Dynamics of plant mitochondrial genome: model of a three-level selection process

Abstract

The plant mitochondrial genome is composed of a set of molecules of various sizes that generate each other through recombination between repeated sequences. Molecular observations indicate that these different molecules are present in an equilibrium state. Different compositions of molecules have been observed within species. Recombination could produce deleted molecules with a high replication rate but bearing little useful information for the cell (such as "petite" mutants in yeast). In this paper we use a multilevel model to examine selection among rapidly replicating incomplete molecules and relatively slowly replicating complete molecules. Our model simulates the evolution of mitochondrial information through a three-level selection process including intermolecular, intermitochondrial, and intercellular selection. The model demonstrates that maintenance of the mitochondrial genome can result from multilevel selection, but maintenance is difficult to explain without the existence of selection at the intermitochondrial level. This study shows that compartmentation into mitochondria is useful for maintenance of the mitochondrial information. Our examination of evolutionary equilibria shows that different equilibria (with different combinations of molecules) can be obtained when recombination rates are lower than a threshold value. This may be interpreted as a drift-mutation balance.