Disentangling Complex Inheritance Patterns of Plant Organellar Genomes: An Example From Carrot

Abstract

Abstract Plant mitochondria and plastids display an array of inheritance patterns and varying levels of heteroplasmy, where individuals harbor more than 1 version of a mitochondrial or plastid genome. Organelle inheritance in plants has the potential to be quite complex and can vary with plant growth, development, and reproduction. Few studies have sought to investigate these complicated patterns of within-individual variation and inheritance using experimental crosses in plants. We carried out crosses in carrot, Daucus carota L. (Apiaceae), which has previously been shown to exhibit organellar heteroplasmy. We used mitochondrial and plastid markers to begin to disentangle the patterns of organellar inheritance and the fate of heteroplasmic variation, with special focus on cases where the mother displayed heteroplasmy. We also investigated heteroplasmy across the plant, assaying leaf samples at different development stages and ages. Mitochondrial and plastid paternal leakage was rare and offspring received remarkably similar heteroplasmic mixtures to their heteroplasmic mothers, indicating that heteroplasmy is maintained over the course of maternal inheritance. When offspring did differ from their mother, they were likely to exhibit a loss of the genetic variation that was present in their mother. Finally, we found that mitochondrial variation did not vary significantly over plant development, indicating that substantial vegetative sorting did not occur. Our study is one of the first to quantitatively investigate inheritance patterns and heteroplasmy in plants using controlled crosses, and we look forward to future studies making use of whole genome information to study the complex evolutionary dynamics of plant organellar genomes.