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Open Access Research article

Molecular adaptation and expression evolution following duplication of genes for organellar ribosomal protein S13 in rosids

Shao-Lun Liu and Keith Adams*

Author Affiliations

UBC Botanical Garden & Centre for Plant Research and Botany Department, University of British Columbia, Vancouver, BC, V6T1Z4, Canada

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BMC Evolutionary Biology 2008, 8:25  doi:10.1186/1471-2148-8-25

Published: 26 January 2008

Abstract

Background

Gene duplication has been a fundamental process in the evolution of eukaryotic genomes. After duplication one copy (or both) can undergo divergence in sequence, expression pattern, and function. Two divergent copies of the ribosomal protein S13 gene (rps13) of chloroplast origin are found in the nucleus of the rosids Arabidopsis, Gossypium, and Glycine. One encodes chloroplast-imported RPS13 (nucp rps13), while the other encodes mitochondria-imported RPS13 (numit rps13). The rps13 gene has been lost from mitochondrial DNA (mt rps13) of many rosids.

Results

We studied sequence evolution of numit rps13 in comparison with nucp rps13 in seven rosid genera. Ka/Ks analysis and likelihood ratio tests showed considerably higher Ka values and Ka/Ks ratios in numit rps13 than in nucp rps13, indicating increased amino acid sequence divergence in numit rps13. Two positively selected codons were detected in numit RPS13 in regions that are inferred to interact with the 16S rRNA. Several amino acids in numit RPS13 have changed from the one present in nucp RPS13 to the one present in mt RPS13, showing that numit rps13 is becoming more like mt rps13. Comparison of expression patterns and levels of numit rps13 and nucp rps13 in Arabidopsis using microarray data indicated divergence in gene expression. We discovered that in addition to numit rps13, Malus (apple) contains a transcribed mt rps13 gene. To determine if partitioning of expression takes place between numit rps13 and mt rps13, expression of both copies and RNA editing of mt rps13 were examined by RT-PCR, qRT-PCR, and sequencing from 14 different organ types plus seedlings subjected to five different abiotic stresses. Co-expression of numit rps13 and mt rps13 was observed in all the organs and various stress treatments. We determined that purifying selection is acting on both numit rps13 and mt rps13 in Malus.

Conclusion

Our data provide evidence that numit rps13 genes in rosids have experienced adaptive sequence evolution and convergent evolution with mt rps13. Co-expression of numit rps13 and mt rps13 and purifying selection on both genes in Malus suggest that both are functional. The three organellar rps13 genes in rosids provide a distinctive case of gene duplication involving the co-evolution of the nuclear and cytoplasmic genomes.