Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms

Abstract

Background: Both single gene and whole genome duplications (WGD) have recurred in angiosperm evolution. However, the evolutionary effects of different modes of gene duplication, especially regarding their contributions to genetic novelty or redundancy, have been inadequately explored.

Results: In Arabidopsis thaliana and Oryza sativa (rice), species that deeply sample botanical diversity and for which expression data are available from a wide range of tissues and physiological conditions, we have compared expression divergence between genes duplicated by six different mechanisms (WGD, tandem, proximal, DNA based transposed, retrotransposed and dispersed), and between positional orthologs. Both neo-functionalization and genetic redundancy appear to contribute to retention of duplicate genes. Genes resulting from WGD and tandem duplications diverge slowest in both coding sequences and gene expression, and contribute most to genetic redundancy, while other duplication modes contribute more to evolutionary novelty. WGD duplicates may more frequently be retained due to dosage amplification, while inferred transposon mediated gene duplications tend to reduce gene expression levels. The extent of expression divergence between duplicates is discernibly related to duplication modes, different WGD events, amino acid divergence, and putatively neutral divergence (time), but the contribution of each factor is heterogeneous among duplication modes. Gene loss may retard inter-species expression divergence. Members of different gene families may have non-random patterns of origin that are similar in Arabidopsis and rice, suggesting the action of pan-taxon principles of molecular evolution.

Conclusion: Gene duplication modes differ in contribution to genetic novelty and redundancy, but show some parallels in taxa separated by hundreds of millions of years of evolution.

Figure 1. Flowchart of the procedure for classifying gene pairs based on mode of duplication.

Figure 2. Comparison of expression divergence among different modes of gene duplication.

(A) Comparison of distributions of expression divergence in Arabidopsis. (B) Comparison of levels of expression divergence in Arabidopsis. (C) Comparison of distributions of expression divergence in rice. (D) Comparison of levels of expression divergence in rice. Green lines in (B, D) indicate average expression divergence across duplication modes.

Figure 3. Comparison of expression levels between genes created by different duplication modes.

(A) Comparison of expression levels between Arabidopsis genes created by different duplication modes. (B) Comparison of expression levels between rice genes created by different duplication modes. Green lines indicate average expression levels.

Figure 4. Comparison of distributions of expression divergence among different WGD events.

(A) Comparison of distributions of expression divergence among different Arabidopsis WGD events. (B) Comparison of distributions of expression divergence among different rice WGD events. α, β and ρ were relatively recent WGD events, while γ and σ were more ancient WGD events.

Figure 5. Fitted smooth spline curves between expression divergence and Ks for different WGD events.

(A) Fitted smooth spline curves between expression divergence and Ks for different Arabidopsis WGD events. (B) Fitted smooth spline curves between expression divergence and Ks for different rice WGD events. α, β and ρ were relatively recent WGD events, while γ and σ were more ancient WGD events.

Figure 6. Comparison of expression divergence between different types of Arabidopsis-rice orthologs: singleton-singleton (S-S), singleton-duplicate (S-D) and duplicate-duplicate (D-D).

Figure 7. Comparison of Ks and Ka distributions for gene pairs duplicated by different modes.

(A) Comparison of Ks distributions in Arabidopsis. (B) Comparison of Ks distributions in rice. (C) Comparison of Ka distributions in Arabidopsis. (D) Comparison of Ka distributions in rice.

Figure 8. Fitted smooth spline curves between expression divergence and Ks or Ka for different modes of gene duplication.

(A) Fitted smooth spline curves between expression divergence and Ks in Arabidopsis. (B) Fitted smooth spline curves between expression divergence and Ks in rice. (C) Fitted smooth spline curves between expression divergence and Ka in Arabidopsis. (D) Fitted smooth spline curves between expression divergence and Ka in rice.

Figure 9. Gene duplication modes among the members of selected gene families.

(A) Arabidopsis disease resistance gene homologs. (B) Arabidopsis Cytochrome P450 gene family. (C) Rice Cytochrome P450 gene family. (D) Arabidopsis cytoplasmic ribosomal gene family. (E) Arabidopsis C2H2 zinc finger gene family. (F) Rice C2H2 zinc finger gene family. Different gene duplication modes are indicated by different colors.