Whole-genome duplications (WGD) through polyploid speciation are associated with disruptions of well-tuned relationships among the three plant cell genomes. Key metabolic processes comprising multi-subunit enzyme complexes, for which partner proteins are both nuclear- and plastid-encoded, are dependent on maintenance of stoichiometric ratios among the subunits to avoid cytonuclear imbalances after WGDs. By using qPCR for gene copy and transcript number quantification, we have studied the relationship of subunit expression in the two gene pairs rbcL/rbcS (the two subunits of RuBisCO) and psbA/psbO (two members of photosystem II) in closely related members of Leucanthemum (Compositae, Anthemideae), comprising a diploid, a tetraploid, and a hexaploid species. While gene copy numbers exhibit the expected pattern of an increase in the nuclear-encoded partner gene relative to the plastid-encoded one, we find that the two partner gene systems behave differently after WGD: While in the psbA/psbO partner gene system, shifts in the gene copy balance caused by polyploidization are not accommodated for through changes in transcription intensities of the two partner genes, the rbcL/rbcS system even shows an unexpected reversed dosage effect with up-regulated transcription intensities on both the nuclear and the plastidal side. We interpret the behavior of the psbA/psbO partner gene system as being due to the stoichiometrically relaxed relationship between the two gene products caused by a fast, damage-provoked combustion of the psbA gene product (the D1 core protein of PSII). Conversely, the finely tuned expression dependencies of the rbcL/rbcS system may be the reason for the observed positive feedback runaway signal as reaction to gene copy imbalances caused by a polyploidization shock.