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 (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.

Genome‐wide analysis of MIKC‐type MADS‐box genes in wheat: pervasive duplications, functional conservation and putative neofunctionalization

“…Together, this might indicate more frequent tandem duplication events in distal telomeric segments. These findings are in line with the observation that subtelomeric segments are targets of recombination events and that many fast‐evolving genes lie within these segments (Glover et al ., ; Chen et al ., ; Ramírez‐González et al ., ).…”

“…The cause of the expansion of the FLC-, AGL17-SEP1-OsMADS30-like subfamilies might be the chromosomal position of their genes. Distal telomeric segments have previously been described as targets of recombination events, and many fastevolving genes lie within these evolutionary hotspots (Glover et al, 2015;Chen et al, 2018). In wheat specifically, genes related to stress response and external stimuli, notably traits with a high requirement for adaptability, have been found to be located in distal chromosomal segments (IWGSC, 2018;Ram ırez-Gonz alez et al, 2018).…”

Comprehensive Analysis of Human Subtelomeres by Whole Genome Mapping

“…Subtelomeric segmental duplications (often referred to as subtelomeric repeats) are an almost universal feature of eukaryotic genomes and, like in humans, are highly variable and nearly impossible to assemble with current sequencing methods. In addition, the expansion and rapid evolution of functional gene families associated with subtelomeres has been noted in a very wide range of species, from yeasts and protozoans to complex plants and animals [14,[44][45][46]. Application of this methodology could be used to efficiently map large-scale subtelomeric structural variation in any eukaryote to enable completion of accurate subtelomeric assemblies and analysis of embedded gene families.…”

Common bean resistance to Xanthomonas is associated with upregulation of the salicylic acid pathway and downregulation of photosynthesis

“…The genes involved in these pathways were scattered throughout the whole common bean genome, which reflects the complexity of CBB resistance. In particular, large clusters of dozens of NLR genes exist at common bean subtelomeres [101][102][103][104] but the 34 NLR repressed in JaloEEP558 following X. phaseoli pv. phaseoli infection did not correspond to the specific repression of one of these clusters.…”