Variable Populations Within Variable Populations: Quantifying Mitochondrial Heteroplasmy in Natural Populations of the Gynodioecious PlantSilene vulgaris

Abstract

Populations of mitochondria reside within individuals. Among angiosperms, these populations are rarely considered as genetically variable entities and typically are not found to be heteroplasmic in nature, leading to the widespread assumption that plant mitochondrial populations are homoplasmic. However, empirical studies of mitochondrial variation in angiosperms are relatively uncommon due to a paucity of sequence variation. Recent greenhouse studies of Silene vulgaris suggested that heteroplasmy might occur in this species at a level that it is biologically relevant. Here, we use established qualitative methods and a novel quantitative PCR method to study the intraindividual population genetics of mitochondria across two generations in natural populations of S. vulgaris. We show incidences of heteroplasmy for mitochondrial atpA and patterns of inheritance that are suggestive of more widespread heteroplasmy at both atpA and cox1. Further, our results demonstrate that quantitative levels of mitochondrial variation within individuals are high, constituting 26% of the total in one population. These findings are most consistent with a biparental model of mitochondrial inheritance. However, selection within individuals may be instrumental in the maintenance of variation because S. vulgaris is gynodioecious. Male sterility is, in part, regulated by the mitochondrial genome, and strong selection pressures appear to influence the frequency of females in these populations.

The Effect of Breeding System on Polymorphism in Mitochondrial Genes of Silene

“…Further evidence of intragenic as well as intergenic recombination in S. vulgaris has recently been shown for several mitochondrial genes (Houliston and Olson 2006;McCauley and Ellis 2008). In addition, data have been shown that are congruent with the idea that heteroplasmy can occur through occasional paternal leakage in S. vulgaris Welch et al 2006), one of the conditions that can yield recombination between variant mitochondrial genomes. Without overestimating the role of recombination in shaping intragenic diversity in Silene mitochondria (see discussion in Barr et al 2007 andEllis 2008), the accumulation of evidence of four-gamete types for several species and genes suggests a common occurrence of this phenomenon in the genus, most likely through past heteroplasmy events.…”

Genetic determination of male sterility in gynodioecious Silene nutans

“…The most likely mechanism that generates heteroplasmy is paternal transmission of mitochondria, as has been found for Silene vulgaris Welch et al, 2006;Pearl et al, 2009). We checked the mitotypes of progenies from our crosses and found no cases suggesting paternal transmission of mitochondria (unpublished data).…”

Detection of rare paternal chloroplast inheritance in controlled crosses of the endangered sunflower Helianthus verticillatus

“…Documentation of chloroplast heteroplasmy is rare (but see Frey et al, 2005) perhaps due in part to the dogma of strict maternal inheritance in angiosperms. Intraindividual variation has been observed and quantified for plant mitochondrial genes in several cases, (Hattori et al, 2002;McCauley et al, 2005;Welch et al, 2006) but such observations remain rare. Perhaps not surprisingly heteroplasmy occurs if paternal leakage takes place given that the mother presumably always transfers organelles to her offspring.…”