Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes

被引:60
作者
Choi, Kyuha [1 ]
Reinhard, Carsten [1 ]
Serra, Heidi [1 ]
Ziolkowski, Piotr A. [1 ,2 ]
Underwood, Charles J. [1 ,3 ]
Zhao, Xiaohui [1 ]
Hardcastle, Thomas J. [1 ]
Yelina, Nataliya E. [1 ]
Griffin, Catherine [1 ]
Jackson, Matthew [1 ]
Mezard, Christine [4 ]
McVean, Gil [5 ]
Copenhaver, Gregory P. [6 ,7 ,8 ]
Henderson, Ian R. [1 ]
机构
[1] Univ Cambridge, Dept Plant Sci, Downing St, Cambridge, England
[2] Adam Mickiewicz Univ, Dept Biotechnol, Poznan, Poland
[3] Cold Spring Harbor Lab, Watson Sch Biol Sci, POB 100, Cold Spring Harbor, NY 11724 USA
[4] Univ Paris Saclay, Inst Jean Pierre Bourgin, INRA, AgroParisTech,CNRS, RD10, Versailles, France
[5] Univ Oxford, Wellcome Trust Ctr Human Genet, Oxford, England
[6] Univ N Carolina, Dept Biol, Chapel Hill, NC USA
[7] Univ N Carolina, Integrat Program Biol & Genome Sci, Chapel Hill, NC USA
[8] Univ N Carolina, Lineberger Comprehens Canc Ctr, Sch Med, Chapel Hill, NC 27599 USA
基金
美国国家科学基金会; 英国生物技术与生命科学研究理事会; 中国国家自然科学基金;
关键词
DOWNY MILDEW RESISTANCE; CROSSOVER HOT-SPOTS; NBS-LRR PROTEIN; MEIOTIC RECOMBINATION; RUST RESISTANCE; EVOLUTIONARY DYNAMICS; BALANCING SELECTION; ANTIGENIC VARIATION; REVERSE GENETICS; GENOME SEQUENCE;
D O I
10.1371/journal.pgen.1006179
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
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 similar to 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.
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页数:30
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