Cytoplasmic genomes change allelic expression bias in plant seeds independently of parental imprinting: evidence for cytonuclear regulatory epistasis in Arabidopsis thaliana

Abstract

Cytoplasmic genomes play critical roles in plant cells, yet their potential contribution to regulation of the nuclear genome remains largely unexplored. Here, we examine how cytoplasmic genotype affects allelic dominance at nuclear loci by identifying allele-specific expression in hybrid plant lines in which cytoplasmic genomes have been swapped between accessions. After developing a bias-free ASE analysis pipeline based on dual pseudo-genome alignment, we determined ASE across 48 RNA-seq datasets of the model plant, Arabidopsis thaliana and distinguished between allelic bias under the control of the genotype and or the cytoplasm. Of 7,997 nuclear genes for which informative SNPs could be mapped, 2,702 displayed allelic imbalances, the great majority controlled by the nuclear background. However cytoplasmic interactions with nuclear genotype were found to regulate ASE at 24 genes. We also tested interactions with genomic imprinting, a specific form of ASE in which parental inheritance determines expression state, within seed transcriptomes: while we detected both novel and previously-reported imprinted genes, only three genes (VFB1, ANNAT3, ENODL2) exhibited both parent-of-origin bias and cytoplasm-responsiveness. This indicates that these two parental inheritance mechanisms are largely independent, with implications for maternal-cytoplasmic coadaptation theories. Interestingly, genes subject to cytoplasmic ASE were enriched in the ascorbate and aldarate metabolism pathway, with the highest ASE biases found in GAE4 and UGD3. We conclude that cytoplasmic variation can selectively alter expression of nuclear-encoded alleles and that this may represent a novel source of control of cellular energy balance and metabolic signalling pathways.