Nucleotide diversity of the Chlamydomonas reinhardtii plastid genome: addressing the mutational-hazard hypothesis

Background: The mutational-hazard hypothesis argues that the noncoding-DNA content of a genome is a consequence of the mutation rate (mu) and the effective number of genes per locus in the population (N-g). The hypothesis predicts that genomes with a high N-g mu will be more compact than those with a small Ng mu. Approximations of Ng mu can be gained by measuring the nucleotide diversity at silent sites (pi(silent)). We addressed the mutation-hazard hypothesis apropos plastid-genome evolution by measuring p silent of the Chlamydomonas reinhardtii plastid DNA (ptDNA), the most noncoding-DNA-dense plastid genome observed to date. The data presented here in conjunction with previously published values of p silent for the C. reinhardtii mitochondrial and nuclear genomes, which are respectively compact and bloated, allow for a complete analysis of nucleotide diversity and genome compactness in all three genetic compartments of this model organism. Results: In C. reinhardtii, the mean estimate of pi(silent) for the ptDNA (14.5 x 10(-3)) is less than that of the nuclear DNA (32 x 10(-3)) and greater than that of the mitochondrial DNA (8.5 x 10(-3)). On average, C. reinhardtii has similar to 4 times more silent-site ptDNA diversity than the mean value reported for land plants, which have more compact plastid genomes. The silent-site nucleotide diversity of the different ptDNA loci that were studied varied significantly: from 0 to 71 x 10(-3) for synonymous sites and from 0 to 42 x 10(-3) for intergenic regions. Conclusion: Our findings on silent-site ptDNA diversity are inconsistent with what would be expected under the mutational-hazard hypothesis and go against the documented trend in other systems of p silent positively correlating with genome compactness. Overall, we highlight the lack of reliable nucleotide-diversity measurements for ptDNA and hope that the values presented here will act as sound data for future research concerning the mutational-hazard hypothesis and plastid evolution in general.