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MBE Advance Access published online on October 11, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl138
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© 2006 The Authors This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Accepted September 25, 2006

Research Article

Rate and Polarity of Gene Fusion and Fission in Oryza sativa and Arabidopsis thaliana

Yoji Nakamura 1 *, Takeshi Itoh 2, and William Martin 3

1 Division of Bioengineering and Bioinformatics, Graduate School of Information Science and Technology, Hokkaido University Kita 14, Nishi 9, Kita-ku, Sapporo, 060-0814, Japan; Institut für Botanik III, Heinrich-Heine Universität Düsseldorf Universitätstraße 1, 40225 Düsseldorf, Germany
2 Genome Research Department, National Institute of Agrobiological Sciences 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602, Japan
3 Institut für Botanik III, Heinrich-Heine Universität Düsseldorf Universitätstraße 1, 40225 Düsseldorf, Germany

* To whom correspondence should be addressed.
Yoji Nakamura, E-mail: yojnakam{at}ist.hokudai.ac.jp


  Abstract

Eukaryotic gene fusion and fission events are mechanistically more complicated than in prokaryotes and their quantitative contributions to genome evolution are still poorly understood. We have identified all differentially composite or split genes in two fully sequenced plant genomes, Oryza sativa and Arabidopsis thaliana. Out of 10,172 orthologous gene pairs, 60 (0.6% of the total) revealed a verified fusion or fission event in either lineage after the divergence of O. sativa and A. thaliana. Polarizing these events by outgroup comparison revealed differences in the rate of gene fission, but not of gene fusion, in the rice and Arabidopsis lineages. Gene fission occurred at a higher rate than gene fusion in the O. sativa lineage and was furthermore more common in rice than in Arabidopsis. Nucleotide insertion bias has promoted gene fission in the O. sativa lineage, consistent with its generally longer nucleotide sequences than A. thaliana in selectively neutral regions, and with the abundance of transposable elements in rice. The divergence time of monocots and dicots (140-200 million years) indicates that gene fusion/fission events occur at an average rate of 1-2 x 10-11 events per gene per year, ~100-fold slower than the average per site nuclear nucleotide substitution rate in these lineages. Gene fusion and fission are thus rare and slow processes in higher plant genomes; they should be of utility to address deeper evolutionary relationships among plants -- and the relationship of plants to other eukaryotic lineages -- where sequence-based phylogenies provide equivocal or conflicting results.

Keywords: gene fusion and fission; introns; transposable elements; plant phylogeny.
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