Low Nucleotide Diversity for the Expanded Organelle and Nuclear Genomes of Volvox carteri Supports the Mutational-Hazard Hypothesis

Abstract

The noncoding-DNA content of organelle and nuclear genomes can vary immensely. Both adaptive and nonadaptive explanations for this variation have been proposed. This study addresses a nonadaptive explanation called the mutational-hazard hypothesis and applies it to the mitochondrial, plastid, and nuclear genomes of the multicellular green alga Volvox carteri. Given the expanded architecture of the V. carteri organelle and nuclear genomes (60-85% noncoding DNA), the mutational-hazard hypothesis would predict them to have less silent-site nucleotide diversity (π(silent)) than their more compact counterparts from other eukaryotes-ultimately reflecting differences in 2N(g)μ (twice the effective number of genes per locus in the population times the mutation rate). The data presented here support this prediction: Analyses of mitochondrial, plastid, and nuclear DNAs from seven V. carteri forma nagariensis geographical isolates reveal low values of π(silent) (0.00038, 0.00065, and 0.00528, respectively), much lower values than those previously observed for the more compact organelle and nuclear DNAs of Chlamydomonas reinhardtii (a close relative of V. carteri). We conclude that the large noncoding-DNA content of the V. carteri genomes is best explained by the mutational-hazard hypothesis and speculate that the shift from unicellular to multicellular life in the ancestor that gave rise to V. carteri contributed to a low V. carteri population size and thus a reduced 2N(g)μ. Complete mitochondrial and plastid genome maps for V. carteri are also presented and compared with those of C. reinhardtii.