Frequent, geographically structured heteroplasmy in the mitochondria of a flowering plant, ribwort plantain (Plantago lanceolata).

N Levsen,D Charlesworth,R Bergero,K Wolff

doi:10.1038/hdy.2016.15

N Levsen, D Charlesworth + Show 2 more

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https://doi.org/10.1038/hdy.2016.15

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Journal: Heredity	Publication Date: Mar 9, 2016
Citations: 17	License type: CC BY 4.0

Affiliation: University of Edinburgh, Newcastle University

Abstract

Recent research has convincingly documented cases of mitochondrial heteroplasmy in a small set of wild and cultivated plant species. Heteroplasmy is suspected to be common in flowering plants and investigations of additional taxa may help understand the mechanisms generating heteroplasmy as well as its effects on plant phenotypes. The role of mitochondrial heteroplasmy is of particular interest in plants as cytoplasmic male sterility is controlled by mitochondrial genotypes, sometimes leading to co-occurring female and hermaphroditic individuals (gynodioecy). Paternal leakage may be important in the evolution of mating systems in such populations. We conducted a genetic survey of the gynodioecious plant Plantago lanceolata, in which heteroplasmy has not previously been reported, and estimated the frequencies of mitochondrial genotypes and heteroplasmy. Sanger sequence genotyping of 179 individuals from 15 European populations for two polymorphic mitochondrial loci, atp6 and rps12, identified 15 heteroplasmic individuals. These were distributed among 6 of the 10 populations that had polymorphisms in the target loci and represented 8% of all sampled individuals and 15% of the individuals in those 6 populations. The incidence was highest in Northern England and Scotland. Our results are consistent with geographic differences in the incidence of paternal leakage and/or the rates of nuclear restoration of male fertility.

Highlights

In genetic studies of flowering plants, it is often assumed that most individuals carry a single complement of mitochondrial genes inherited from the maternal parent
All individuals represented by dried leaf or living material were genotyped, whereas wild collected seeds were germinated and one plant per seed family was chosen for downstream analyses
Our results show that gynodioecious populations of P. lanceolata contain single-nucleotide polymorphism sequence variants in mitochondrial genes, including both synonymous and nonsynonymous variants

Summary

Introduction

In genetic studies of flowering plants, it is often assumed that most individuals carry a single complement of mitochondrial genes inherited from the maternal parent. Increasing numbers of reports from crop (see, for example, Bragin et al, 2012; Szklarczyk et al, 2014) and wild species (see, for example, McCauley et al, 2005; Mandel and McCauley, 2015) have documented the co-occurrence of multiple mitochondrial genotypes within plant cells (termed mitochondrial heteroplasmy), suggesting that it might be common in many angiosperms (Kmiec et al, 2006). Flowering plants generally exhibit low mitochondrial mutation rates (Wolfe et al, 1987); paternal leakage is considered the predominant mechanism generating heteroplasmy in angiosperms (McCauley, 2013; Christie et al, 2015). Highly pathogenic point mutations in human mitochondrial genes often remain heteroplasmic (Ye et al, 2014). Such heteroplasmy could be deleterious because of mitochondrial competition, either between functional mitotypes or between functional and nonfunctional mitotypes that could produce metabolic dysfunction (Sharpley et al, 2012; Greiner et al, 2014)

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