When One Genome Is Not Enough: Organellar Heteroplasmy in Plants

Abstract

Heteroplasmy occurs when copies of an organellar genome (plastid or mitochondrial) differ from one another either within a cell or among cells within an individual. This phenomenon was first discovered in plastids over 100 years ago, though ‘heteroplasmy’ was not formally defined until decades later. Mitochondrial and plastid heteroplasmy have since been discovered in diverse taxa, including numerous plants, particularly those with the gynodioecious breeding system. Though heteroplasmy can arise through mutations in organellar genomes, biparental inheritance of organelles often generates heteroplasmy. This article is intended to summarise the cytoploid nature of organellar genomes and different aspects of mitochondrial and plastid heteroplasmy, from its discovery, to the development of detection methods. We will also discuss the effects of heteroplasmy on individuals, populations, and species, with regard to fitness, cytonuclear interactions, and genome evolution. Finally, we highlight a few research questions which we consider in need of further investigation to understand the prevalence and effects of heteroplasmy in natural settings.

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…In this case, CMS will only be revealed in crosses involving populations that do not contain the proper nuclear Rf locus [62,63]. Thus, in case of hybridization between populations/species, CNI can be the result of CMS-Rf systems disruption among hybrids containing mismatched CMS genes and nuclear Rf [12,64]. Rf genes are often part of the PPR gene family which encodes proteins targeted to organelles and involved in organellar biogenesis, transcription regulation and RNAe [65].…”

“…Biparental transmission has arisen multiple times within the angiosperms and about 20% of the angiosperm species have the potential for biparental inheritance [55,64,83]. Accidental paternal transmission of organellar genomes (i.e., paternal leakage) can occur in crosses of divergent populations or species, due to a breakdown of mechanisms preventing biparental transmission [19,64,82].…”

“…Biparental transmission has arisen multiple times within the angiosperms and about 20% of the angiosperm species have the potential for biparental inheritance [55,64,83]. Accidental paternal transmission of organellar genomes (i.e., paternal leakage) can occur in crosses of divergent populations or species, due to a breakdown of mechanisms preventing biparental transmission [19,64,82]. In this case, paternal organellar DNA can endure different fates: it can be (i) destroyed within the sperm cell, (ii) physically excluded from the egg cell during fertilization or (iii) successfully replicated and maintained in the zygote after fertilization [39,64,82].…”

“…Accidental paternal transmission of organellar genomes (i.e., paternal leakage) can occur in crosses of divergent populations or species, due to a breakdown of mechanisms preventing biparental transmission [19,64,82]. In this case, paternal organellar DNA can endure different fates: it can be (i) destroyed within the sperm cell, (ii) physically excluded from the egg cell during fertilization or (iii) successfully replicated and maintained in the zygote after fertilization [39,64,82]. The latter case will lead to heteroplasmic individuals with two organellar haplotypes.…”

“…Hybrids will have variegated leaves or fully green/white ones, as a result of sorting-out the two plastid types during ontogenesis [83,84]. It indicates that one of the two parental plastids is unable to develop and undergo normal differentiation under the hybrid nuclear background, potentially because it is incompatible, while the other one is not [37,[84][85][86][87], leading to chlorophyll-deficiency leaf sectors (i.e., white or yellowish sectors) [64,85].…”