Common Bean Subtelomeres Are Hot Spots of Recombination and Favor Resistance Gene Evolution

Abstract

Subtelomeres of most eukaryotes contain fast-evolving genes usually involved in adaptive processes. In common bean (<i>Phaseolus vulgaris</i>), the <i>Co-2</i> anthracnose resistance (<i>R</i>) locus corresponds to a cluster of nucleotide-binding-site leucine-rich-repeat (NL) encoding sequences, the prevalent class of plant <i>R</i> genes. To study the recent evolution of this <i>R</i> gene cluster, we used a combination of sequence, genetic and cytogenetic comparative analyses between common bean genotypes from two distinct gene pools (Andean and Mesoamerican) that diverged 0.165 million years ago. <i>Co-2</i> is a large subtelomeric cluster on chromosome 11 comprising from 32 (Mesoamerican) to 52 (Andean) NL sequences embedded within <i>khipu</i> satellite repeats. Since the recent split between Andean and Mesoamerican gene pools, the <i>Co-2</i> cluster has experienced numerous gene-pool specific NL losses, leading to distinct NL repertoires. The high proportion of solo-LTR retrotransposons indicates that the <i>Co-2</i> cluster is located in a hot spot of unequal intra-strand homologous recombination. Furthermore, we observe large segmental duplications involving both Non-Homologous End Joining and Homologous Recombination double-strand break repair pathways. Finally, the identification of a Mesoamerican-specific subtelomeric sequence reveals frequent interchromosomal recombinations between common bean subtelomeres. Altogether, our results highlight that common bean subtelomeres are hot spots of recombination and favor the rapid evolution of <i>R</i> genes. We propose that chromosome ends could act as <i>R</i> gene incubators in many plant genomes.