Evolution of ribonuclease H genes in prokaryotes to avoid inheritance of redundant genes.
BACKGROUND
A theoretical model of genetic redundancy has proposed that the fates of redundant genes depend on the degree of functional redundancy, and that functionally redundant genes will not be inherited together. However, no example of actual gene evolution has been reported that can be used to test this model. Here, we analyzed the molecular evolution of the ribonuclease H (RNase H) family in prokaryotes and used the results to examine the implications of functional redundancy for gene evolution.


RESULTS
In prokaryotes, RNase H has been classified into RNase HI, HII, and HIII on the basis of amino acid sequences. Using 353 prokaryotic genomes, we identified the genes encoding the RNase H group and examined combinations of these genes in individual genomes. We found that the RNase H group may have evolved in such a way that the RNase HI and HIII genes will not coexist within a single genome--in other words, these genes are inherited in a mutually exclusive manner. Avoiding the simultaneous inheritance of the RNase HI and HIII genes is remarkable when RNase HI contains an additional non-RNase H domain, double-stranded RNA, and an RNA-DNA hybrid-binding domain, which is often observed in eukaryotic RNase H1. This evolutionary process may have resulted from functional redundancy of these genes, because the substrate preferences of RNase HI and RNase HIII are similar.


CONCLUSIONS
We provide two possible evolutionary models for RNase H genes in which functional redundancy contributes to the exclusion of redundant genes from the genome of a species. This is the first empirical study to show the effect of functional redundancy on changes in gene constitution during the course of evolution.
Institute for Advanced Biosciences, Keio University, Tsuruoka, Japan. hiromi@sfc.keio.ac.jp <hiromi@sfc.keio.ac.jp>
Hiromi
H
Kochiwa
Masaru
M
Tomita
Akio
A
Kanai
D000595:Amino Acid Sequence; D001426:Bacterial Proteins / Q000235:genetics; D001499:Bayes Theorem; D030541:Databases, Genetic; D019143:Evolution, Molecular; D019766:Genes, Archaeal / Q000235:genetics*; D005798:Genes, Bacterial / Q000235:genetics*; D020745:Genome, Archaeal; D016680:Genome, Bacterial; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010802:Phylogeny; D011387:Prokaryotic Cells / Q000201:enzymology / Q000378:metabolism; D016914:Ribonuclease H / Q000235:genetics*; D012260:Ribonucleases / Q000235:genetics; D017386:Sequence Homology, Amino Acid
D001426:Bacterial Proteins; D012260:Ribonucleases; C091139:ribonuclease HII; C117079:ribonuclease HIII; D016914:Ribonuclease H; C078856:ribonuclease HI