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Penaeid shrimp brachyury: sequence analysis and expression during gastrulation

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Abstract

Gastrulation occurs by a variety of morphogenetic movements, often correlated with diverse expression of the T-box transcription factor Brachyury (Bra). Bra may be expressed in ectoderm, mesoderm, or endoderm, but its role in cell fate specification or regulation of gastrulation movements has not been studied in the development of crustaceans. Penaeid shrimp (Decapoda: Dendrobranchiata: Penaeidae) develop by complete cleavage and gastrulation by invagination to a free-swimming nauplius larva. Penaeid gastrulation diverges from other decapods and from insects, occurring early at a low cell number with the formation of a radial invagination. Toward a better understanding of gastrulation movements in penaeid shrimp, bra was identified from newly available penaeid shrimp genomes and transcriptomes of Litopenaeus vannamei, Marsupenaeus japonicus, and Penaeus monodon. Additional bra homologs were obtained from the outgroups Sicyonia ingentis (Decapoda: Dendrobranchiata: Sicyoniidae) and the caridean shrimp Caridina multidentata (Decapoda: Pleocymata). The genes encoded penaeid shrimp Bra proteins of 551–552 amino acids, containing the highly conserved T-box DNA-binding region. The N-terminal Smad1-binding domain, conserved in most animals, was absent in shrimp Bra. The R1 repressor domain was the best conserved of the C-terminal regulatory domains, which were widely divergent compared to other species. The penaeid shrimp bra gene consisted of six exons, with splice sites conserved with other phyla across the animal kingdom. Real-time qPCR and FPKM analysis showed that shrimp bra mRNA was strongly expressed during gastrulation. These findings begin to address the evolution of gastrulation in shrimp at the molecular level.

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Acknowledgments

The authors thank the students of the 2015 Developmental Biology class through the Biology Department at Central Michigan University (including A.P.D.) for the cloning and sequencing of M. japonicus PCR products. The authors are grateful to Dr. Eric Linton, Central Michigan University, for assistance with phylogenetic analysis and to two anonymous reviewers for their suggestions for improving the manuscript.

Funding

This work was supported by the CSIRO Food Futures Flagship Cluster on “Sex ratio and sterility for commercial animal production” with funding from the CSIRO Flagship Collaboration Fund and FRCE grants from Central Michigan University to P.L.H. and the National High-Tech Research and Development Program of China (863 Program, 2012AA10A404) to J.X.

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Correspondence to Philip L. Hertzler.

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Communicated by Nico Posnien

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Hertzler, P.L., Wei, J., Droste, A.P. et al. Penaeid shrimp brachyury: sequence analysis and expression during gastrulation. Dev Genes Evol 228, 219–225 (2018). https://doi.org/10.1007/s00427-018-0618-7

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  • DOI: https://doi.org/10.1007/s00427-018-0618-7

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