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

ABSTRACT 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” between the paternal subgenome and the cytoplasmic genomes in allopolyploids might lead to accelerated rates of evolution in the paternal homoeologs of allopolyploids, either through relaxed purifying selection or strong directional selection to rectify these mismatches. We tested this hypothesis in maternal vs. paternal copies of organelle-targeted genes in six allotetraploids: Brachypodium hybridum, Chenopodium quinoa, Coffea arabica, Gossypium hirsutum, Nicotiana tabacum, and Triticum dicoccoides. We report evidence that allopolyploid subgenomes exhibit unequal rates of protein-sequence evolution, but we did not observe global effects of cytonuclear incompatibilities on paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes re-diploidize more rapidly than non-organelle-targeted genes. Together, these global analyses provide insights into the complex evolutionary dynamics of allopolyploids, showing that allopolyploid subgenomes have separate evolutionary trajectories despite sharing the same nucleus, generation time, and ecological context. AUTHOR SUMMARY Whole genome duplication, in which the size and content of the nuclear genome is instantly doubled, represents one of the most profound forms of mutational change. The consequences of duplication events are equally monumental, especially considering that almost all eukaryotes have undergone whole genome duplications during their evolutionary history. While myriad genetic, cellular, organismal, and ecological effects of whole genome duplications have been extensively documented, relatively little attention has been paid to the diminutive but essential “other” genomes present inside the cell, those of chloroplasts and mitochondria. In this study, we compared the evolutionary patterns of >340,000 genes from 23 species to test whether whole genome duplications are associated with genetic mismatches between the nuclear, mitochondrial, and chloroplast genomes. We discovered tremendous differences between duplicated copies of nuclear genomes; however, mitochondria-nuclear and chloroplast-nuclear mismatches do not appear to be common following whole genome duplications. Together these genomic data represent the most extensive analysis yet performed on how polyploids maintain the delicate and finely tuned balance between the nuclear, mitochondrial, and chloroplast genomes.