MBE Advance Access originally published online on October 6, 2008
Molecular Biology and Evolution 2008 25(12):2717-2733; doi:10.1093/molbev/msn215
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Articles |
Origins and Evolution of the Formin Multigene Family That Is Involved in the Formation of Actin Filaments
,1,2
* Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park
Department of Biology, Pennsylvania State University, University Park
Institute for Bioinformatics, Faculty of Medicine, University of Muenster, Muenster, Germany
E-mail: duc136{at}psu.edu.
Accepted for publication September 24, 2008.
In eukaryotes, the assembly and elongation of unbranched actin filaments is controlled by formins, which are long, multidomain proteins. These proteins are important for dynamic cellular processes such as determination of cell shape, cell division, and cellular interaction. Yet, no comprehensive study has been done about the origins and evolution of this gene family. We therefore performed extensive phylogenetic and motif analyses of the formin genes by examining 597 prokaryotic and 53 eukaryotic genomes. Additionally, we used three-dimensional protein structure data in an effort to uncover distantly related sequences. Our results suggest that the formin homology 2 (FH2) domain, which promotes the formation of actin filaments, is a eukaryotic innovation and apparently originated only once in eukaryotic evolution. Despite the high degree of FH2 domain sequence divergence, the FH2 domains of most eukaryotic formins are predicted to assume the same fold and thus have similar functions. The formin genes have experienced multiple taxon-specific duplications and followed the birth-and-death model of evolution. Additionally, the formin genes experienced taxon-specific genomic rearrangements that led to the acquisition of unrelated protein domains. The evolutionary diversification of formin genes apparently increased the number of formin's interacting molecules and consequently contributed to the development of a complex and precise actin assembly mechanism. The diversity of formin types is probably related to the range of actin-based cellular processes that different cells or organisms require. Our results indicate the importance of gene duplication and domain acquisition in the evolution of the eukaryotic cell and offer insights into how a complex system, such as the cytoskeleton, evolved.
Key Words: formin family • FH2 • domain acquisition • birth-and-death evolution • eukaryotes
1 Present address: Center for Molecular and Mitochondrial Medicine and Genetics, Department of Biological Chemistry, University of California, Irvine.
2 Present address: Department of Biological Science, College of Natural Sciences and Mathematics, California State University, Fullerton.