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Development Genes and Evolution

, Volume 224, Issue 3, pp 159–174 | Cite as

Development of blastomere clones in the Ilyanassa embryo: transformation of the spiralian blastula into the larval body plan

  • Xin Yi Chan
  • J. David Lambert
Original Article

Abstract

Spiralian embryogenesis is deeply conserved and seems to have been in place in the last common ancestor of the large assemblage of protostome phyla known as the Lophotrochozoa. While the blastula fate maps of several spiralian embryos have been determined, little is known about the events that link the early embryo and the larva. For all cells in the Ilyanassa blastula, we determined the clonal morphology at four time points between the blastula and veliger stages. We found that ectomesoderm comes mostly from 3a and 3b, but also from 2c and 2b. We also observed the ingression and early proliferation of 3a- and 3b-derived ectomesoderm. We found cells in the 2b clone that marked the anterior edge of the blastopore and later the mouth and cells in the 3c/3d clones that marked the posterior edges of these structures. This demonstrates directly that the mouth forms in the same location as the blastopore. In the development of the shell field, we observed dramatic cell migration events that invert the positions of the 2b and 2d clones that contribute to the shell. Using time-lapse imaging, we followed and described the cleavage pattern of the conserved endomesodermal blast cell, 4d, up to 4d + 45 h, when there were 52 cells in the clone. Our results show the growth and movement of clones derived from cells of the spiralian blastula as they transform into the trochophore-like and veliger stages. They have implications for the evolution of the shell in gastropods, the origins of mesoderm in spiralians, and the evolution of mouth formation in metazoans.

Keywords

Mollusc Spiralian Fate map Lineage tracing 

Notes

Acknowledgments

We thank Morgan Goulding, Pamela Agbu and Adam Johnson for thoughtful comments on the manuscript. This work was supported by a grant by the N.S.F to J.D.L. (IOB-1146782).

Supplementary material

427_2014_474_MOESM1_ESM.mpg (1.3 mb)
Movie S1 Stack of confocal images of 1a clone at veliger larva stage. Anterior view. (MPG 1,374 kb)
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Movie S2 Stack of confocal images of 1c clone at veliger larva stage. Anterior view. (MPG 1,622 kb)
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Movie S3 Stack of confocal images of 1a clone at two day-old stage. Dorsal view. (MPG 2,012 kb)
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Movie S4 Stack of confocal images of 1c clone at two day-old stage. Dorsal view. (MPG 1,674 kb)
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Movie S5 Stack of confocal images of 1a clone at three day-old stage. Dorsal view. (MPG 1,326 kb)
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Movie S6 Stack of confocal images of 1c clone at three day-old stage. Dorsal view. (MPG 2,016 kb)
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Movie S7 Stack of confocal images of 1a clone at four day-old stage. Dorsal view. (MPG 1,732 kb)
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Movie S8 Stack of confocal images of 1c clone at four day-old stage. Dorsal view. (MPG 2,158 kb)
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Movie S9 Stack of confocal images of 1b clone at veliger larva stage. Anterior view. (MPG 766 kb)
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Movie S10 Stack of confocal images of 1b clone at two day-old stage. Dorsal view. (MPG 1,634 kb)
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Movie S11 Stack of confocal images of 1b clone at two day-old stage. Ventral view. (MPG 1,580 kb)
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Movie S12 Stack of confocal images of 1b clone at three day-old stage. Dorsal view. (MPG 1,530 kb)
427_2014_474_MOESM13_ESM.mpg (1.2 mb)
Movie S13 Stack of confocal images of 1b clone at four day-old stage. Dorsal view. (MPG 1,244 kb)
427_2014_474_MOESM14_ESM.mpg (870 kb)
Movie S14 Stack of confocal images of 1d clone at veliger larva stage. Anterior view. (MPG 870 kb)
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Movie S15 Stack of confocal images of 1d clone at two day-old stage. Dorsal view. (MPG 1,102 kb)
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Movie S16 Stack of confocal images of 1d clone at three day-old stage. Dorsal view. (MPG 1,134 kb)
427_2014_474_MOESM17_ESM.mpg (2.3 mb)
Movie S17 Stack of confocal images of 1d clone at four day-old stage. Ventral view. (MPG 2,316 kb)
427_2014_474_MOESM18_ESM.mpg (1.6 mb)
Movie S18 Stack of confocal images of 2a clone at veliger larva stage. Ventral view. (MPG 1,594 kb)
427_2014_474_MOESM19_ESM.mpg (1.3 mb)
Movie S19 Stack of confocal images of 2c clone at veliger larva stage. Ventral view. (MPG 1,316 kb)
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Movie S20 Stack of confocal images of 2c clone at veliger larva stage. Left view. (MPEG 1,109 kb)
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Movie S21 Stack of confocal images of 2a clone at two day-old stage. Posterior ventral view. (MPG 2,036 kb)
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Movie S22 Stack of confocal images of 2c clone at two day-old stage. Posterior ventral view. (MPG 2,156 kb)
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Movie S23 Stack of confocal images of 2a clone at three day-old stage. Ventral view. (MPG 1,358 kb)
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Movie S24 Stack of confocal images of 2c clone at three day-old stage. Ventral view. (MPG 2,020 kb)
427_2014_474_MOESM25_ESM.mpg (924 kb)
Movie S25 Stack of confocal images of 2a clone at four day-old stage. Ventral view. (MPG 924 kb)
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Movie S26 Stack of confocal images of 2c clone at four day-old stage. Ventral view. (MPG 992 kb)
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Movie S27 Stack of confocal images of 2c clone at four day-old stage. Dorsal view. (MPG 1,220 kb)
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Movie S28 Stack of confocal images of 2b clone at veliger larva stage. Anterior view. (MPG 1,566 kb)
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Movie S29 Stack of confocal images of 2b clone at two day-old stage. Ventral view. (MPG 1,344 kb)
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Movie S30 Stack of confocal images of 2b clone at three day-old stage. Dorsal view. (MPG 1,794 kb)
427_2014_474_MOESM31_ESM.mpg (1.4 mb)
Movie S31 Stack of confocal images of 2b clone at three day-old stage. Ventral view. (MPG 1,390 kb)
427_2014_474_MOESM32_ESM.docx (323 kb)
Fig. S32 The development of the 2b clone. (AD) Ventral view. At two days-old, the future mouth cells are positioned on the ventral midline and connected to the band of cells. During the transition from two day-old to three day-old, they disconnected from the band of cells and remain on the ventral midline. (EH) Dorsal view. At two day-old, the arms of the band of cells are apart from each other on the dorsal side. Transitioning from two day-old to three day-old, the arms of the band of cells extend and join at the dorsal side. In a three day-old embryo, the cells that are part of the shell field bud off from the joined arms. Green: Oregon Green dextran; Blue: DAPI. Dotted line: blastopore; asterisk: developing mouth. (DOCX 322 kb)
427_2014_474_MOESM33_ESM.mpg (1.1 mb)
Movie S33 Stack of confocal images of 2b clone at four day-old stage. Dorsal view. (MPG 1,154 kb)
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Movie S34 Stack of confocal images of 2b clone at four day-old stage. Ventral view. (MPG 1,930 kb)
427_2014_474_MOESM35_ESM.mpg (908 kb)
Movie S35 Stack of confocal images of 2d clone at veliger larva stage. Anterior view. (MPG 908 kb)
427_2014_474_MOESM36_ESM.mpg (1.2 mb)
Movie S36 Stack of confocal images of 2d clone at two day-old stage. Posterior dorsal view. (MPG 1,224 kb)
427_2014_474_MOESM37_ESM.mpg (2 mb)
Movie S37 Stack of confocal images of 2d clone at three day-old stage. Ventral view. (MPG 2,096 kb)
427_2014_474_MOESM38_ESM.mpg (1.2 mb)
Movie S38 Stack of confocal images of 2d clone at four day-old stage. Ventral view. (MPG 1,186 kb)
427_2014_474_MOESM39_ESM.mpg (3.3 mb)
Movie S39 Stack of confocal images of 3a clone at veliger larva stage. Anterior view. (MPG 3,396 kb)
427_2014_474_MOESM40_ESM.mpg (1.9 mb)
Movie S40 Stack of confocal images of 3b clone at veliger larva stage. Anterior view. (MPG 1,968 kb)
427_2014_474_MOESM41_ESM.mpg (606 kb)
Movie S41 Stack of confocal images of 3a clone at two day-old stage. Ventral view. (MPG 606 kb)
427_2014_474_MOESM42_ESM.mpg (432 kb)
Movie S42 Stack of confocal images of 3b clone at two day-old stage. Ventral view. (MPG 432 kb)
427_2014_474_MOESM43_ESM.docx (240 kb)
Fig. S43 The mesodermal population derived from the ectomesodermal clone, 3a. (AB) Ventral view of two day-old embryo. (A) Projection of stacks of mesodermal layers in the two day-old embryo. The mesodermal progenitor cells derived from the 3a clone is shown. (B) Projection of a whole mount embryo showing the clonal distribution of the 3a cell. (CD) Ventral view of three day-old embryo. (C) Projection of stacks of mesodermal layers in the three day-old embryo. The mesodermal population has divided and extended to the posterior region. Meanwhile, the esophageal cell sheet (ectodermal) has started internalizing through the future mouth opening. (D) Projection of a whole mount three day-old embryo showing the 3a lineage. Green is lineage tracer. Blue is DAPI staining of nuclei. Red is phalloidin staining of filamentous actin. (DOCX 239 kb)
427_2014_474_MOESM44_ESM.mpeg (1.1 mb)
Movie S44 Stack of confocal images of 3a clone at three day-old stage. Ventral view. Red: rhodamine dextran; cyan blue: phalloidin; Blue: DAPI. (MPEG 1,109 kb)
427_2014_474_MOESM45_ESM.mpg (1.1 mb)
Movie S45 Stack of confocal images of 3b clone at three day-old stage. Ventral view. (MPG 1,128 kb)
427_2014_474_MOESM46_ESM.mpg (2.1 mb)
Movie S46 Stack of confocal images of 3a clone at four day-old stage. Ventral view. Red: rhodamine dextran; cyan blue: phalloidin; Blue: DAPI. (MPG 2,132 kb)
427_2014_474_MOESM47_ESM.mpg (892 kb)
Movie S47 Stack of confocal images of 3b clone at four day-old stage. Ventral view. (MPG 892 kb)
427_2014_474_MOESM48_ESM.mpg (1 mb)
Movie S48 Stack of confocal images of 3c clone at veliger larva stage. Anterior view. (MPG 1,046 kb)
427_2014_474_MOESM49_ESM.mpg (746 kb)
Movie S49 Stack of confocal images of 3d clone at veliger larva stage. Anterior view. (MPG 746 kb)
427_2014_474_MOESM50_ESM.mpeg (869 kb)
Movie S50 Stack of confocal images of 3c clone at two day-old stage. Posterior ventral view. (MPEG 869 kb)
427_2014_474_MOESM51_ESM.mpg (1.3 mb)
Movie S51 Stack of confocal images of 3d clone at two day-old stage. Posterior ventral view. (MPG 1,350 kb)
427_2014_474_MOESM52_ESM.mpg (3.4 mb)
Movie S52 Stack of confocal images of 3c clone at three day-old stage. Ventral view. (MPG 3,512 kb)
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Movie S53 Stack of confocal images of 3d clone at three day-old stage. Ventral view. (MPG 1,558 kb)
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Movie S54 Stack of confocal images of 3c clone at four day-old stage. Ventral view. (MPG 1,120 kb)
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Movie S55 Stack of confocal images of 3d clone at four day-old stage. Ventral view. (MPG 2,798 kb)
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Movie S56 Stack of confocal images of 3c clone at veliger larva stage. Right view. (MPEG 1,019 kb)
427_2014_474_MOESM57_ESM.mpg (1 mb)
Movie S57 Stack of confocal images of 4A clone at two day-old stage. Ventral view. (MPG 1,058 kb)
427_2014_474_MOESM58_ESM.mpg (1.3 mb)
Movie S58 Stack of confocal images of 4B clone at two day-old stage. Ventral view. (MPG 1,356 kb)
427_2014_474_MOESM59_ESM.mpg (1.3 mb)
Movie S59 Stack of confocal images of 4C clone at two day-old stage. Ventral view. (MPG 1,306 kb)
427_2014_474_MOESM60_ESM.mpg (962 kb)
Movie S60 Stack of confocal images of 4A clone at three day-old stage. Ventral view. (MPG 962 kb)
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Movie S61 Stack of confocal images of 4B clone at three day-old stage. Ventral view. (MPG 1,870 kb)
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Movie S62 Stack of confocal images of 4C clone at three day-old stage. Ventral view. (MPG 1,646 kb)
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Movie S63 Stack of confocal images of 4A clone at four day-old stage. Right view. (MPG 1,462 kb)
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Movie S64 Stack of confocal images of 4B clone at four day-old stage. Right view. (MPG 1,094 kb)
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Movie S65 Stack of confocal images of 4C clone at four day-old stage. Right view. (MPG 1,500 kb)
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Movie S66 Stack of confocal images of 4A clone at veliger larva stage. Left view. (MPG 6,466 kb)
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Movie S67 Stack of confocal images of 4B clone at veliger larva stage. Left view. (MPG 1,268 kb)
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Movie S68 Stack of confocal images of 4C clone at veliger larva stage. Left view. (MPG 1,576 kb)
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Movie S69 Stack of confocal images of 4a clone at two day-old stage. Posterior ventral view. (MPG 1,246 kb)
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Movie S70 Stack of confocal images of 4b clone at two day-old stage. Posterior ventral view. (MPG 1,204 kb)
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Movie S71 Stack of confocal images of 4c clone at two day-old stage. Posterior ventral view. (MPG 1,124 kb)
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Movie S72 Stack of confocal images of 4a clone at three day-old stage. Ventral view. (MPG 1,434 kb)
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Movie S73 Stack of confocal images of 4b clone at three day-old stage. Ventral view. (MPG 2,014 kb)
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Movie S74 Stack of confocal images of 4c clone at three day-old stage. Ventral view. (MPG 1,654 kb)
427_2014_474_MOESM75_ESM.mpg (884 kb)
Movie S75 Stack of confocal images of 4a clone at four day-old stage. Ventral view. (MPG 884 kb)
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Movie S76 Stack of confocal images of 4b clone at four day-old stage. Dorsal view. (MPG 1,668 kb)
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Movie S77 Stack of confocal images of 4c clone at four day-old stage. Ventral view. (MPG 1,058 kb)
427_2014_474_MOESM78_ESM.mpg (1 mb)
Movie S78 Stack of confocal images of 4a clone at veliger larva stage. Right view. (MPG 1,044 kb)
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Movie S79 Stack of confocal images of 4b clone at veliger larva stage. Right view. (MPG 942 kb)
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Movie S80 Stack of confocal images of 4c clone at veliger larva stage. Left view. (MPG 2,228 kb)
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Movie S81 Stack of confocal images of 4d clone at two day-old stage. Posterior dorsal view. (MPG 1,968 kb)
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Movie S82 Stack of confocal images of 4d clone at three day-old stage. Ventral view. (MPG 2,226 kb)
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Movie S83 Stack of confocal images of 4d clone at four day-old stage. Ventral view. (MPG 4,234 kb)
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Movie S84 Stack of confocal images of 4d clone at veliger larva stage. Dorsal view. (MPG 2,800 kb)
427_2014_474_MOESM85_ESM.docx (98 kb)
Fig. S85 4d blast cell lineage. The reference lineage is the most extended lineage obtained and thus, is used as reference for comparison to other lineages examined. Lineages after the 4d + 24 h mark are derived from the live-time imaging result of four different embryos including the reference embryo. Left axis is time after the birth of 4d. Color code: long orange line (t = 4d + 24 h mark); black lines (reference); red, blue and green lines each represents division happened in three other individual lineages examined. (DOCX 98 kb)
Movie S86

Time-lapse movie of cell divisions in the 4d lineages. This time-lapsed movie was recorded at 4d + 26.5 h when each side of the lineage contains 12 cells. Chromatin is visualized with H2B-eGFP. Dorsal view. (MPG 5,794 kb)

427_2014_474_MOESM87_ESM.docx (220 kb)
Fig. S87 The development of the foregut: mouth and esophagus. The positions of the 2nd quartet cells (2a and 2b) and 3rd quartet cells (3a) in relation to the blastopore and the developing mouth. (AB) Double labeling of the 2a (green) and 3a (red) clones in two day-old and three day-old embryos. (CD) Double labeling of the 2b (green) and 3a (red) clones in two day-old and three day-old embryos. Green: Oregon Green dextran; Red: Rhodamine dextran; Blue: DAPI. Dotted line: blastopore/developing mouth. (DOCX 219 kb)
427_2014_474_MOESM88_ESM.mpeg (3.3 mb)
Movie S88 Stack of confocal images of 2a and 3a double labeling at two day-old stage. Ventral view. Red: Rhodamine dextran (3a); Green: Oregon green dextran (2a); cyan blue: phalloidin; Blue: DAPI. (MPEG 3,374 kb)
427_2014_474_MOESM89_ESM.mpeg (1.2 mb)
Movie S89 Stack of confocal images of 2a and 3a double labeling at three day-old stage. Ventral view. Red: Rhodamine dextran (3a); Green: Oregon green dextran (2a); cyan blue: phalloidin; Blue: DAPI. (MPEG 1,198 kb)
427_2014_474_MOESM90_ESM.mpeg (924 kb)
Movie S90 Stack of confocal images of 2b and 3a double labeling at two day-old stage. Ventral view. Red: Rhodamine dextran (3a); Green: Oregon green dextran (2b); cyan blue: phalloidin; Blue: DAPI. (MPEG 923 kb)
427_2014_474_MOESM91_ESM.mpeg (1.2 mb)
Movie S91 Stack of confocal images of 2b and 3a double labeling at three day-old stage. Ventral view. Red: Rhodamine dextran (3a); Green: Oregon green dextran (2b); cyan blue: phalloidin; Blue: DAPI. (MPEG 1,241 kb)
427_2014_474_MOESM92_ESM.docx (221 kb)
Fig. S92 Shell field invagination in early trochophores. (AD) Individual labeling of all 2nd quartet micromeres. (A) 2a clone contributes to upper left part of the shell field. (B) 2c clone contributes to upper right part of the shell field. (C) Higher magnification of the 2b clone contribution to the upper middle part of the shell gland. (D) 2d clone gives rise to a portion of the ventral part of the shell gland that is similar in size to the 2a and 2c contributions. Green: Oregon Green dextran; Blue: DAPI. (DOCX 220 kb)
427_2014_474_MOESM93_ESM.docx (341 kb)
Fig. S93 Summary of the early cell lineages and the contributions derived from fate mapping. Abbreviation: L, Left; R, Right. (DOCX 340 kb)

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of BiologyUniversity of RochesterRochesterUSA

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