Abstract
Meiotic crossover frequency varies extensively along chromosomes and is typically concentrated in hotspots. As recombination increases genetic diversity, hotspots are predicted to occur at immunity genes, where variation may be beneficial. A major component of plant immunity is recognition of pathogen Avirulence (Avr) effectors by resistance (R) genes that encode NBS-LRR domain proteins. Therefore, we sought to test whether NBS-LRR genes would overlap with meiotic crossover hotspots using experimental genetics in Arabidopsis thaliana. NBS-LRR genes tend to physically cluster in plant genomes; for example, in Arabidopsis most are located in large clusters on the south arms of chromosomes 1 and 5. We experimentally mapped 1,439 crossovers within these clusters and observed NBS-LRR gene associated hotspots, which were also detected as historical hotspots via analysis of linkage disequilibrium. However, we also observed NBS-LRR gene coldspots, which in some cases correlate with structural heterozygosity. To study recombination at the fine-scale we used high-throughput sequencing to analyze ~1,000 crossovers within the RESISTANCE TO ALBUGO CANDIDA1 (RAC1) R gene hotspot. This revealed elevated intragenic crossovers, overlapping nucleosome-occupied exons that encode the TIR, NBS and LRR domains. The highest RAC1 recombination frequency was promoter-proximal and overlapped CTT-repeat DNA sequence motifs, which have previously been associated with plant crossover hotspots. Additionally, we show a significant influence of natural genetic variation on NBS-LRR cluster recombination rates, using crosses between Arabidopsis ecotypes. In conclusion, we show that a subset of NBS-LRR genes are strong hotspots, whereas others are coldspots. This reveals a complex recombination landscape in Arabidopsis NBS-LRR genes, which we propose results from varying coevolutionary pressures exerted by host-pathogen relationships, and is influenced by structural heterozygosity.
Highlights
During meiosis, homologous chromosomes recombine via reciprocal exchanges of DNA, called crossovers [1,2]
The majority of plants, animals and fungi reproduce sexually, which has a profound effect on patterns of genetic diversity
Using Arabidopsis ecotypes we show that natural genetic variation has a strong modifying effect on resistance gene cluster recombination rates
Summary
Homologous chromosomes recombine via reciprocal exchanges of DNA, called crossovers [1,2]. The “two-speed” genome hypothesis proposes that crossover hotspots will be differentially distributed among immunity versus housekeeping genes, as the former participate directly in hostpathogen coevolution, where recombination and diversity may be beneficial [8,9,10,11,12]. We investigate this hypothesis by experimentally mapping patterns of meiotic crossover recombination in relation to Arabidopsis NBS-LRR disease resistance genes
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