlCrossRefPubMedWeb of Science
    1. Evans T. C.,
    2. Crittenden S. L.,
    3. Kodoyianni V.,
    4. Kimble J.
    (1994) Translational control of maternal glp-1 mRNA establishes an asymmetry in the C. elegans embryo. Cell 77, 183–194
    OpenUrlCrossRefPubMedWeb of Science
    1. Goldstein B.
    (1992) Induction of gut in Caenorhabditis elegans embryos. Nature 357, 255–257
    OpenUrlCrossRefPubMedWeb of Science
    1. Greenwald I.,
    2. Rubin G. M.
    (1992) Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68, 271–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Hird S. N.,
    2. White J. G.
    (1993) Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J. Cell Biol 121, 1343–1355
    OpenUrlAbstract/FREE Full Text
    1. Hyman A. A.,
    2. White J. G.
    (1987) Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J. Cell Biol 105, 2123–2135
    OpenUrlAbstract/FREE Full Text
    1. Kemphues K. J.,
    2. Priess J. R.,
    3. Morton D.,
    4. Cheng N.
    (1988) Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311–320
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimble J.,
    2. Hirsch D.
    (1979) The post-embryonic cell lineages of the hermaphrodite and male gonads inCaenorhabditis elegans. Dev. Biol 70, 396–417
    OpenUrlCrossRefPubMedWeb of Science
    1. Kimble J.
    (1981) Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans. Dev. Biol 87, 286–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Kodoyianni V.,
    2. Maine E. M.,
    3. Kimble J.
    (1992) Molecular basis of loss-of-function mutations in the glp-1 gene of Caenorhabditis elegans. Mol. Biol. Cell 3, 1199–1213
    OpenUrlAbstract/FREE Full Text
    1. Kuwada J. Y.,
    2. Goodman C. S.
    (1985) Neuronal determination during embryonic development of the grasshopper nervous system. Dev. Biol 110, 114–126
    OpenUrlCrossRefPubMedWeb of Science
    1. Lambie E. J.,
    2. Kimble J.
    (1991) Genetic control of cell interactions in nematode development. Ann. Rev. Genetics 25, 411–436
    OpenUrlCrossRefPubMed
    1. Lambie E. J.,
    2. Kimble J.
    (1991) Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 112, 231–240
    OpenUrlAbstract
    1. Mello C. C.,
    2. Draper B. W.,
    3. Krause M.,
    4. Weintraub H.,
    5. Priess J. R.
    (1992) The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos. Cell 70, 163–176
    OpenUrlCrossRefPubMedWeb of Science
    1. Mello C. C.,
    2. Draper B. W.,
    3. Priess J. R.
    (1994) The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77, 95–106
    OpenUrlCrossRefPubMedWeb of Science
    1. Miller D. M.,
    2. Ortiz I.,
    3. Berliner G. C.,
    4. Epstein H. F.
    (1983) Differential localization of two myosins within nematode thick filaments. Cell 34, 477–490
    OpenUrlCrossRefPubMedWeb of Science
    1. Okamoto H.,
    2. Thomson J. N.
    (1985) Monoclonal antibodies which distinguish certain classes of neuronal and supporting cells in the nervous tissue of the nematode Caenorhabditis elegans. J. Neurosci 5, 643–653
    OpenUrlAbstract
    1. Priess J. R.,
    2. Thomson J. N.
    (1987) Cellular interactions in early C. elegans embryos. Cell 48, 241–250
    OpenUrlCrossRefPubMedWeb of Science
    1. Priess J. R.,
    2. Schnabel H.,
    3. Schnabel R.
    (1987) The glp-1 locus and cellular interactions in the early C. elegans embryo. Cell 51, 601–611
    OpenUrlCrossRefPubMedWeb of Science
    1. Pruss R. M.,
    2. Mirsky R.,
    3. Raff M. C.,
    4. Thorpe R.,
    5. Dowding A.J.,
    6. Anderton B.H.
    (1981) All classes of intermediate filaments share a common antigenic determinant defined by a monoclonal antibody. Cell 27, 419–428
    OpenUrlCrossRefPubMedWeb of Science
    1. Strome S.,
    2. Wood W. B.
    (1983) Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15–25
    OpenUrlCrossRefPubMedWeb of Science
    1. Sulston J. E.,
    2. White J. G.
    (1980) Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev. Biol 78, 577–597
    OpenUrlCrossRefPubMedWeb of Science
    1. Sulston J. E.,
    2. Schierenberg E.,
    3. White J. G.,
    4. Thomson J.N.
    (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol 100, 64–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Taghert P. H.,
    2. Doe C. Q.,
    3. Goodman C. S.
    (1984) Cell determination and regulation during development of neuroblasts and neurones in grasshopper embryo. Nature 307, 163–165
    OpenUrlCrossRefPubMed
    1. Tax F. E.,
    2. Yeargers J. J.,
    3. Thomas J. H.
    (1994) Sequence of C. elegans lag-2 reveals a cell-signalling domain shared with Delta and Serrate of Drosophila. Nature 368, 150–154
    OpenUrlCrossRefPubMed
    1. Weisblat D. A.,
    2. Blair S. S.
    (1984) Developmental interdependency in embryos of the leech Helobdella triserialis. Dev. Biol 101, 326–335
    OpenUrlCrossRefPubMedWeb of Science
    1. Wood W. B.,
    2. Edgar L. G.
    (1994) Patterning in the C. elegans embryo. Trends in Genet 10, 37–67
    OpenUrlCrossRefPubMed
    1. Yochem J.,
    2. Greenwald I.
    (1989) glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans encode similar transmembrane proteins. Cell 58, 553–563
    OpenUrlCrossRefPubMedWeb of Science
    1. Young J. M.,
    2. Hope I. A.
    (1993) Molecular markers of differentiation in Caenorhabditis elegans obtained by promoter trapping. Developmental Dynamics 196, 124–132
    OpenUrlPubMed
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JOURNAL ARTICLES
Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo
S.E. Mango, C.J. Thorpe, P.R. Martin, S.H. Chamberlain, B. Bowerman
Development 1994 120: 2305-2315;
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