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Early mesodermal expression of Hox genes in the polychaete Alitta virens (Annelida, Lophotrochozoa)

Abstract

Hox genes are the key regulators of axial regionalization of bilaterian animals. However, their main function is fulfilled differently in the development of animals from different evolutionary branches. Early patterning of the developing embryos by Hox gene expression in the representatives of protostomes (arthropods, mollusks) starts in the ectodermal cells. On the contrary, the instructive role of the mesoderm in the axial patterning was demonstrated for vertebrates. This makes it difficult to understand if during the axial regionalization of ancestral bilaterians Hox genes first expressed in the developing mesoderm or the ectoderm. To resolve this question, it is necessary to expand the number of models for investigation of the early axial patterning. Here, we show that three Hox genes of the polychaete Alitta virens (formerly Nereis virens, Annelida, Lophotrochozoa)—Hox2, Hox4, and Lox5—are expressed in the mesodermal anlagen of the three future larval chaetigerous segments in spatially colinear manner before the initiation of Hox expression in the larval ectoderm. This is the first evidence of sequential Hox gene expression in the mesoderm of protostomes to date.

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Acknowledgments

The authors thank Olga B. Lavrova for maintaining the A. virens culture in the laboratory of experimental embryology and Alexander Y. Nesterenko for participating in the material collection. We are also grateful to the staff of the White Sea Biological Station “Kartesh” (Zoological Institute, Russian Academy of Science) for providing an opportunity to collect A. virens. We thank the “Chromas” center for the opportunity to use the workstation Leica DMRXA. The research was supported by RFBR grants 14-04-31683-mol-a and 14-04-01531-a and the grant from St. Petersburg State University № 1.38.209.2014.

Authors’ contributions

Milana A. Kulakova performed WMISH and analyzed the results. Elena L. Novikova drafted the manuscript. All the authors participated in the maintenance of the larval culture and material preparation. All the authors have analyzed and discussed the results, read, and approved the final manuscript.

Author information

Correspondence to Elena L. Novikova.

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Competing interests

The authors declare that they have no competing interests.

Additional information

Communicated by David A. Weisblat

Electronic supplementary material

Figure S1
figure5

The initiation of mesodermal Nvi-Hox2 expression in the embryo (38 hpf) in large endomesodermal cells, the descendants of 4d-macromere. Deep ventral view, apical pole to the top. Scalebar - 50 μm. (GIF 28 kb)

Figure S2
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Expression of Nvi-Hox2, Nvi-Hox4 and Nvi-Lox5 gradually disappear in the mesodermal bands on the stage of mid-trochophore. Hox2, Lox5 - deep ventral views, apical to the top, Hox4 – view from the vegetal pole, ventral to the top. Scalebar - 50 μm. (JPEG 1877 kb)

Figure S3
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The initiation of ectodermal Nvi-Hox4 expression (arrowhead) in the 2d-descendants, which come in contact with Hox4-positive mesoderm. Protrochophore (54 hpf), deep lateral view, dorsal on the left. Scalebar - 50 μm. (GIF 560 kb)

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Kulakova, M.A., Bakalenko, N.I. & Novikova, E.L. Early mesodermal expression of Hox genes in the polychaete Alitta virens (Annelida, Lophotrochozoa). Dev Genes Evol 227, 69–74 (2017). https://doi.org/10.1007/s00427-016-0563-2

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Keywords

  • Hox genes
  • Mesoderm
  • Larva
  • Polychaetes
  • Embryogenesis
  • Colinearity