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Expansion of TALE homeobox genes and the evolution of spiralian development

Abstract

Spiralians, including molluscs, annelids and platyhelminths, share a unique development process that includes the typical geometry of early cleavage and early segregation of cell fate in blastomeres along the animal–vegetal axis. However, the molecular mechanisms underlying this early cell fate segregation are largely unknown. Here, we report spiralian-specific expansion of the three-amino-acid loop extension (TALE) class of homeobox genes. During early development, some of these TALE genes are expressed in staggered domains along the animal–vegetal axis in the limpet Nipponacmea fuscoviridis and the polychaete Spirobranchus kraussii. Inhibition or overexpression of these genes alters the developmental fate of blastomeres, as predicted by the gene expression patterns. These results suggest that the expansion of novel TALE genes plays a critical role in the establishment of a novel cell fate segregation mechanism in spiralians.

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Fig. 1: Molecular phylogenetic tree of the TALE genes from spiralians, ecdysozoans, deuterostomes and cnidarians.
Fig. 2: Spatiotemporal expression patterns of limpet N. fuscoviridis SPILE genes.
Fig. 3: Effects of inhibition or overexpression of SPILE genes on gene expression during early cleavage of limpet N . fuscoviridis.
Fig. 4: Phenotypes of trochophora larvae injected with MO or SPILE gene mRNA.

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Acknowledgements

This work was supported by the 'Tree of Life' research project of the University of Tsukuba.

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Authors

Contributions

Y.M. and H.W. contributed to the design of the experiments. Y.M. and N.H. collected the samples. Y.M. performed the experiments and analysed the data. Y.M. and H.W. wrote the manuscript.

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Correspondence to Yoshiaki Morino.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Figures 1–6, Supplementary Table 6.

Life Sciences Reporting Summary

Supplementary Table 1

Lists of TALE sequences in Spiralia.

Supplementary Table 2

Results of Blast searches using TALE sequences against genome assemblies of each of the three spiralian species, Lottia gigantea, Crassostrea gigas and Capitella teleta.

Supplementary Table 3

Results of Blast searches using the TALE sequences against protein database of each of three spiralian species, Pinctada fucata, Echinococcus multilocularis and Adineta vaga.

Supplementary Table 4

Lists of species and database for sequence collection and Blast analysis.

Supplementary Table 5

Results of Blast searches using the SPILE sequences against genome and protein database of non-spiralian.

Supplementary Data 1

TALE homeobox sequences alignment file for phylogenetic analysis of Supplementary Fig. 1.

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Morino, Y., Hashimoto, N. & Wada, H. Expansion of TALE homeobox genes and the evolution of spiralian development. Nat Ecol Evol 1, 1942–1949 (2017). https://doi.org/10.1038/s41559-017-0351-z

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