Paternal leakage and heteroplasmy of mitochondrial genomes in Silene vulgaris: evidence from experimental crosses

Abstract

The inheritance of mitochondrial genetic (mtDNA) markers in the gynodioecious plant Silene vulgaris was studied using a series of controlled crosses between parents of known mtDNA genotype followed by quantitative PCR assays of offspring genotype. Overall, approximately 2.5% of offspring derived from crosses between individuals that were homoplasmic for different mtDNA marker genotypes showed evidence of paternal leakage. When the source population of the pollen donor was considered, however, population-specific rates of leakage varied significantly around this value, ranging from 10.3% to zero. When leakage did occur, the paternal contribution ranged from 0.5% in some offspring (i.e., biparental inheritance resulting in a low level of heteroplasmy) to 100% in others. Crosses between mothers known to be heteroplasmic for one of the markers and homoplasmic fathers showed that once heteroplasmy enters a maternal lineage it is retained by approximately 17% of offspring in the next generation, but lost from the others. The results are discussed with regard to previous studies of heteroplasmy in open-pollinated natural populations of S. vulgaris and with regard to the potential impact of mitochondrial paternal leakage and heteroplasmy on both the evolution of the mitochondrial genome and the evolution of gynodioecy.

Figure 1.—

The distribution of the relative magnitudes of the paternal contribution to the atp1 genotypes of the 29 offspring from the experimental crosses that show paternal leakage. The number of offspring showing paternal leakage in the A/D assay (shaded bars) is stacked above the number obtained from the A/B assay (solid bars).

Figure 2.—

The distribution of 29 paternal leakage events observed in the experimental crosses among the 13 natural populations of Silene vulgaris from which pollen donors were derived. For each source population the proportion of offspring displaying leakage is presented along with the total number of offspring fathered by all pollens donor derived from that population.

Figure 3.—

Offspring from the heteroplasmic crosses standardized as a proportion of the heteroplasmy found in their respective heteroplasmic mothers. Owing to the standardization, all mothers have a score of one and an offspring with a score of one would indicate no change between generations. Results from the A/B assay are presented on the right and the A/D assay on the left side. Note that in four cases the thickness of the line is indicative of multiple individuals with approximately equivalent trajectories, with the number of individuals contributing to those lines indicated. The scale of the upper end of the A/D assay offspring axis has been altered to accommodate a single observation of offspring heteroplasmy that is nearly nine times that of its mother.