Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes

Autor: Choi, Kyuha, Reinhard, Carsten, Serra, Heïdi, Ziolkowski, Piotr A, Underwood, Charles J, Zhao, Xiaohui, Hardcastle, Thomas J, Yelina, Nataliya E, Griffin, Catherine, Jackson, Matthew, Mézard, Christine, McVean, Gil, Copenhaver, Gregory P, Henderson, Ian R
Přispěvatelé: Department of Plant Sciences, University of Cambridge [UK] (CAM), Adam Mickiewicz University in Poznań (UAM), Cold Spring Harbor Laboratory (CSHL), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Centre National de la Recherche Scientifique (CNRS), The Wellcome Trust Centre for Human Genetics [Oxford], University of Oxford [Oxford], University of North Carolina, Royal Society, Gatsby Charitable Foundation [2962], BBSRC [BB/N007557/1], National Natural Science Foundation of China [61403318], EMBO [ALTF 807-2009], Polish Mobility Plus Fellowship [605/MOB/2011/0], National Science Foundation [MCB-1121563], Underwood, Charles J [0000-0001-5730-6279], Zhao, Xiaohui [0000-0001-9922-2815], Hardcastle, Thomas J [0000-0002-9328-5011], Griffin, Catherine [0000-0001-8862-1386], Copenhaver, Gregory P [0000-0002-7962-3862], Apollo - University of Cambridge Repository
Jazyk: angličtina
Rok vydání: 2016
Předmět:
nbs-lrr protein
genome sequence
[SDV]Life Sciences [q-bio]
Arabidopsis
rust resistance
Artificial Gene Amplification and Extension
Plant Science
Plant Genetics
Biochemistry
Polymerase Chain Reaction
Linkage Disequilibrium
plant immune receptor
[SDV.IDA]Life Sciences [q-bio]/Food engineering
Plant Genomics
downy mildew resistance
Disease Resistance
Recombination
Genetic
meiotic recombination
Plant Anatomy
Nucleic Acid Hybridization
food and beverages
Genomics
Plants
major histocompatibility complex
Nucleic acids
Meiosis
Multigene Family
Pollen
Sequence Analysis
Research Article
Biotechnology
Heterozygote
Genotyping
lcsh:QH426-470
DNA recombination
Arabidopsis Thaliana
crossover hot-spots
chemical and pharmacologic phenomena
Brassica
Genes
Plant
Research and Analysis Methods
Model Organisms
Plant and Algal Models
Sequence Motif Analysis
transcription factors
Genetics
[SDV.BV]Life Sciences [q-bio]/Vegetal Biology
[SPI.GPROC]Engineering Sciences [physics]/Chemical and Process Engineering
Molecular Biology Techniques
Sequencing Techniques
Molecular Biology
Alleles
Crosses
Genetic
Plant Diseases
Arabidopsis Proteins
Gene Mapping
fungi
Organisms
Genetic Variation
Biology and Life Sciences
DNA
lcsh:Genetics
evolutionary dynamics
Plant Biotechnology
Zdroj: PLoS Genetics
PLoS Genetics, Public Library of Science, 2016, 12 (7), pp.1-30. ⟨10.1371/journal.pgen.1006179⟩
PLoS Genetics, Vol 12, Iss 7, p e1006179 (2016)
ISSN: 1553-7390
1553-7404
DOI: 10.1371/journal.pgen.1006179⟩
Popis: 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.
Author Summary The majority of plants, animals and fungi reproduce sexually, which has a profound effect on patterns of genetic diversity. For sexual reproduction to occur a specialized cell division called meiosis generates gametes (sex cells) with recombined DNA. During meiosis homologous chromosomes undergo reciprocal exchange of genetic material called crossover, which mixes parental sequences. Crossover frequency is highly variable along chromosomes and is typically concentrated in narrow regions called hotspots. Sexual reproduction is proposed to provide a major advantage during host-pathogen coevolution. This theory predicts that crossover hotspots will be associated with genes that play important roles in the immune system, where diversity may be beneficial. To investigate this idea we mapped patterns of crossover frequency in relation to genes that plants use to recognize pathogens. We observe that a subset of Arabidopsis thaliana resistance genes overlap with strong crossover hotspots. However, we also observe resistance gene coldspots, which correlate with chromosomal rearrangements between varietal lines (ecotypes). Using Arabidopsis ecotypes we also show that natural genetic variation has a strong modifying effect on resistance gene cluster recombination rates. Together our work shows complex variation in resistance gene crossover patterns, which may relate to heterogeneity in coevolutionary pressures experienced at different loci, in addition to the effects of structural genetic diversity.
Databáze: OpenAIRE
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