Dataset Information

Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication.

ABSTRACT: BACKGROUND: Various evolutionary models have been proposed to interpret the fate of paralogous duplicates, which provides substrates on which evolution selection could act. In particular, domestication, as a special selection, has played important role in crop cultivation with divergence of many genes controlling important agronomic traits. Recent studies have indicated that a pair of duplicate genes was often sub-functionalized from their ancestral functions held by the parental genes. We previously demonstrated that the rice cell-wall invertase (CWI) gene GIF1 that plays an important role in the grain-filling process was most likely subjected to domestication selection in the promoter region. Here, we report that GIF1 and another CWI gene OsCIN1 constitute a pair of duplicate genes with differentiated expression and function through independent selection. RESULTS: Through synteny analysis, we show that GIF1 and another cell-wall invertase gene OsCIN1 were paralogues derived from a segmental duplication originated during genome duplication of grasses. Results based on analyses of population genetics and gene phylogenetic tree of 25 cultivars and 25 wild rice sequences demonstrated that OsCIN1 was also artificially selected during rice domestication with a fixed mutation in the coding region, in contrast to GIF1 that was selected in the promoter region. GIF1 and OsCIN1 have evolved into different expression patterns and probable different kinetics parameters of enzymatic activity with the latter displaying less enzymatic activity. Overexpression of GIF1 and OsCIN1 also resulted in different phenotypes, suggesting that OsCIN1 might regulate other unrecognized biological process. CONCLUSION: How gene duplication and divergence contribute to genetic novelty and morphological adaptation has been an interesting issue to geneticists and biologists. Our discovery that the duplicated pair of GIF1 and OsCIN1 has experienced sub-functionalization implies that selection could act independently on each duplicate towards different functional specificity, which provides a vivid example for evolution of genetic novelties in a model crop. Our results also further support the established hypothesis that gene duplication with sub-functionalization could be one solution for genetic adaptive conflict.

SUBMITTER: Wang E

PROVIDER: S-EPMC2873416 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication.

Wang Ertao E Xu Xun X Zhang Lin L Zhang Hong H Lin Lin L Wang Qin Q Li Qun Q Ge Song S Lu Bao-Rong BR Wang Wen W He Zuhua Z

BMC evolutionary biology 20100423

<h4>Background</h4>Various evolutionary models have been proposed to interpret the fate of paralogous duplicates, which provides substrates on which evolution selection could act. In particular, domestication, as a special selection, has played important role in crop cultivation with divergence of many genes controlling important agronomic traits. Recent studies have indicated that a pair of duplicate genes was often sub-functionalized from their ancestral functions held by the parental genes. W ...[more]

PMID: 20416079

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Project description:BackgroundMicroRNAs (miRNAs) posttranscriptionally down-regulate gene expression by binding target mRNAs. Analysis of the evolution of miRNA binding sites is helpful in understanding the co-evolution between miRNAs and their targets. To understand this process in plants a comparative analysis of miRNA-targeted duplicated gene pairs derived from a well-documented whole genome duplication (WGD) event in combination with a population genetics study of six experimentally validated miRNA binding sites in rice (O. sativa) was carried out.ResultsOf the 1,331 pairs of duplicate genes from the WGD, 41 genes (29 pairs) were computationally predicted to be miRNA targets. Sequence substitution analysis indicated that the synonymous substitution rate was significantly lower in the miRNA binding sites than their 5' and 3' flanking regions. Of the 29 duplicated gene pairs, 17 have only one paralog been targeted by a miRNA. This could be due to either gain of a miRNA binding site after the WGD or because one of the duplicated genes has escaped from being a miRNA target after the WGD (loss of miRNA binding site). These possibilities were distinguished by separating miRNAs conserved in both dicots and monocot plants from rice-specific miRNAs and by phylogenetic analysis of miRNA target gene families. The gain/loss rate of miRNA binding sites was estimated to be 3.0 x 10(-9) gain/loss per year. Most (70.6%) of the gains/losses were due to nucleotide mutation. By analysis of cultivated (O. sativa; n = 30) and wild (O. rufipogon; n = 15) rice populations, no segregating site was observed in six miRNA binding sites whereas 0.12-0.20 SNPs per 21-nt or 1.53-1.80 x 10(-3) of the average pairwise nucleotide diversity (pi) were found in their flanking regions.ConclusionBoth molecular evolution and population genetics support the hypothesis that conservation of miRNA binding sites is maintained by purifying selection through elimination of deleterious alleles. Nucleotide mutations play a major role in the gain/loss of miRNA binding sites during evolution.

Project description:BackgroundConvergent and parallel evolution provide unique insights into the mechanisms of natural selection. Some of the most striking convergent and parallel (collectively recurrent) amino acid substitutions in proteins are adaptive, but there are also many that are selectively neutral. Accordingly, genome-wide assessment has shown that recurrent sequence evolution in orthologs is chiefly explained by nearly neutral evolution. For paralogs, more frequent functional change is expected because additional copies are generally not retained if they do not acquire their own niche. Yet, it is unknown to what extent recurrent sequence differentiation is discernible after independent gene duplications in different eukaryotic taxa.ResultsWe develop a framework that detects patterns of recurrent sequence evolution in duplicated genes. This is used to analyze the genomes of 90 diverse eukaryotes. We find a remarkable number of families with a potentially predictable functional differentiation following gene duplication. In some protein families, more than ten independent duplications show a similar sequence-level differentiation between paralogs. Based on further analysis, the sequence divergence is found to be generally asymmetric. Moreover, about 6% of the recurrent sequence evolution between paralog pairs can be attributed to recurrent differentiation of subcellular localization. Finally, we reveal the specific recurrent patterns for the gene families Hint1/Hint2, Sco1/Sco2 and vma11/vma3.ConclusionsThe presented methodology provides a means to study the biochemical underpinning of functional differentiation between paralogs. For instance, two abundantly repeated substitutions are identified between independently derived Sco1 and Sco2 paralogs. Such identified substitutions allow direct experimental testing of the biological role of these residues for the repeated functional differentiation. We also uncover a diverse set of families with recurrent sequence evolution and reveal trends in the functional and evolutionary trajectories of this hitherto understudied phenomenon.

Dataset Information

Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication.

Publications

Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication.

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