Global patterns of subgenome evolution in organelle-targeted genes of six allotetraploid angiosperms

Whole-genome duplications (WGDs), in which the number of nuclear genome copies is elevated as a result of autopolyploidy or allopolyploidy, are a prominent process of diversification in eukaryotes. The genetic and evolutionary forces that WGD imposes upon cytoplasmic genomes are not well understood, despite the central role that cytonuclear interactions play in eukaryotic function and fitness. Cellular respiration and photosynthesis depend upon successful interaction between the 3000+ nuclear-encoded proteins destined for the mitochondria or plastids and the gene products of cytoplasmic genomes in multi-subunit complexes such as OXPHOS, organellar ribosomes, Photosystems I and II, and Rubisco. Allopolyploids are thus faced with the critical task of coordinating interactions between nuclear and cytoplasmic genes that were inherited from different species. Because cytoplasmic genomes share a more recent history of common descent with the maternal nuclear subgenome than the paternal subgenome, evolutionary “mismatches” in allopolyploids might lead to accelerated rates of evolution in paternal homoeologs of organelle-targeted genes. We tested this hypothesis in maternal vs. paternal copies of organelle-targeted genes in six allotetraploids: Brachypodium hybridum (Poaceae), Chenopodium quinoa (Amaranthaceae), Coffea arabica (Rubiaceae), Gossypium hirsutum (Malvaceae), Nicotiana tabacum (Solanaceae), and Triticum dicoccoides (Poaceae). We report evidence that allopolyploid subgenomes exhibit highly biased rates of protein-sequence evolution genome-wide, but we did not observe global effects of cytonuclear incompatibilities on paternal homoeologs of organelle-targeted genes. We did, however, find taxon- and complex-specific evidence of cytonuclear incompatibilities in the mitochondrial enzyme complexes of allotetraploid wheat. There was mixed evidence for whether organelle-targeted genes re-diploidize more rapidly than non-organelle-targeted genes, indicating that additional work is needed to understand the evolution of cytonuclear stoichiometry. These global analyses provide insights into the complex evolutionary dynamics of allopolyploid genomes, showing that despite sharing the same nucleus, generation time, and ecological context, allopolyploid subgenomes have separate evolutionary trajectories.