Early mesodermal development in the patellogastropod Lottia goshimai

Mesodermal development is essential to explore the interlineage variations in the development of spiralians. Compared with model mollusks such as Tritia and Crepidula, knowledge about the mesodermal development of other molluscan lineages is limited. Here, we investigated early mesodermal development in the patellogastropod Lottia goshimai, which shows equal cleavage and has a trochophore larva. The endomesoderm derived from the 4d blastomere, that is, the mesodermal bandlets, was situated dorsally and showed a characteristic morphology. Investigations of the potential mesodermal patterning genes revealed that twist1 and snail1 were expressed in a proportion of these endomesodermal tissues, while all of the five genes we investigated (twist1, twist2, snail1, snail2, and mox) were expressed in ventrally located ectomesodermal tissues. Relatively dynamic snail2 expression suggests additional roles in various internalization processes. By tracing snail2 expression in early gastrulae, the 3a211 and 3b211 blastomeres were suggested to be the precursors of the ectomesoderm, which elongated to become internalized before division. These results help to understand the variations in the mesodermal development of different spiralians and explore the different mechanisms by which ectomesodermal cells are internalized, which has important evolutionary implications.

[1]  Yan Liang,et al.  ERK1/2 is an ancestral organising signal in spiral cleavage , 2022, Nature Communications.

[2]  Baozhong Liu,et al.  Molluskan Dorsal–Ventral Patterning Relying on BMP2/4 and Chordin Provides Insights into Spiralian Development and Evolution , 2021, Molecular biology and evolution.

[3]  J. D. Lambert,et al.  A serpin is required for ectomesoderm, a hallmark of spiralian development. , 2020, Developmental biology.

[4]  Ferdinand Marlétaz,et al.  Unravelling spiral cleavage , 2020, Development.

[5]  Baozhong Liu,et al.  Dorsoventral decoupling of Hox gene expression underpins the diversification of molluscs , 2019, Proceedings of the National Academy of Sciences.

[6]  M. Martindale,et al.  Molecular patterning during the development of Phoronopsis harmeri reveals similarities to rhynchonelliform brachiopods , 2019, EvoDevo.

[7]  M. Telford,et al.  Reinvestigating the early embryogenesis in the flatworm Maritigrella crozieri highlights the unique spiral cleavage program found in polyclad flatworms , 2019, EvoDevo.

[8]  M. Shankland,et al.  Ectomesoderm and epithelial–mesenchymal transition‐related genes in spiralian development , 2018, Developmental dynamics : an official publication of the American Association of Anatomists.

[9]  C. Nielsen Origin of the trochophora larva , 2018, Royal Society Open Science.

[10]  M. Vervoort,et al.  Cell lineage and cell cycling analyses of the 4d micromere using live imaging in the marine annelid Platynereis dumerilii , 2017, eLife.

[11]  Baozhong Liu,et al.  Expression patterns indicate that BMP2/4 and Chordin, not BMP5-8 and Gremlin, mediate dorsal–ventral patterning in the mollusk Crassostrea gigas , 2016, Development, Genes and Evolution.

[12]  M. Martindale,et al.  The developmental basis for the recurrent evolution of deuterostomy and protostomy , 2016, Nature Ecology &Evolution.

[13]  H. Wada,et al.  Evolution of the molluscan body plan: the case of the anterior adductor muscle of bivalves , 2016 .

[14]  J. D. Lambert,et al.  Mollusc models I. The snail Ilyanassa. , 2016, Current opinion in genetics & development.

[15]  J. J. Henry,et al.  Molluscan models: Crepidula fornicata. , 2016, Current opinion in genetics & development.

[16]  R. P. Kostyuchenko,et al.  Mesoderm patterning and morphogenesis in the polychaete Alitta virens (Spiralia, Annelida): Expression of mesodermal markers Twist, Mox, Evx and functional role for MAP kinase signaling , 2016, Mechanisms of Development.

[17]  K. Kocot On 20 years of Lophotrochozoa , 2016, Organisms Diversity & Evolution.

[18]  Antje H L Fischer,et al.  Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc Crepidula , 2015, Developmental dynamics : an official publication of the American Association of Anatomists.

[19]  J. Henry,et al.  Spiralian gastrulation: germ layer formation, morphogenesis, and fate of the blastopore in the slipper snail Crepidula fornicata , 2015, EvoDevo.

[20]  M. Martindale,et al.  Mesodermal gene expression during the embryonic and larval development of the articulate brachiopod Terebratalia transversa , 2015, EvoDevo.

[21]  E. Seaver Variation in spiralian development: insights from polychaetes. , 2014, The International journal of developmental biology.

[22]  Xin Yi Chan,et al.  Development of blastomere clones in the Ilyanassa embryo: transformation of the spiralian blastula into the larval body plan , 2014, Development Genes and Evolution.

[23]  G. Wolfstetter,et al.  Maternal Inheritance of Twist and Analysis of MAPK Activation in Embryos of the Polychaete Annelid Platynereis dumerilii , 2014, PloS one.

[24]  J. Henry Spiralian model systems. , 2014, The International journal of developmental biology.

[25]  J. Henry,et al.  Ins and outs of Spiralian gastrulation. , 2014, The International journal of developmental biology.

[26]  D. Arendt,et al.  Mesoteloblast-like mesodermal stem cells in the polychaete annelid Platynereis dumerilii (Nereididae). , 2013, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[27]  J. Henry,et al.  Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development , 2012, EvoDevo.

[28]  D. Weisblat,et al.  Lineage analysis of micromere 4d, a super-phylotypic cell for Lophotrochozoa, in the leech Helobdella and the sludgeworm Tubifex. , 2011, Developmental biology.

[29]  A. Hejnol A twist in time--the evolution of spiral cleavage in the light of animal phylogeny. , 2010, Integrative and comparative biology.

[30]  J. D. Lambert,et al.  Developmental Patterns in Spiralian Embryos , 2010, Current Biology.

[31]  C. Nielsen Some aspects of spiralian development , 2010 .

[32]  H. Wada,et al.  Early Development and Cleavage Pattern of the Japanese Purple Mussel, Septifer virgatus , 2009, Zoological science.

[33]  J. D. Lambert,et al.  Mesoderm in spiralians: the organizer and the 4d cell. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[34]  M. Martindale,et al.  High-resolution fate map of the snail Crepidula fornicata: the origins of ciliary bands, nervous system, and muscular elements. , 2007, Developmental biology.

[35]  Kariena Dill,et al.  Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I , 2007, Development Genes and Evolution.

[36]  E. Furlong,et al.  A core transcriptional network for early mesoderm development in Drosophila melanogaster. , 2007, Genes & development.

[37]  H. Barak,et al.  Cell fate specification along the anterior–posterior axis of the intermediate mesoderm , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[38]  M. Martindale,et al.  Conservation and innovation in spiralian development , 1999, Hydrobiologia.

[39]  A. Nederbragt,et al.  A lophotrochozoan twist gene is expressed in the ectomesoderm of the gastropod mollusk Patella vulgata , 2002, Evolution & development.

[40]  A. Nederbragt,et al.  Characterisation of two snail genes in the gastropod mollusc Patella vulgata. Implications for understanding the ancestral function of the snail-related genes in Bilateria , 2002, Development Genes and Evolution.

[41]  M. Baylies,et al.  A Twist in fate: evolutionary comparison of Twist structure and function. , 2002, Gene.

[42]  V. Hinman,et al.  Mox homeobox expression in muscle lineage of the gastropod Haliotis asinina: evidence for a conserved role in bilaterian myogenesis , 2002, Development Genes and Evolution.

[43]  M. Nieto,et al.  The snail superfamily of zinc-finger transcription factors , 2002, Nature Reviews Molecular Cell Biology.

[44]  W. Dictus,et al.  Cell-lineage and clonal-contribution map of the trochophore larva of Patella vulgata (Mollusca) 1 Both authors contributed equally to this work. 1 , 1997, Mechanisms of Development.

[45]  J. van den Biggelaar Cleavage pattern in embryos of Haliotis tuberculata (Archaeogastropoda) and gastropod phylogeny , 1993, Journal of morphology.

[46]  J. Nadeau,et al.  Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. , 1992, Development.

[47]  J. A. van den Biggelaar,et al.  Development of dorsoventral polarity and mesentoblast determination in Patella vulgata , 1977, Journal of morphology.

[48]  F. G. Smith The Development of Patella vulgata , 1935 .