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GENOME ANALYSIS

Divergence of the Dof Gene Families in Poplar, Arabidopsis, and Rice Suggests Multiple Modes of Gene Evolution after Duplication^1,[W]

Department of Plant Sciences, University of Tennessee, Knoxville, Tennessee 37996 (X.Y., G.A.T., Z.-M.C.); and Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831 (X.Y., G.A.T.)

It is widely accepted that gene duplication is a primary source of genetic novelty. However, the evolutionary fate of duplicated genes remains largely unresolved. The classical Ohno's Duplication-Retention-Non/Neofunctionalization theory, and the recently proposed alternatives such as subfunctionalization or duplication-degeneration-complementation, and subneofunctionalization, each can explain one or more aspects of gene fate after duplication. Duplicated genes are also affected by epigenetic changes. We constructed a phylogenetic tree using Dof (DNA binding with one finger) protein sequences from poplar (Populus trichocarpa) Torr. & Gray ex Brayshaw, Arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). From the phylogenetic tree, we identified 27 pairs of paralogous Dof genes in the terminal nodes. Analysis of protein motif structure of the Dof paralogs and their ancestors revealed six different gene fates after gene duplication. Differential protein methylation was revealed between a pair of duplicated poplar Dof genes, which have identical motif structure and similar expression pattern, indicating that epigenetics is involved in evolution. Analysis of reverse transcription-PCR, massively parallel signature sequencing, and microarray data revealed that the paralogs differ in expression pattern. Furthermore, analysis of nonsynonymous and synonymous substitution rates indicated that divergence of the duplicated genes was driven by positive selection. About one-half of the motifs in Dof proteins were shared by non-Dof proteins in the three plants species, indicating that motif co-option may be one of the forces driving gene diversification. We provided evidence that the Ohno's Duplication-Retention-Non/Neofunctionalization, subfunctionalization/duplication-degeneration-complementation, and subneofunctionalization hypotheses are complementary with, not alternative to, each other.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: (Max) Zong-Ming Cheng (zcheng{at}utk.edu).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.106.083642

^* Corresponding author; e-mail zcheng{at}utk.edu; fax 865–974–5365.

Received May 15, 2006; accepted August 26, 2006; published September 15, 2006.

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