Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth

Authors

  • Hongzhi Kong,

    Corresponding author
    1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China,
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  • Lena L. Landherr,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, PA 16802, USA, and
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  • Michael W. Frohlich,

    1. Department of Botany, Natural History Museum, London, SW7 5BD, UK
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  • Jim Leebens-Mack,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, PA 16802, USA, and
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    • Present address: Department of Plant Biology, University of Georgia, Athens, GA 30602, USA

  • Hong Ma,

    1. Department of Biology, The Huck Institutes of the Life Sciences, and Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, PA 16802, USA, and
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  • Claude W. DePamphilis

    Corresponding author
    1. Department of Biology, The Huck Institutes of the Life Sciences, and Institute of Molecular Evolutionary Genetics, The Pennsylvania State University, University Park, PA 16802, USA, and
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(fax +86 10 6259 0843; email hzkong@ibcas.ac.cn or fax +1 814 863 1357; email cwd3@psu.edu).

Summary

Gene duplication plays important roles in organismal evolution, because duplicate genes provide raw materials for the evolution of mechanisms controlling physiological and/or morphological novelties. Gene duplication can occur via several mechanisms, including segmental duplication, tandem duplication and retroposition. Although segmental and tandem duplications have been found to be important for the expansion of a number of multigene families, the contribution of retroposition is not clear. Here we show that plant SKP1 genes have evolved by multiple duplication events from a single ancestral copy in the most recent common ancestor (MRCA) of eudicots and monocots, resulting in 19 ASK (Arabidopsis SKP1-like) and 28 OSK (Oryza SKP1-like) genes. The estimated birth rates are more than ten times the average rate of gene duplication, and are even higher than that of other rapidly duplicating plant genes, such as type I MADS box genes, R genes, and genes encoding receptor-like kinases. Further analyses suggest that a relatively large proportion of the duplication events may be explained by tandem duplication, but few, if any, are likely to be due to segmental duplication. In addition, by mapping the gain/loss of a specific intron on gene phylogenies, and by searching for the features that characterize retrogenes/retrosequences, we show that retroposition is an important mechanism for expansion of the plant SKP1 gene family. Specifically, we propose that two and three ancient retroposition events occurred in lineages leading to Arabidopsis and rice, respectively, followed by repeated tandem duplications and chromosome rearrangements. Our study represents a thorough investigation showing that retroposition can play an important role in the evolution of a plant gene family whose members do not encode mobile elements.

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