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Common Evolutionary Origin and Birth-and-Death Process in the Replication-Independent Histone H1 Isoforms from Vertebrate and Invertebrate Genomes

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Abstract

The H1 histone multigene family shows the greatest diversity of isoforms among the five histone gene families, including replication-dependent (RD) and replication-independent (RI) genes, according to their expression patterns along the cell cycle and their genomic organization. Although the molecular characterization of the RI isoforms has been well documented in vertebrates, similar information is lacking in invertebrates. In this work we provide evidence for a polyadenylation signature in the Mytilus “orphon” H1 genes similar to the polyadenylation characteristic of RI H1 genes. These mussel genes, together with the sea urchin H1δ genes, are part of a lineage of invertebrate “orphon” H1 genes that share several control elements with vertebrate RI H1 genes. These control elements include the UCE element, H1-box and H4-box. We provide evidence for a functional evolution of vertebrate and invertebrate RI H1 genes, which exhibit a clustering pattern by type instead of by species, with a marked difference from the somatic variants. In addition, these genes display an extensive silent divergence at the nucleotide level which is always significantly larger than the nonsilent. It thus appears that RI and RD H1 isoforms display similar long-term evolutionary patterns, best described by the birth-and-death model of evolution. Notably, this observation is in contrast with the theoretical belief that clustered RD H1 genes evolve in a concerted manner. The split of the RI group from the main RD group must therefore have occurred before the divergence between vertebrates and invertebrates about 815 million years ago. This was the result of the transposition of H1 genes to solitary locations in the genome.

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Acknowledgments

We thank Dr. Alejandro Rooney and Dr. Helen Piontkivska for fruitful discussions and comments on an early version of this work. We are also very grateful to Patricia González Greciano, Sergio Casas-Tintó, and Clara Goday at the Departamento de Biología Celular y del Desarrollo, CIB-CSIC, Spain, as well as to Lindsay J. Frehlick at the Department of Biochemistry and Microbiology, University of Victoria, for skillful technical assistance in the lab and for their critical comments. This work was funded by a PGIDT Grant (10PX110304) to J.M., by a Canadian Institutes of Health Research Grant-CIHR (MOP-57718) to J.A., and by a predoctoral FPU fellowship from the Spanish Government awarded to J.M.E.-L. We thank two anonymous reviewers for helpful discussions and comments.

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Authors and Affiliations

  1. Departamento de Biología Celular y Molecular, Universidade da Coruña, Campus de A Zapateira s/n, E-15071, A Coruña, Spain

    José M. Eirín-López, Ana M. González-Tizón, Andrés Martínez & Josefina Méndez

  2. Departamento de Biología Celular y del Desarrollo, Centro de Investigaciones Biológicas—CSIC, E-28040, Madrid, Spain

    M. Fernanda Ruiz & Lucas Sánchez

  3. Department of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, V8W 3P6, Canada

    Juan Ausió

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  1. José M. Eirín-López
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Correspondence to José M. Eirín-López.

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Eirín-López, J.M., Ruiz, M.F., González-Tizón, A.M. et al. Common Evolutionary Origin and Birth-and-Death Process in the Replication-Independent Histone H1 Isoforms from Vertebrate and Invertebrate Genomes. J Mol Evol 61, 398–407 (2005). https://doi.org/10.1007/s00239-004-0328-9

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