Trends in Genetics
Update
Genome AnalysisExternal factors accelerate expression divergence between duplicate genes
Genome Analysis
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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2012, Current Opinion in Plant BiologyCitation Excerpt :Especially altered dosage of regulatory genes can result in expression changes of their target genes as these regulators are entangled in circuits where the activity of each component depends on their relative dosage with other genes in the same circuit. Indeed, Ha et al. [31••] suggested that genes involved in endogeneous responses are often entangled in more complex networks compared to the simple cascading network to which, for instance, stress-related genes belong, explaining their difference in expression divergence. Likewise, changes in gene dosage of individual components of a protein complex can affect the efficiency of the whole complex.