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Left-right positioning of the adult rudiment in sea urchin larvae is directed by the right side

Department of Integrated Biosciences, Graduate School of Frontier Science, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba Prefecture 277-8562, Japan

View larger version (85K): [in a new window]   Fig. 1. Vital dye staining of the embryos. The embryos are viewed from the aboral (dorsal) side, with the animal side at the top. The left and right sides of the embryos correspond to those of the viewer. (A) An early gastrula H. pulcherrimus embryo stained with Nile Blue dye on the right side (arrow). The pressure of the glass needle has slightly indented the embryo along the midplane (arrowheads), through which the embryo is about to be dissected. (B) An H. pulcherrimus larva derived from the left half of an embryo that had been stained on the left side and dissected along the midplane in the early gastrula stage. The archenteron of the half larva is indicated by arrowheads. The staining is on the left side of the half larva (arrow). Scale bar: 100 µm.

View larger version (153K): [in a new window]   Fig. 2. LR placement of the adult rudiment in left and right half of S. mirabilis larvae dissected in the early or mid-late gastrula stage. The LR axis of a larva coincides with that of a gastrula embryo. The axial relationship of the animal-vegetal and the oral-aboral embryonic axes is as follows: the larval oral (anterior) side corresponds to the embryonic oral side, while the larval-ventral and the larval-dorsal sides correspond to the vegetalmost and the animal-side portions, respectively, of the embryonic aboral side. The larvae are viewed from the dorsal side, with the oral side at the top. The left and right sides of the larvae correspond to those of the viewer. (A) A larva corresponding to the six-armed pluteus derived from the right half dissected in the early gastrula stage and developing an adult rudiment on the left side (arrow). (B) A larva corresponding to the six-armed pluteus derived from the left half dissected in the early gastrula stage and containing a developing hydrocoel (white arrow) on the right side. Evidence of the vestibule (black arrows) is also visible on the right side of the larva. (C) A larva corresponding to the six-armed pluteus derived from the left half dissected in the early gastrula stage, with a vestibule (black arrow) and a hydrocoel (white arrows) developing on the left side. (D) A larva corresponding to the six-armed pluteus derived from the left half dissected in the mid-late gastrula stage and developing an adult rudiment on the right side (large arrow). The left anterolateral arm (small arrow with c) and skeletal rod of the right anterolateral arm (small arrow with d) and the left (small arrow with a) and right (small arrow with e) postdorsal arms are growing in the half larva. No postoral arm is growing on the cut side of the larva, but the left postoral arm (small arrow with b) can be seen to be growing in the larva. Scale bars: 100 µm.

View larger version (28K): [in a new window]   Fig. 3. Comparison of the arm length of larvae derived from the left and the right halves of embryos dissected in the gastrula stage. (A) This larva corresponds to the six-armed pluteus derived from the left half and shows the parts of the larvae that were measured. The length of the anterolateral-arm-rod plus body-rod (al-length), postoral-arm-rod plus body rod (po-length), and the postdorsal-arm-rod (pd-length) were measured. (B) Differences in the arm length of the left and the right half larvae. The al-length on the unoperated side represents the length of the larva along the anteroposterior axis in the late larval stage. The ratio of the length of the arms on the cut side to the anteroposterior length of one larva is plotted, and the differences in arm length on the cut side between populations are shown. The plots for both the al- and the pd-lengths on the cut side of S. mirabilis show similar distributions in the group with right halves and a left rudiment, the group with left halves and a left rudiment, and the group with left halves and a right rudiment. The plots also show similar distributions for the al-length on the cut side of the H. pulcherrimus larvae in the group with left halves and a left rudiment, and the group with left halves and a right rudiment.

View larger version (58K): [in a new window]   Fig. 4. LR positioning of the hydropore canal in the left half H. pulcherrimus larvae dissected in the mid-late gastrula stage. Two left lateral views of a four-armed pluteus, with the oral side (anterior side) to the left of the figures are shown. (A) A larva with the focal plane on the left coelomic sac (arrow). No hydrocoel has developed from the left coelomic sac. (B) The same larva as shown in A, with the focal plane on the right coelomic sac. A hydrocoel (arrow) is seen developing from the right coelomic sac. Scale bar: 100 µm.

View larger version (63K): [in a new window]   Fig. 5. Excision of the tissue lateral to the midline, including a part of archenteron and ecto-mesodermal tissue. The embryos are viewed from the aboral side, with the animal side at the top, and the larvae are viewed from the dorsal side, with the oral side at the top. The left and right sides of the embryos correspond to those of the viewer. (A,B) A schematic drawing (A) and a bright field image (B) of an embryo subjected to the right EME cut. (A) The mid-sagittal plane of the embryo is represented by a broken line and the cut plane by a broad line. (B) An S. mirabilis embryo after the right EME cut. The right animal side of the embryo has been removed. The embryo was first marked with the glass needle in the mid-sagittal plane (arrows) to confirm that the cut region has not invaded the left side of the embryo. The upper part of the archenteron in the right side area was removed. The region corresponding to the ablated archenteron on the left side remains in the embryo. (C) A fixed specimen of two-armed pluteus larvae of S. mirabilis after the right EME cut in the gastrula stage. At this stage, the operated right side of the larva is smaller than the intact left side. The right coelomic sac (arrows) has formed on the right side of the foregut. The right coelomic sac is smaller than the left coelomic sac (arrowheads). (D,E). A schematic drawing (D) and a bright field image (E) of an embryo in which the right vegetal side has been removed. (D) The mid-sagittal plane of the embryo is represented by the broken line, and the cut plane by the broad line. (E) An H. pulcherrimus embryo whose right vegetal side (arrow) has been removed. (F) An S. mirabilis embryo subjected to the sham operation. The embryo is almost completely divided in the mid-sagittal plane (arrows). Scale bars: 50 µm.

View larger version (77K): [in a new window]   Fig. 6. LR placement of the adult rudiment in the late pluteus H. pulcherrimus larvae from which part of the tissue lateral to the midplane, including the archenteron and the ecto-mesodermal tissues, has been removed in the mid-late gastrula stage. The larvae are viewed from the dorsal side, with the oral side at the top. The left and right sides of the larvae correspond to those of the viewer. (A) An eight-armed pluteus larva of H. pulcherrimus subjected to the right EME cut in the gastrula stage, as shown in Fig. 5A,B. The adult rudiment has formed on the right side of the larval body (arrow). (B) A control S. mirabilis larva in the early stage of adult rudiment formation. A vestibule (large arrow) and a hydrocoel (small arrow) have formed on the left side of the larva. There are no marks for vestibule formation in the ectoderm (large arrowhead) and for hydrocoel formation in the right coelomic sac (small arrowhead) on the right side of the larva. (C) An S. mirabilis pluteus larva in the early stage of adult rudiment formation that was subjected to the right EME cut in the gastrula stage. A vestibule (black arrow) and a hydrocoel (white arrow) have formed on the right side of the larva. Note that there are no marks for vestibule formation in the ectoderm (black arrowhead) or for hydrocoel formation in the left coelomic sac (white arrowhead) on the left side of the larva. (D) A six-armed pluteus H. pulcherrimus larva from which the tissue on the right vegetal side has been removed in the mid-late gastrula stage as shown in Fig. 5D,E. A vestibule (large arrow) and a hydrocoel (small arrow) have formed on the left side of the larval body. The right postoral arm did not regenerate and is absent, whereas the left postoral arm (arrowhead) is intact. Scale bars: 100 µm.

View larger version (47K): [in a new window]   Fig. 7. Excision of ecto-mesodermal tissue lateral to the midplane, avoiding the archenteron (EM cut). (A,B) A schematic drawing (A) of ablations of ecto-mesodermal tissue lateral to the archenteron (right EM cut) and a bright field image (B) of an embryo subjected to the right EM cut. The embryos are viewed from the aboral side, with the animal side at the top. (A) The mid-sagittal plane of the embryo is represented by a broken line, and the cut plane by a broad line. (B) An S. mirabilis embryo subjected to the right EM cut. The right animal region lateral to the archenteron was removed from the embryo. The epithelium of the embryo has adhered at the cut plane so that the cut end is closed. The archenteron was not severely damaged and is almost intact. (C) An oral side view of a two-armed pluteus S. mirabilis larva subjected to the right EM cut. The animal side is towards the top, and thus the left and the right sides of the larva are on the right and the left, respectively, of the viewer. The morphology of the coelom of the right coelomic sac (arrow with r) on the cut side appears normal, the same as the left coelomic sac (arrow with l). Scale bars: 50 µm in B and 100 µm in C.

View larger version (52K): [in a new window]   Fig. 8. LR placement of the adult rudiment in the left and right half H. pulcherrimus larvae dissected in the two-armed pluteus stage. The larvae are viewed from the dorsal side, with the oral side (anterior side) at the top. The left and right sides of the larvae correspond to those of the viewer. (A) A larva corresponding to the six-armed pluteus derived from the left half dissected in the two-armed pluteus stage, with an adult rudiment on both the left and the right sides (arrows). (B) A larva corresponding to the six-armed pluteus derived from the right half dissected in the two-armed pluteus stage, with an adult rudiment on the left side (arrow). Scale bar: 100 µm.

View larger version (31K): [in a new window]   Fig. 9. A schematic representation of the LR placement of the adult rudiment in the left and the right half larvae subjected to dissection at three different stages during the period from the early gastrula stage to the two-armed pluteus stage. The left side of the left halves (colored blue in A-C) and the right side of the right halves (colored green in D-F) have been untouched by the dissecting operation. The LR placement of the adult rudiment in the left halves showed distinct patterns according to the stage at which they were dissected. Larvae with a left adult rudiment and larvae with a right adult rudiment were found in about equal proportions after dissection in the early gastrula stage (A). Almost all of the left half larvae formed a right adult rudiment after dissection in the mid-late gastrula stage (B), and the left half larvae formed a left- and a right-adult rudiment after dissection in the prism-pluteus stage (C). Normal LR placement of the adult rudiment was always re-established in the right halves dissected in the early gastrula stage (D), the mid-late gastrula (E) and in the prism-pluteus stage (F).

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