Due to the endosymbiotic origin of organelles, a pattern of coevolution and coadaptation between organellar and nuclear genomes is required for proper cell function. In this review, we focus on the impact of cytonuclear interaction on the reproductive isolation of plant species. We give examples of cases where species exhibit barriers to reproduction which involve plastid-nuclear or mito-nuclear genetic incompatibilities, and describe the evolutionary processes at play. We also discuss potential mechanisms of hybrid fitness recovery such as paternal leakage. Finally, we point out the possible interplay between plant mating systems and cytonuclear coevolution, and its consequence on plant speciation.

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IntroductionFollowing the integration of cyanobacteria into the eukaryotic cells, many genes were transferred from the plastid to the nucleus. As a result, plastid complexes are encoded both by plastid and nuclear genes. Tight co-adaptation is required between these genes as plastid and nuclear genomes differ in several characteristics, such as mutation rate and inheritance patterns. Among these are complexes from the plastid ribosome, composed of two main subunits: a large and a small one, both composed of nuclear and plastid gene products. This complex has been identified as a potential candidate for sheltering plastid–nuclear incompatibilities in a Caryophyllaceae species, Silene nutans. This species is composed of four genetically differentiated lineages, which exhibit hybrid breakdown when interlineage crosses are conducted. As this complex is composed of numerous interacting plastid–nuclear gene pairs, in the present study, the goal was to reduce the number of gene pairs that could induce such incompatibilities. MethodWe used the previously published 3D structure of the spinach ribosome to further elucidate which of the potential gene pairs might disrupt plastid–nuclear interactions within this complex. After modeling the impact of the identified mutations on the 3D structure, we further focused on one strongly mutated plastid–nuclear gene pair: rps11–rps21. We used the centrality measure of the mutated residues to further understand if the modified interactions and associated modified centralities might be correlated with hybrid breakdown. Results and discussionThis study highlights that lineage-specific mutations in essential plastid and nuclear genes might disrupt plastid–nuclear protein interactions of the plastid ribosome and that reproductive isolation correlates with changes in residue centrality values. Because of this, the plastid ribosome might be involved in hybrid breakdown in this system.