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WIREs Dev Biol
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The maternal muscle determinant in the ascidian egg

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Muscle formation in ascidian embryos has been investigated for more than a century as a representative example of cell fate specification by localized maternal factors within the egg cytoplasm. Observations of colored cytoplasm in combination with micromanipulation techniques have suggested the presence of a muscle‐forming factor. The molecular basis has been elucidated with the discovery of macho‐1. macho‐1 mRNA is already present in the unfertilized egg, and translocates to the posterior region of the egg during ooplasmic movements. It encodes a zinc‐finger transcription factor that positively regulates the expression of target genes. macho‐1‐binding cis‐elements have been identified in muscle‐specific zygotic genes. Maternally localized macho‐1 appears to have originated in the ascidian lineage, but it activates a muscle‐forming developmental program that is shared by the vertebrates. macho‐1 is also involved in establishment of the anterior–posterior axis as a competence factor in mesenchyme induction in the posterior region. It is suggested that translation of the macho‐1 protein is initiated at the eight‐cell stage, and that the protein is inherited by all descendant blastomeres of the posterior‐vegetal region. The macho‐1 activities in nonmuscle descendants are suppressed or modified by cell interactions during the cleavage stages. In addition to the primary muscle specified by maternal macho‐1, ascidian embryos develop secondary muscle, whose fate is determined by cell interactions. Dozens of maternal mRNAs show similar localization to macho‐1, and these are known as postplasmic/PEM RNAs, being also involved in various posterior‐specific developmental events. Evolutionary aspects relevant to macho‐1 and tail muscle formation are also discussed in this article. WIREs Dev Biol 2012, 1:425–433. doi: 10.1002/wdev.22

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Figure 1.

The ascidian, Halocynthia roretzi. (a) Adult. (b) Neurula with closing neural tube on the dorsal side.1 (c) Tadpole larva just before hatching at 35 h of development.

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Figure 2.

Ooplasmic movements and localization of various factors. Cytoplasmic and cortical reorganization proceed in two major phases during the first cell cycle. (a) Yellow myoplasm in Styela partita. Copy of the original drawings by Conklin (1905).5 Yellow cytoplasm is localized to the unfertilized egg cortex. It is concentrated at the vegetal pole just after fertilization, then gradually moves toward the future posterior pole before the first cleavage takes place. It is segregated into the posterior‐vegetal muscle lineage blastomeres, and eventually into tail muscle cells of the tadpole larva. (b) Distribution of muscle‐forming activity inferred from the results of cytoplasmic transfer experiments. (c) Localization of maternal mRNA of macho‐1. Ani, animal pole; Veg, vegetal pole; Ant, anterior; Post, posterior. (Reprinted with permission from Ref 7. Copyright 2001 Nature Publishing Group)

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Figure 3.

macho‐1 as a muscle determinant. (a),(b) Larval morphology and myosin expression in tail muscle cells in the control experiment. (c)–(e) Larvae in which antisense oligonucleotide against macho‐1 mRNA has been injected. (f)–(h) Muscle actin mRNA expression at the 110‐cell stage. (i) Myosin expression in larvae into which macho‐1 mRNA has been injected. (j) Nuclear localization of flag‐tagged macho‐1 protein that was translated from injected mRNA, in every nucleus at the 110‐cell stage. (Reprinted with permission from Ref 7. Copyright 2001 Nature Publishing Group)

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Figure 4.

The primary (green) and secondary (orange and red) muscle lineages.33 Primary muscle cells are derived from the B‐line (posterior‐vegetal) blastomeres. Secondary muscle cells originate from the A‐line (anterior‐vegetal) and b‐line (posterior‐animal) blastomeres. macho‐1 is involved in muscle fate determination in the primary lineage. Anterior is to the left. Note that the anterior‐posterior order of muscle progenitor cells is reversed during the gastrula and neurula stages.

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Figure 5.

Fate specification in the vegetal hemisphere at the 32‐cell and 64‐cell stages.34 Anterior is to the left. An FGF signal (arrows) secreted from the vegetal endoderm blastomeres promotes asymmetric cell divisions in the marginal zone. The signal induces notochord and mesenchyme fates. The default fates are nerve cord and muscle, respectively. Sister blastomeres are connected with bars.

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Comparative Development and Evolution > Body Plan Evolution
Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
Early Embryonic Development > Fertilization to Gastrulation