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Published on August 20, 2008; 10.1104/pp.108.122457

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Received May 8, 2008
Accepted August 16, 2008

Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli

Kousuke Hanada , Cheng Zou , Melissa D. Lehti-Shiu , Kazuo Shinozaki , and Shin-Han Shiu *

Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA; Gene Discovery Research Group, RIKEN Plant Science Center, Yokohama, Kanagawa, 230-0045, Japan

* Corresponding author; email: shius{at}msu.edu.

Plants have substantially higher gene duplication rates compared to most other eukaryotes. These plant gene duplicates are mostly derived from whole genome and/or tandem duplications. Earlier studies have shown that a large number of duplicate genes are retained over a long evolutionary time and there is a clear functional bias in retention. However, the influence of duplication mechanism, particularly tandem duplication, on duplicate retention has not been thoroughly investigated. We have defined orthologous groups (OGs) between Arabidopsis thaliana and three other land plants to examine the functional bias of retained duplicate genes during vascular plant evolution. Based on analysis of Gene Ontology categories, it is clear that genes in orthologous groups that expanded via tandem duplication tend to be involved in responses to environmental stimuli while those that expanded via non-tandem mechanisms tend to have intracellular regulatory roles. Using Arabidopsis stress expression data, we further demonstrate that tandem duplicates in expanded OGs are significantly enriched in genes that are up-regulated by biotic stress conditions. In addition, tandem duplication of genes in an OG tends to be highly asymmetric. That is, expansion of OGs with tandem genes in one organismal lineage tends to be coupled with losses in the other. This is consistent with the notion that these tandem genes have experienced lineage-specific selection. In contrast, OGs with genes duplicated via non-tandem mechanisms tend to experience convergent expansion where similar numbers of genes are gained in parallel. Our study demonstrates that the expansion of gene families and retention of duplicates in plants exhibits substantial functional biases that are strongly influenced by the mechanism of duplication. In particular, genes involved in stress response have an elevated probability of retention in a single-lineage fashion following tandem duplication, suggesting that these tandem duplicates are likely important for adaptive evolution to rapidly changing environments.




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