A photosynthesis operon in the chloroplast genome drives speciation in evening primroses

Incompatibility between the cytoplasm and the nucleus is considered as major factor in species formation, but mechanistic understanding is poor. In evening primroses, a model plant for organelle genetics and population biology, hybrid offspring regularly displays chloroplast-nuclear incompatibility. These incompatibilities affect photosynthesis, a trait under selection in changing environments. Here we show that light-dependent misregulation of the plastid psbB operon (encoding core subunits of photosystem II and the cytochrome b6f complex), can lead to hybrid incompatibility, thus ultimately driving speciation. This misregulation results in an impaired light acclimation response in incompatible plants. Moreover, as a result of their different chloroplast genotypes, the parental lines differ in their photosynthesis performance upon exposure to different light conditions. Significantly, the incompatible chloroplast genome is naturally found in xeric habitats with high light intensities, whereas the compatible one is limited to mesic habitats. Consequently, our data raise the possibility that the hybridization barrier evolved as a result of adaptation to specific climatic conditions.