Expression Pattern Shifts Following Duplication Indicative of Subfunctionalization and Neofunctionalization in Regulatory Genes of Arabidopsis

Authors: Duarte, Jill M.; Cui, Liying; Wall, P. Kerr; Zhang, Qing; Zhang, Xiaohong; Leebens-Mack, Jim; Ma, Hong; Altman, Naomi; dePamphilis, Claude W.

Source: Molecular Biology and Evolution, Volume 23, Number 2, 20 February 2006 , pp. 469-478(10)

Publisher: Oxford University Press

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Abstract:

Gene duplication plays an important role in the evolution of diversity and novel function and is especially prevalent in the nuclear genomes of flowering plants. Duplicate genes may be maintained through subfunctionalization and neofunctionalization at the level of expression or coding sequence. In order to test the hypothesis that duplicated regulatory genes will be differentially expressed in a specific manner indicative of regulatory subfunctionalization and/or neofunctionalization, we examined expression pattern shifts in duplicated regulatory genes in Arabidopsis. A two-way analysis of variance was performed on expression data for 280 phylogenetically identified paralogous pairs. Expression data were extracted from global expression profiles for wild-type root, stem, leaf, developing inflorescence, nearly mature flower buds, and seedpod. Gene, organ, and gene by organ interaction (G × O) effects were examined. Results indicate that 85% of the paralogous pairs exhibited a significant G × O effect indicative of regulatory subfunctionalization and/or neofunctionalization. A significant G × O effect was associated with complementary expression patterns in 45% of pairwise comparisons. No association was detected between a G × O effect and a relaxed evolutionary constraint as detected by the ratio of nonsynonymous to synonymous substitutions. Ancestral gene expression patterns inferred across a Type II MADS-box gene phylogeny suggest several cases of regulatory neofunctionalization and organ-specific nonfunctionalization. Complete linkage clustering of gene expression levels across organs suggests that regulatory modules for each organ are independent or ancestral genes had limited expression. We propose a new classification, regulatory hypofunctionalization, for an overall decrease in expression level in one member of a paralogous pair while still having a significant G × O effect. We conclude that expression divergence specifically indicative of subfunctionalization and/or neofunctionalization contributes to the maintenance of most if not all duplicated regulatory genes in Arabidopsis and hypothesize that this results in increasing expression diversity or specificity of regulatory genes after each round of duplication.

Keywords: expression; gene duplication; ANOVA; microarray; regulatory genes

Document Type: Research article

DOI: http://dx.doi.org/10.1093/molbev/msj051

Publication date: 2006-02-20

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Molecular Biology and Evolution publishes research at the interface between molecular and evolutionary biology. The journal publishes investigations of molecular evolutionary patterns and processes, tests of evolutionary hypotheses that use molecular data, and studies that use molecular evolutionary information to address questions about biological function at all levels of organization.

Expression Pattern Shifts Following Duplication Indicative of Subfunctionalization and Neofunctionalization in Regulatory Genes of Arabidopsis

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