Publications

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2017
Lyons, DC, Perry KJ, Henry JQ.  2017.  Morphogenesis along the animal-vegetal axis: fates of primary quartet micromere daughters in the gastropod Crepidula fornicata. Bmc Evolutionary Biology. 17   10.1186/s12862-017-1057-1   AbstractWebsite

Background: The Spiralia are a large, morphologically diverse group of protostomes (e.g. molluscs, annelids, nemerteans) that share a homologous mode of early development called spiral cleavage. One of the most highly-conserved features of spiralian development is the contribution of the primary quartet cells, 1a-1d, to the anterior region of the embryo (including the brain, eyes, and the anterior ciliary band, called the prototroch). Yet, very few studies have analyzed the ultimate fates of primary quartet sub-lineages, or examined the morphogenetic events that take place in the anterior region of the embryo. Results: This study focuses on the caenogastropod slipper snail, Crepidula fornicata, a model for molluscan developmental biology. Through direct lineage tracing of primary quartet daughter cells, and examination of these cells during gastrulation and organogenesis stages, we uncovered behaviors never described before in a spiralian. For the first time, we show that the 1a(2)-1d(2) cells do not contribute to the prototroch (as they do in other species) and are ultimately lost before hatching. During gastrulation and anterior-posterior axial elongation stages, these cells cleavage-arrest and spread dramatically, contributing to a thin provisional epidermis on the dorsal side of the embryo. This spreading is coupled with the displacement of the animal pole, and other pretrochal cells, closer to the ventrally-positioned mouth, and the vegetal pole. Conclusions: This is the first study to document the behavior and fate of primary quartet sub-lineages among molluscs. We speculate that the function of 1a(2)-1d(2) cells (in addition to two cells derived from 1d(12), and the 2b lineage) is to serve as a provisional epithelium that allows for anterior displacement of the other progeny of the primary quartet towards the anterior-ventral side of the embryo. These data support a new and novel mechanism for axial bending, distinct from canonical models in which axial bending is suggested to be driven primarily by differential proliferation of posterior dorsal cells. These data suggest also that examining sub-lineages in other spiralians will reveal greater variation than previously assumed.

2015
Lyons, DC, Perry KJ, Henry JQ.  2015.  Spiralian gastrulation: germ layer formation, morphogenesis, and fate of the blastopore in the slipper snail Crepidula fornicata. Evodevo. 6   10.1186/s13227-015-0019-1   AbstractWebsite

Background: Gastrulation is a critical step in bilaterian development, directly linked to the segregation of germ layers, establishment of axes, and emergence of the through-gut. Theories about the evolution of gastrulation often concern the fate of the blastopore (site of endomesoderm internalization), which varies widely in a major branch of bilaterians, the Spiralia. In this group, the blastopore has been said to become the mouth, the anus, both, or neither. Different developmental explanations for this variation exist, yet no modern lineage tracing study has ever correlated the position of cells surrounding the blastopore with their contribution to tissues of the mouth, foregut, and anus in a spiralian. This is the first study to do so, using the gastropod Crepidula fornicata. Results: Crepidula gastrulation occurs by epiboly: the first through third quartet micromeres form an epithelial animal cap that expands to cover vegetal endomesodermal precursors. Initially, descendants of the second and third quartet micromeres (2a-2d, 3a-3d) occupy a portion of the blastopore lip. As the blastopore narrows, the micromeres' progeny exhibit lineage-specific behaviors that result in certain sublineages leaving the lip's edge. Anteriorly, cells derived from 3a(2) and 3b(2) undergo a unique epithelial-to-mesenchymal transition involving proliferation and a collective movement of cells into the archenteron. These cells make a novel spiralian germ layer, the ectomesoderm. Posteriorly, cells derived from 3c(2) and 3d(2) undergo a form of convergence and extension that involves zippering of cells and their intercalation across the ventral midline. During this process, several of these cells, as well as the 2d clone, become displaced posteriorly, away from the blastopore. Progeny of 2a-2c and 3a-3d make the mouth and foregut, and the blastopore becomes the opening to the mouth. The anus forms days later, as a secondary opening within the 2d(2) clone, and not from the classically described "anal cells", which we identify as the 3c(221) and 3d(221) cells. Conclusions: Our analysis of Crepidula gastrulation constitutes the first description of blastopore lip morphogenesis and fates using lineage tracing and live imaging. These data have profound implications for hypotheses about the evolution of the bilaterian gut and help explain observed variation in blastopore morphogenesis among spiralians.

2006
Agee, SJ, Lyons DC, Weisblat DA.  2006.  Maternal expression of a NANOS homolog is required for early development of the leech Helobdella robusta. Developmental Biology. 298:1-11.   10.1016/j.ydbio.2006.04.473   AbstractWebsite

The gene nanos (nos) is a maternal posterior group gene required for normal development of abdominal segments and the germ line in Drosophila. Expression of nos-related genes is associated with the germ line in a broad variety of other taxa, including the leech Helobdella robusta, where zygotically expressed Hro-nos appears to be associated with primordial germ cells. The function of maternally inherited Hro-nos transcripts remains to be determined, however. Here, the function of maternal Hro-nos is examined using an antisense morpholino (MO) knockdown strategy, as confirmed by immunostaining and western blot analysis. HRO-NOS knockdown embryos exhibit abnormalities in the distribution of micromeres during cleavage. Subsequently, their germinal bands are positioned abnormally with respect to the embryonic midline and the micromere cap, epiboly fails, and the HRO-NOS knockdown embryos die. This lethality can be rescued by injection of mRNA encoding an eGFP::HRO-NOS fusion protein. HRO-NOS knockdown embryos make their normal complements of mesodermal and ectodermal teloblasts, and the progeny of these teloblasts segregate into distinct mesodermal and ectodermal layers. These results suggest that maternal Hro-nos is required for embryonic development. However, contrary to previous suggestions, maternal inherited Hro-nos does not appear necessary for ectoderm specification. (c) 2006 Elsevier Inc. All rights reserved.