Replicators, genes, and the C-value enigma: High-quality genome assembly of barley provides direct evidence that self-replicating DNA forms ‘cooperative’ associations with genes in arms races

Abstract

AbstractThe C-value enigma—the apparent disjunction between the complexity of organisms and the sizes of their genomes—could be in part resolved if it were definitively shown that tolerance of self-copying DNA elements incurred an occasional selective advantage. We leverage the power of the latest genome assembly of the exceptionally repetitive and well-studied cereal crop barley (Hordeum vulgareL.) to explicitly test the hypothesis that the population of genes that have been repeatedly replicated by the action of replication-inducing sequences has undergone selection, favouring genes involved in co-evolutionary arms races (such as genes implicated in pathogen resistance). This was achieved by algorithmically identifying 1,999 genomic stretches that are locally rich in long repeated units. In these loci, we identified 554 geanes, belonging to 42 gene families. These gene families strongly overlap with a test set of pathogen resistance and other likely evolutionary ‘arms-race’ genes compiled independently from the literature. By statistically demonstrating that selection has systematically influenced the composition of replicator-associated genes at a genome-wide scale we provide evidence that tolerance of repeat-inducing DNA sequences is an adaptive strategy that may contribute to enigmatically inflated C-values, and invite more detailed research on how particular genes become prone to duplication, to the organism’s advantage. To this end, we examined the genomic sequences surrounding several of the candidate gene families, and find a repeated pattern of genomic disperse-and-expand dynamics, but where the repeated genomic unit itself varies between sites of expansion. This suggests that genes effectively form opportunistic relationships with replication-inducing DNA elements. We mention implications for agriculture.