Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes

Choi, K., Reinhard, C., Serra, H., Ziolkowski, P. A., Underwood, C. J., Zhao, X., Hardcastle, T. J., Yelina, N. E., Griffin, C., Jackson, M., Mezard, C., McVean, G., Copenhaver, G. P., Henderson, I. R. (July 2016) Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes. PLoS Genet, 12 (7). e1006179. ISSN 1553-7404 (Electronic)1553-7390 (Linking)

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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.

Item Type: Paper
Subjects: organism description > plant > Arabidopsis
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification
bioinformatics > genomics and proteomics
bioinformatics > genomics and proteomics > genetics & nucleic acid processing > DNA, RNA structure, function, modification > recombination
CSHL Authors:
Communities: CSHL labs > Martienssen lab
School of Biological Sciences > Publications
Depositing User: Matt Covey
Date: 14 July 2016
Date Deposited: 22 Jul 2016 19:47
Last Modified: 07 Oct 2016 15:41
PMCID: PMC4945094
Related URLs:
URI: https://repository.cshl.edu/id/eprint/32969

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