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 (μ) and the effective number of genes per locus in the population (N(g)). The hypothesis predicts that genomes with a high N(g)μ will be more compact than those with a small N(g)μ. Approximations of N(g)μ can be gained by measuring the nucleotide diversity at silent sites (π(silent)). We addressed the mutation-hazard hypothesis apropos plastid-genome evolution by measuring π(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 π(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 π(silent )forthe ptDNA (14.5 × 10(-3)) is less than that of the nuclear DNA (32 × 10(-3)) and greater than that of the mitochondrial DNA (8.5 × 10(-3)). On average, C. reinhardtii has ~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 × 10(-3 )for synonymous sites and from 0 to 42 × 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 π(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.