Do duplication-inducing elements "cooperate" with genes in evolutionary arms races? : A case study on cereal crop pathogenesis

Abstract

Background

Crop improvement depends on the human ability to harness naturally- or artificially-occurring gene variants. Genomic segmental duplication can create redundant gene copies that can more freely ‘explore’ the space of possible mutations without adverse selective consequences. Such efficient generation of genetic diversity can be especially beneficial for organisms involved in evolutionary arms races such as the conflict between pathogens and their hosts. Given that some genomic regions are more prone to spontaneously duplicate themselves than others, we hypothesised that lineages in which arms-race-implicated genes fall within duplication-prone regions might enjoy a selective advantage, resulting in a measurable statistical association between the two. Results

We subjected the exceptionally repetitive and high-quality barley (Hordeum vulgare L.) genome assembly to a novel analysis to explicitly test, and confirm, that natural selection must have favoured lineages in which arms-race genes—in particular pathogen defence genes—are associated with duplication-inducers, most notably Kb-scale tandem repeats. Moreover, many well-studied pathogen resistance gene families such as NBS-LRRs and RLKs are independently identifiable by their associations with self-duplicating DNA. Such duplication-prone regions show a history of repeated long-distance ‘dispersal’ to distant genomic sites, followed by local expansion by tandem duplication. Often, the long tandemly duplicated motif differs between sites suggesting they arise often. Conclusions

The data support the view that genes in arms races have sometimes formed effectively cooperative associations with duplication-inducing sequences, supporting the view that some tolerance of genome-expanding genetic elements can be an evolutionarily advantageous strategy at the lineage level. Heavily duplicated genes are therefore more likely to be involved in arms races (such as pathogen defence) and hence may make suitable targets for crop improvement via targeted breeding or genome editing—as might the diversity-generating sequences they associate with.