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MBE Advance Access published online on May 23, 2008

Molecular Biology and Evolution, doi:10.1093/molbev/msn121
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

The sperm proteins from amphioxus mirror its basal position among chordates and redefine the origin of vertebrate protamines

José María Eirín-López1,2, Lindsay J. Frehlick1, Manel Chiva3, Núria Saperas4 and Juan Ausió1,§

1 Department of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada V8W 3P6
2 Departamento de Biología Celular y Molecular, Universidade da Coruña, Campus de A Zapateira s/n, A Coruña, Spain E-15071
3 Departament de Ciències Fisiològiques II, Facultat de Medicina, Campus de Bellvitge, Universitat de Barcelona, L'Hospitalet de Llobregat, Barcelona E-08907, Spain
4 Departament d'Enginyeria Química, ETSEIB, Universitat Politècnica de Catalunya, Diagonal, 647, Barcelona E-08028, Spain

§ To whom editorial correspondence should be addressed at: University of Victoria, Department of Biochemistry and Microbiology, Petch Building, Room 220, Victoria, BC, Canada V8W 3P6. Phone: 250-721 8863, fax: 250-721 8855, email: jausio{at}uvic.ca

Received for publication March 14, 2008. Revision received May 9, 2008. Accepted for publication May 20, 2008.

The sperm nuclear basic proteins (SNBPs) that participate in chromatin condensation in spermatozoa belong to three groups: histone (H), protamine-like (PL) and protamine type. They share a common origin with histone H1 resulting from the segregation of PL components, corresponding to different regions of an H1 precursor molecule (N-terminal, winged-helix domain, C-terminal), becoming independent and following a subsequent process of parallel vertical evolution (H {leftrightarrow} PL {leftrightarrow} P). In the present work we describe the sequence and primary structure of the main SNBP component in the sperm of the cephalochordate Branchiostoma floridae (amphioxus), revealing that it represents the deuterostome counterpart of the PL-III SNBP component from molluscs corresponding to the H1 N-terminal region. Until now, this has been a missing piece needed to complete the evolutionary history of SNBPs in metazoan genomes. The discovery of this PL lineage in deuterostomes definitively validates the parallel vertical evolution of SNBPs across metazoans, giving further support to the ‘basal’ position of amphioxus among chordates, with respect to tunicates. Sequence analyses suggest that later on in evolution the appearance of positively selected arginine-rich protamines, derived from the H1 C-terminal region, led to the extinction of this PL lineage in the genomes of early protostomes and deuterostomes. Given that tunicates are now viewed as a sister group of vertebrates, the lysine to arginine transition responsible for the origin of vertebrate protamines must be set a step back from tunicates.

Key Words: Reproductive proteins • protamines • metazoans • long-term evolution • chromatin


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