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Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes.

Published version
Peer-reviewed

Type

Article

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Authors

Choi, Kyuha 
Reinhard, Carsten 
Serra, Heïdi 
Ziolkowski, Piotr A 
Underwood, Charles J  ORCID logo  https://orcid.org/0000-0001-5730-6279

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.

Description

Keywords

Alleles, Arabidopsis, Arabidopsis Proteins, Crosses, Genetic, Disease Resistance, Genes, Plant, Genetic Variation, Heterozygote, Linkage Disequilibrium, Meiosis, Multigene Family, Nucleic Acid Hybridization, Plant Diseases, Pollen, Recombination, Genetic

Journal Title

PLoS Genet

Conference Name

Journal ISSN

1553-7390
1553-7404

Volume Title

12

Publisher

Public Library of Science (PLoS)
Sponsorship
Biotechnology and Biological Sciences Research Council (BB/N007557/1)
Biotechnology and Biological Sciences Research Council (BB/K007882/1)
Biotechnology and Biological Sciences Research Council (BB/L006847/1)
Biotechnology and Biological Sciences Research Council (BB/M004937/1)
Research in the Henderson laboratory was supported by a Royal Society University Research Fellowship, Gatsby Charitable Foundation grant 2962, BBSRC grant BB/N007557/1 and National Natural Science Foundation of China grant 61403318. KC was funded by an EMBO long term postdoctoral fellowship ALTF 807-2009. PAZ was supported by a Polish Mobility Plus Fellowship 605/MOB/2011/0. GPC is funded by a National Science Foundation Grant (MCB-1121563). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.