Abstract
Subtelomeres of most eukaryotes contain fast-evolving genes usually involved in adaptive processes. In common bean (Phaseolus vulgaris), the Co-2 anthracnose resistance (R) locus corresponds to a cluster of nucleotide-binding-site leucine-rich-repeat (NL) encoding sequences, the prevalent class of plant R genes. To study the recent evolution of this R 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. Co-2 is a large subtelomeric cluster on chromosome 11 comprising from 32 (Mesoamerican) to 52 (Andean) NL sequences embedded within khipu satellite repeats. Since the recent split between Andean and Mesoamerican gene pools, the Co-2 cluster has experienced numerous gene-pool specific NL losses, leading to distinct NL repertoires. The high proportion of solo-LTR retrotransposons indicates that the Co-2 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 R genes. We propose that chromosome ends could act as R gene incubators in many plant genomes.
Highlights
Plant immunity is activated after direct or indirect perception of pathogen molecules by resistance (R) genes (Jones and Dangl, 2006; Kourelis and van der Hoorn, 2018)
In order to study the evolution of the Co-2 R-gene cluster since the divergence between Andean and Mesoamerican gene pools, we selected and sequenced nine Bacterial Artificial Chromosome (BAC) from a Mesoamerican common bean genotype (BAT93), leading to 1.07 Mb organized in four contigs (PvM11A to PvM11D, Figure 1B)
PCR-based mapping confirms that macrosynteny between G19833 and BAT93 contigs is consistent with microsynteny (Figures 1B,C)
Summary
Plant immunity is activated after direct or indirect perception of pathogen molecules by resistance (R) genes (Jones and Dangl, 2006; Kourelis and van der Hoorn, 2018). Genes encoding CC-NB-LRR (CNL) and TIR-NB-LRR (TNL) proteins correspond to two ancient lineages (Bai et al, 2002; Meyers et al, 2003; Ameline-Torregrosa et al, 2008) and are often organized in clusters of two to dozens of copies evolving at different rates (Kuang, 2004; Smith et al, 2004; Bresson et al, 2011; Ratnaparkhe et al, 2011; Luo et al, 2012; Baggs et al, 2017). Clustering of duplicated R genes, as observed in numerous plant species (Pryor and Ellis, 1993; Crute and Pink, 1996), has been suggested to favor R gene evolution against an ever changing array of pathogens (Hulbert et al, 2001). Little is known about the dynamics of R gene clusters on a short (infra-species) time scale (Kuang, 2004; Zhou et al, 2007)
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