Maternal mRNAs and the Making of Cell
3 Lineages in the Early Xenopus Embryo
Douglas W. Houston
CONTENTS
3.1. Historical Perspectives: The Localization Problem in Amphibians ............................................................................. 25
3.2. Molecular Characterization of Maternal and Localized RNAs ................................................................................... 26
3.2.1. Localized Maternal mRNAs ........................................................................................................................... 26
3.2.2. mRNA Localization Mechanisms ................................................................................................................... 27
3.3. Analysis of Maternal Gene Function in Xenopus Development .................................................................................. 28
3.4. Maternal Control of Germ Layer Induction and Patterning ......................................................................................... 29
3.4.1. Maternal Control of Endoderm and Mesoderm by Vegt ................................................................................. 29
3.4.2. Maternal Secreted Molecules in Germ Layer Induction................................................................................. 30
3.4.3. Ectoderm Specif cation ................................................................................................................................... 30
3.4.4. β-Catenin in Dorsal Gene Activation .............................................................................................................. 31
3.4.5. Cytoplasmic Activation of Dorsal β-Catenin .................................................................................................. 31
3.4.6. Secreted Ligand Activation of β-Catenin........................................................................................................ 32
3.5. Maternal Control of Primordial Germ Cell Formation ................................................................................................ 32
3.5.1. The Germ Plasm.............................................................................................................................................. 32
3.5.2. Germ Plasm mRNAs in PGC Specif cation .................................................................................................... 33
3.5.3. Assembly of Maternal Germ Plasm ................................................................................................................ 33
3.6. Concluding Remarks .................................................................................................................................................... 34
Acknowledgments .................................................................................................................................................................. 35
References.............................................................................................................................................................................. 35
Spemann’s egg constriction experiments ( Figure 3.1 )
3.1. HISTORICAL PERSPECTIVES: THE
LOCALIZATION PROBLEM IN AMPHIBIANS showed that often only one-half of the embryo would form
a dorsal lip (having inherited grey crescent material) and
For over 200 years, embryologists have speculated on the develop into a normally proportioned larva, whereas the
extent that the pattern and organization of the body is deter- other half would develop ventral derivatives of all three germ
mined by that of the egg. The study of amphibian develop- layers, failing to form axial tissues (Spemann, 1903, 1902,
ment is somewhat unique among model organisms in that 1901). Conversely, in cases in which each half-embryo formed
many modern research problems follow the questions and part of the dorsal lip, two normally proportioned embryos
traditions of what perhaps were the very f rst embryologi- would arise. These experiments in amphibians paralleled
cal studies, which were aimed at addressing this very issue. contemporaneous ones in aquatic invertebrates, eventually
The idea that the frog embryo body is organized into germ leading to the realization that so-called “mosaic” versus
layers and along axes of polarity was introduced by the early “regulative” development (i.e. cell autonomous versus norembryologists von Baer (1834 ) and Remak (1855 ), who mal development of isolated blastomeres) was merely a funcnoted the regional origins of the germ layers, and by Newport tion of whether maternal determinants were asymmetrically
(1854 , 1851 ) and Roux (1888 , 1887 ), who described rela- or symmetrically distributed in the early embryo (reviewed
tionships between the site of sperm entry and the alignment in Davidson, 1986; and in Wilson, 1928). Cytoplasmic deterof the body axis. Roux also described what came to be called minants were later hypothesized to determine the fates of
the grey crescent, a pale section of the frog egg opposite the largely equivalent nuclei in the embryo.
sperm entry point ( Figure 3.1 ) that formed in the precise
Three prominent examples of cytoplasmic determinants
position of the future dorsal lip (reviewed in Wilson, 1928 ). in amphibians emerged, frst in earlier frog models and
The dorsal lip was identifed by Spemann as the “organizer” salamanders and later in Xenopus. These were: (1) the relative
of axial pattern in the amphibian embryo ( Spemann, 1938 , dorsal movement of the egg cortex in axis formation (“rotation
1921 ; Spemann and Mangold, 1924 ; and see this volume, of symmetrization,” Ancel and Vintemberger, 1948; later
Chapter 4 ).
termed “cortical rotation,” Gerhart et al., 1989), (2) the role
DOI: 10.1201/9781003050230-4
25
3 Lineages in the Early Xenopus Embryo
Douglas W. Houston
CONTENTS
3.1. Historical Perspectives: The Localization Problem in Amphibians ............................................................................. 25
3.2. Molecular Characterization of Maternal and Localized RNAs ................................................................................... 26
3.2.1. Localized Maternal mRNAs ........................................................................................................................... 26
3.2.2. mRNA Localization Mechanisms ................................................................................................................... 27
3.3. Analysis of Maternal Gene Function in Xenopus Development .................................................................................. 28
3.4. Maternal Control of Germ Layer Induction and Patterning ......................................................................................... 29
3.4.1. Maternal Control of Endoderm and Mesoderm by Vegt ................................................................................. 29
3.4.2. Maternal Secreted Molecules in Germ Layer Induction................................................................................. 30
3.4.3. Ectoderm Specif cation ................................................................................................................................... 30
3.4.4. β-Catenin in Dorsal Gene Activation .............................................................................................................. 31
3.4.5. Cytoplasmic Activation of Dorsal β-Catenin .................................................................................................. 31
3.4.6. Secreted Ligand Activation of β-Catenin........................................................................................................ 32
3.5. Maternal Control of Primordial Germ Cell Formation ................................................................................................ 32
3.5.1. The Germ Plasm.............................................................................................................................................. 32
3.5.2. Germ Plasm mRNAs in PGC Specif cation .................................................................................................... 33
3.5.3. Assembly of Maternal Germ Plasm ................................................................................................................ 33
3.6. Concluding Remarks .................................................................................................................................................... 34
Acknowledgments .................................................................................................................................................................. 35
References.............................................................................................................................................................................. 35
Spemann’s egg constriction experiments ( Figure 3.1 )
3.1. HISTORICAL PERSPECTIVES: THE
LOCALIZATION PROBLEM IN AMPHIBIANS showed that often only one-half of the embryo would form
a dorsal lip (having inherited grey crescent material) and
For over 200 years, embryologists have speculated on the develop into a normally proportioned larva, whereas the
extent that the pattern and organization of the body is deter- other half would develop ventral derivatives of all three germ
mined by that of the egg. The study of amphibian develop- layers, failing to form axial tissues (Spemann, 1903, 1902,
ment is somewhat unique among model organisms in that 1901). Conversely, in cases in which each half-embryo formed
many modern research problems follow the questions and part of the dorsal lip, two normally proportioned embryos
traditions of what perhaps were the very f rst embryologi- would arise. These experiments in amphibians paralleled
cal studies, which were aimed at addressing this very issue. contemporaneous ones in aquatic invertebrates, eventually
The idea that the frog embryo body is organized into germ leading to the realization that so-called “mosaic” versus
layers and along axes of polarity was introduced by the early “regulative” development (i.e. cell autonomous versus norembryologists von Baer (1834 ) and Remak (1855 ), who mal development of isolated blastomeres) was merely a funcnoted the regional origins of the germ layers, and by Newport tion of whether maternal determinants were asymmetrically
(1854 , 1851 ) and Roux (1888 , 1887 ), who described rela- or symmetrically distributed in the early embryo (reviewed
tionships between the site of sperm entry and the alignment in Davidson, 1986; and in Wilson, 1928). Cytoplasmic deterof the body axis. Roux also described what came to be called minants were later hypothesized to determine the fates of
the grey crescent, a pale section of the frog egg opposite the largely equivalent nuclei in the embryo.
sperm entry point ( Figure 3.1 ) that formed in the precise
Three prominent examples of cytoplasmic determinants
position of the future dorsal lip (reviewed in Wilson, 1928 ). in amphibians emerged, frst in earlier frog models and
The dorsal lip was identifed by Spemann as the “organizer” salamanders and later in Xenopus. These were: (1) the relative
of axial pattern in the amphibian embryo ( Spemann, 1938 , dorsal movement of the egg cortex in axis formation (“rotation
1921 ; Spemann and Mangold, 1924 ; and see this volume, of symmetrization,” Ancel and Vintemberger, 1948; later
Chapter 4 ).
termed “cortical rotation,” Gerhart et al., 1989), (2) the role
DOI: 10.1201/9781003050230-4
25