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The HMGA gene family in chordates: evolutionary perspectives from amphioxus

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Abstract

High mobility group A proteins of vertebrates, HMGA1 and 2, are chromatin architectural factors involved in development, cell differentiation, and neoplastic transformation. Here, we characterize an amphioxus HMGA gene ortholog and analyze its expression. As a basal chordate, amphioxus is well placed to provide insights into the evolution of the HMGA gene family, particularly in the transition from invertebrates to vertebrates. Our phylogenetic analysis supports the basal position of amphioxus, echinoderm, and hemichordate HMGA sequences to those of vertebrate HMGA1 and HMGA2. Consistent with this, the genomic landscape around amphioxus HMGA shares features with both. Whole mount in situ hybridization shows that amphioxus HMGA mRNA is detectable from neurula stage onwards in both nervous and non-nervous tissues. This correlates with protein expression monitored immunocytochemically using antibodies against human HMGA2 protein, revealing especially high levels of expression in cells of the lamellar body, the amphioxus homolog of the pineal, suggesting that the gene may have, among its many functions, an evolutionarily conserved role in photoreceptor differentiation.

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Acknowledgements

We thank Skip Pierce and John M. Lawrence (Biology Department, USF, Tampa, FL) for providing lab space and equipment, Ray Martinez and Marilyn Wetzel (Department of Biology, USF, Tampa, FL) for logistic support, Linda Holland (Scripps Institute, La Jolla, CA) and Héctor Escriva and colleagues (CNRS, Unité Mixte de Recherche 7232, Université Pierre et Marie Curie Paris 06 and the Observatoire Océanologique, Banyuls-sur-Mèr) for their help obtaining B. floridae and B. lanceolatum adults and embryos, and for providing lab space and technical assistance. We also thank Lorenzo Zambini for sharing unpublished data, Heather Down for assistance preparing Fig. 6a, and two reviewers for their detailed critique of the manuscript. This work was supported by a University of Genoa National Grant and ASSEMBLE grant no.227799 to SC and MP, MIUR grant 2009XW7XSX to RV and GM, and funding from the Lionel G. Harrison Research Trust to TL.

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Author notes

  1. Simone Macrì

    Present address: Institute of Biotechnology, University of Helsinki, Biocenter 3, Viikinkaari 1, PO box 65, FI-00014, Helsinki, Finland

Authors and Affiliations

  1. Dipartimento di Scienze della Terra, dell’Ambiente e della Vita (DISTAV), Università di Genova, viale Benedetto XV 5, 16132, Genoa, Italy

    Matteo Bozzo, Paola Ramoino, Mario Pestarino & Simona Candiani

  2. Dipartimento di Biologia, Unità di Biologia Cellulare e dello Sviluppo, SS12 Abetone e Brennero 4, 56127, Pisa, Italy

    Simone Macrì & Robert Vignali

  3. Laboratorio di Biochimica, Dipartimento di Farmacia (DIFAR), Università di Genova, viale Benedetto XV 3, 16132, Genoa, Italy

    Daniela Calzia

  4. Dipartimento di Scienze della Vita, Università degli Studi di Trieste, via Giorgieri 5, 34127, Trieste, Italy

    Riccardo Sgarra & Guidalberto Manfioletti

  5. Biology Department, University of Victoria, BC V8W-3N5, Victoria, Canada

    Thurston Lacalli

Authors
  1. Matteo Bozzo
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  2. Simone Macrì
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Corresponding author

Correspondence to Simona Candiani.

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Additional information

Communicated by Karen E Sears

Electronic supplementary material

Supplementary file 1

List of the sequences used in the phylogenetic analysis. (DOCX 80 kb).

Supplementary file 2

HMGA expression in B. lanceolatum neurulae and larvae. A: Side view of a mid-neurula. B: Side view of a 24-h late neurula. C,D: Side views of a 36-h and 1-gill slit larvae. po, preoral pit; lmb, lamellar body. Scale bars: 50 μm. (GIF 228 kb).

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Bozzo, M., Macrì, S., Calzia, D. et al. The HMGA gene family in chordates: evolutionary perspectives from amphioxus. Dev Genes Evol 227, 201–211 (2017). https://doi.org/10.1007/s00427-017-0581-8

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  • DOI: https://doi.org/10.1007/s00427-017-0581-8

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