Causes and Consequences of Cytonuclear Incompatibility in Hybrids of Flowering Plants

Abstract Hybridization and polyploidization combine divergent nuclear genomes with maternally inherited organelles, often disrupting cytonuclear coadaptation critical for respiration and photosynthesis. This review examines the mechanisms, outcomes, and evolutionary significance of cytonuclear incompatibility in plants. We focus on how divergence in nuclear-encoded, organelle-targeted proteins and organelle genomes leads to mismatched interactions in protein import, folding, and assembly of multi-subunit enzyme complexes. The evidence highlights taxon- and complex-specific responses that mitigate incompatibilities, including the biased retention and expression of maternal alleles, gene conversions, and regulatory adjustments. We highlight how cytonuclear compatibility in hybrid lineages entails responses at multiple levels of regulation, including methylation/chromatin accessibility, gene expression, alternative splicing, translation rates, organelle import, protein-folding and assembly, and protein degradation pathways. Manifestations such as chlorosis, seed sterility, or hybrid breakdown underscore their role in shaping reproductive barriers. Conversely, maternal bias and compensatory mechanisms often act to restore functional integration of parental genomes, allowing hybrid and polyploid persistence. Beyond their evolutionary role in speciation and adaptation, cytonuclear incompatibilities underpin key practical applications, notably cytoplasmic male sterility, a cornerstone of hybrid crop breeding. We conclude that cytonuclear dynamics reveal both constraints and opportunities, illuminating plant diversification, hybrid resilience, and agricultural innovation.