Trends in Genetics
Volume 23, Issue 4, April 2007, Pages 162-166
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Genome Analysis
External factors accelerate expression divergence between duplicate genes

https://doi.org/10.1016/j.tig.2007.02.005Get rights and content

We examined the evolution of expression of duplicate genes in Arabidopsis thaliana, by analyzing 512 data sets of gene expression microarrays and 2022 recent duplicate gene pairs. Expression divergence between gene duplicates is significantly greater in response to environmental stress than to developmental processes. A slow rate of expression divergence during development might offer dosage-dependent selective advantage, whereas rapid expression divergence in response to external changes might accelerate adaptation.

Introduction

The genomes of all eukaryotes have undergone at least one round of whole-genome duplication (WGD) (see Glossary) during their evolutionary history 1, 2. Duplicate genomes can undergo massive gene loss and genomic rearrangements, leading to a diploidized state, as shown in yeast [3], Arabidopsis4, 5, 6, 7 and rice [8]. During evolution one copy of the gene duplicate can be lost by the accumulation of deleterious mutations [9]. Evidently, many duplicate genes are retained because the redundancy conferred by duplicate genes might facilitate species adaptation [1] and genetic robustness against null mutations [10]. Both copies can be retained if a higher dosage is advantageous [11], or the function of the duplicate can diverge from that of the ancestral gene by subfunctionalization [12] (such as tissue specificity). Alternatively, one gene duplicate can evolve to possess a novel function by neofunctionalization 1, 13.

How duplicate genes diverge in expression is a longstanding issue 1, 14. Of particular interest is what factors affect the rate of expression divergence between duplicate genes? This question has not been well explored, although some factors such as developmental constraint have been investigated 10, 15, 16. Because environmental factors such as abiotic and biotic stresses tend to change faster than internal factors such as developmental programs, we hypothesize that environmental factors accelerate expression divergence between duplicate genes. Similarly, acceleration can also occur in the extracellular transport processes that are affected by environmental conditions. The duplicate genes in Arabidopsis thaliana that were derived from a WGD 20–40 million years ago 4, 5, 6 are ideal for testing our hypothesis because these duplicate genes are old enough to have accumulated a substantial degree of expression divergence but not too old to make statistical inferences difficult.

Section snippets

Preferential induction of duplicate genes by abiotic and biotic stresses

To investigate the expression evolution of duplicate genes in response to exogenous processes, including external factors, we first studied how often these duplicate genes are induced by environmental stresses using microarray data analysis (see Methods, Figure S1 and Table S1 in Online Supplementary Material). The proportion of duplicate genes upregulated under abiotic stress in roots or shoots is significantly greater than that of other genes in the genome (2022 pairs of duplicate genes were

Expression diversity in response to developmental changes

We then studied how duplicate genes respond to endogenous processes, including developmental programs. The differentially regulated genes were detected across 79 different tissues using one-way analysis of variance (ANOVA) (see Table S3 in Online Supplementary Material). We found that the frequency of genes displaying differential expression in various developmental stages was greater in gene duplicates than in other genes. Among five representative tissues (leaf, flower, root, seed and

Faster expression divergence in response to environmental factors than to developmental processes

To evaluate the relative contributions of environmental and developmental factors to expression divergence between duplicate genes, we analyzed the Pearson correlation coefficient of expression (Box 1) between gene duplicates in developmental (Rdev) or environmental (Renv) processes using the same number of expression data sets: 63 in different developmental stages and 63 treatment and time-course combinations in roots and shoots, respectively. The distributions of expression correlation

Biological implications

Duplicate genes display greater levels of expression diversity than do random gene pairs in response to external and internal processes. However, the duplicate genes involved in developmental processes tend to be coregulated, whereas the duplicate genes involved in abiotic and biotic stresses tend to diverge in expression (Figure 2). There is experimental support for the above conclusion. For example, SEP1 (formerly AGL2) and SEP2 (formerly AGL4) are gene duplicates expressed at the flower

Concluding remarks

We propose a model (Figure 2) for different evolutionary fates of duplicate genes in response to external and internal processes. Duplicate genes diverge in expression relatively rapidly in response to abiotic and biotic stresses, which might facilitate subfunctionalization [12], neofunctionalization 1, 13 and the evolution of an adaptive mechanism to cope with environmental changes [28]. In development, duplicate genes diverge in expression relatively slowly and tend to be coregulated. A

Acknowledgements

We thank Justin Borovitz and reviewers for critical comments on the manuscript, and members in the Chen and Li laboratories for valuable suggestions. We especially thank Detlef Weigel and AtGenExpress Consortium for sharing the expression array data. The work was supported by grants from the NIH (W-H.L. and Z.J.C.) and NSF (Z.J.C.).

Glossary

Endogenous process
a biological process, such as organ differentiation, that involves internal signals and developmental switches from vegetative to reproductive growth.
Exogenous process
a biological process that involves external stimuli such as abiotic and biotic stresses.
Neofunctionalization
gain of a novel function (or expression pattern) from a duplicate gene.
Polyploid
an individual or cell that has two or more basic sets of chromosomes.
Subfunctionalization
divergence of function (or

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