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WIREs Dev Biol
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Cytoplasmic localization and reorganization in ascidian eggs: role of postplasmic/PEM RNAs in axis formation and fate determination

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Localization of maternal molecules in eggs and embryos and cytoplasmic movements to relocalize them are fundamental for the orderly cellular and genetic processes during early embryogenesis. Ascidian embryos have been known as ‘mosaic eggs’ because of their autonomous differentiation abilities based on localized cell fate determinants. This review gives a historical overview of the concept of cytoplasmic localization, and then explains the key features such as ooplasmic movements and cell lineages that are essential to grasp the process of ascidian development mediated by localized determinant activities. These activities are partly executed by localized molecules named postplasmic/PEM RNAs, originating from approximately 50 genes, of which the muscle determinant, macho‐1, is an example. The cortical domain containing these RNAs is relocalized to the posterior‐vegetal region of the egg by cytoskeletal movements after fertilization, and plays crucial roles in axis formation and cell fate determination. The cortical domain contains endoplasmic reticulum and characteristic granules, and gives rise to a subcellular structure called the centrosome‐attracting body (CAB), in which postplasmic/PEM RNAs are highly concentrated. The CAB is responsible for a series of unequal partitionings of the posterior‐vegetal cytoplasmic domain and the postplasmic/PEM RNAs at the posterior pole during cleavage. Some components of this domain, which is rich in granules, are eventually inherited by prospective germline cells with particular postplasmic/PEM RNAs such as vasa. The postplasmic/PEM RNAs are classified into two groups according to their final cellular destinations and localization pathways. Localization of these RNAs is regulated by specific nucleotide sequences in the 3′ untranslated regions (3′UTRs). WIREs Dev Biol 2012, 1:501–518. doi: 10.1002/wdev.54

This article is categorized under:

  • Establishment of Spatial and Temporal Patterns > Cytoplasmic Localization
  • Early Embryonic Development > Fertilization to Gastrulation
  • Early Embryonic Development > Development to the Basic Body Plan

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Figure 1.

Ooplasmic movements and localization of the postplasmic/PEM RNA in ascidians. Cytoplasmic and cortical reorganization proceeds in two major phases during the first cell cycle. Eggs of the respective stages in (a–e) are shown in the same orientation. (a) Yellow myoplasm in Styela partita. Copy of the original drawings by Conklin (1905).9 (b) Sections of eggs of Halocynthia roretzi. Yolk granules are stained green, and other cytoplasm is colored red.10 (c) Scanning electron microscope (SEM) images of gastrula and tailbud embryos of H. roretzi.11 (d) Localization of maternal messenger RNA (mRNA) of Hr‐pem showing the typical localization pattern of postplasmic/PEM RNAs. When movements of the egg cytoplasm are complete, it is localized to the posterior‐vegetal egg cytoplasm/cortex (PVC). By the 8‐cell stage, Hr‐PEM1 mRNA is highly concentrated into the centrosome‐attracting body (CAB, red arrow). (Reproduced with permission from Ref 12. Copyright 2007 Elsevier) (e) Diagram showing ooplasmic movements. The first phase is driven by contraction of cortical microfilaments. In the second phase, mitochondria‐rich myoplasm and the postplasmic/PEM RNAs associated with the cortical endoplasmic reticulum (cER) translocate to the future posterior region. This movement is mediated by microtubules extending from the sperm centrosome. (Reproduced with permission from Ref 13. Copyright 1999 the Company of Biologists) ani, animal pole; ant, anterior; post, posterior; veg, vegetal pole.

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Figure 2.

Fate map at the 110‐cell (late blastula/initial gastrula) stage.30 Every blastomere faces the surface of the embryo at this stage. Anterior is up. Names of blastomeres are indicated. (a) Animal hemisphere. (b) Vegetal hemisphere. (c) Organization of tailbud embryos. Mid‐sagittal plane, sagittal plane, and transverse section of the tail. Note that a pair of B7.6 blastomeres at the posterior pole of the vegetal hemisphere in (b) carry the centrosome‐attracting body (CAB) and the postplasmic/PEM RNAs, and develop into the primordial germ cells close to the tip of the tail in (c). TLC, trunk lateral cells; TVC, trunk ventral cells.

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Figure 3.

Localization of maternal factors from fertilization to the 8‐cell stage.1 The different colors indicate localization of different maternal determinants, as inferred from ooplasmic removal and transplantation experiments. The centrosome‐attracting body (CAB) is present in the posterior region of the B4.1 blastomeres of the 8‐cell embryos. The right‐most picture shows localization and inheritance of the postplasmic/PEM RNAs. These RNAs are eventually concentrated into the CAB and inherited by the posterior‐most blastomeres during cleavage.

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Figure 4.

Localization of the postplasmic RNAs of Halocynthia roretzi (Hr) and Ciona intestinalis (Ci) after completion of the second phase of ooplasmic movement. The left three pictures are representative examples of strong localization to the posterior‐vegetal cytoplasm/cortex (PVC). These expression patterns are well conserved in both species. In the right‐hand column, significant staining of the entire egg cytoplasm is evident, in addition to a higher signal in the PVC. (Reproduced with permission from Refs 47, 51, and 52. Copyright 2005, 2003, 2003 Elsevier)

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Figure 5.

Three rounds of unequal cell division during cleavage in ascidian embryos.58 The cleavage pattern is well conserved among species. Sister cells are connected with green bars. Red‐colored blastomeres, which contain the centrosome‐attracting body (CAB) and pem messenger RNA (mRNA), divide unequally in size into larger and smaller daughter cells, always producing small daughter cells at the posterior pole. The smaller daughter cell divides unequally again up to the 64‐cell stage. The names of the blastomeres are indicated at the bottom. Size of the letters corresponds to size of the cells. Ant, anterior; Post, posterior.

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Figure 6.

Centrosome‐attracting body (CAB). (a) Microtubule staining of the 16‐cell Halocynthia embryo. Posterior is to the right. Vegetal view. In the posterior region, the blastomere has divided unequally into larger and smaller blastomeres during the previous cell division. Microtubules emanating from the centrosome (arrows) focus on the CAB in the smaller posterior blastomere, which will divide unequally again.58 (b) The CAB (arrowheads) in extracted and cleared embryo.58 (c and d) Ultrastructures of the entire CAB in Halocynthia and Ciona.60 Median plane is indicated by blue arrows. (e) Closer view of the boundary of the CAB. Asterisks indicate an electron‐dense matrix, which resembles the germ granules in other organisms.60 ant, anterior; ER, rough endoplasmic reticulum‐like tubules; M, mitochondria; post, posterior.

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Figure 7.

Localization of postplasmic/PEM RNAs. (a and b) Distribution of PEM‐1 (pem) and VH (vasa homolog) RNAs in Ciona intestinalis at the tailbud stage. PEM‐1 is detected only in B8.11 cells (arrowheads), while VH is also inherited by B8.12 cells (arrows). (Reproduced with permission from Ref 70. Copyright 2006 the Company of Biologists) (c and d) High‐resolution fluorescence detection of PEM‐1 and macho‐1 messenger RNAs (mRNAs) (green) in the isolated cortices of Halocynthia roretzi unfertilized eggs (c) and the centrosome‐attracting body (CAB) of the 8‐cell embryo (d). The cortical endoplasmic reticulum (cER) is stained red with a lipophilic fluorescent dye. These mRNAs are colocalized with the cER.78 (e and f) macho‐1 and vasa mRNAs (arrowheads, green) in the isolated cortices of Phallusia mammillata unfertilized eggs. macho‐1 mRNA is colocalized with the cER, while vasa mRNA shows granular localization. (Reproduced with permission from Ref 50. Copyright 2009 Elsevier)

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