Recombination Rate Heterogeneity within Arabidopsis Disease Resistance Genes

Choi, Kyuha; Reinhard, Carsten; Serra, Heïdi; Ziolkowski, Piotr A; Underwood, Charles J; Zhao, Xiaohui; Hardcastle, Thomas J.; Yelina, Nataliya E.; Griffin, Catherine; Jackson, Matthew A.; Mézard, Christine; McVean, Gil; Copenhaver, Gregory P.; Henderson, Ian

doi:10.1371/journal.pgen.1006179

Cited by 88 publications

(127 citation statements)

References 134 publications

(266 reference statements)

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“…6A; Supplemental Table S25; Choi et al 2016). The HEI10 Col population contained more than double the number of wild-type Table S1), consistent with our MLH1 focus analysis (Fig.…”

Section: Hei10supporting

confidence: 80%

“…Crossover frequency was measured using fluorescent reporters in seeds (Col-420) and pollen (Col-I2f) (Emmanuel et al 2006; One-hundred-ninety-two individuals were analyzed from wild-type (Choi et al 2016) and HEI10 Col F 2 (Col/Ler) populations. The number of crossovers per F 2 and in total are listed for each chromosome and the whole genome.…”

Section: Arabidopsis Strainsmentioning

confidence: 99%

“…FastQ sequencing data files are available from ArrayExpress accessions E-MTAB-4657 (wild type) (Choi et al 2016) and E-MTAB-4967 (HEI10). Sequencing data were analyzed to identify crossovers as reported previously using the TIGER pipeline (Rowan et al 2015;Yelina et al 2015;Choi et al 2016). Crossovers were tallied in 10-kb windows and plotted along chromosomes after smoothing using the R function "filter."…”

Section: Mapping Crossovers Via Genotyping By Sequencingmentioning

confidence: 99%

“…Immunostaining of Arabidopsis meiocytes for DMC1, RAD51, or the DSB-associated histone variant γH2A.X has revealed ∼100-200 foci distributed along the paired homologous chromosomes at the leptotene stage (Girard et al 2015;Yelina et al 2015). Approximately 10 of these initiating meiotic DSBs mature into crossovers per Arabidopsis meiosis (Giraut et al 2011;Salomé et al 2012;Rowan et al 2015;Choi et al 2016).…”

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confidence: 99%

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Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination

et al. 2017

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During meiosis, homologous chromosomes undergo crossover recombination, which creates genetic diversity and balances homolog segregation. Despite these critical functions, crossover frequency varies extensively within and between species. Although natural crossover recombination modifier loci have been detected in plants, causal genes have remained elusive. Using natural Arabidopsis thaliana accessions, we identified two major recombination quantitative trait loci (rQTLs) that explain 56.9% of crossover variation in Col×Ler F 2 populations. We mapped rQTL1 to semidominant polymorphisms in HEI10, which encodes a conserved ubiquitin E3 ligase that regulates crossovers. Null hei10 mutants are haploinsufficient, and, using genome-wide mapping and immunocytology, we show that transformation of additional HEI10 copies is sufficient to more than double euchromatic crossovers. However, heterochromatic centromeres remained recombination-suppressed. The strongest HEI10-mediated crossover increases occur in subtelomeric euchromatin, which is reminiscent of sex differences in Arabidopsis recombination. Our work reveals that HEI10 naturally limits Arabidopsis crossovers and has the potential to influence the response to selection.

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“…6A; Supplemental Table S25; Choi et al 2016). The HEI10 Col population contained more than double the number of wild-type Table S1), consistent with our MLH1 focus analysis (Fig.…”

Section: Hei10supporting

confidence: 80%

Section: Arabidopsis Strainsmentioning

confidence: 99%

Section: Mapping Crossovers Via Genotyping By Sequencingmentioning

confidence: 99%

mentioning

confidence: 99%

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Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination

et al. 2017

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“…Previous studies in Arabidopsis, Drosophila, and dogs discovered recombination-associated motifs like A-stretch motif, CCT, CCN repeats, and CpG (Comeron et al 2012;Auton et al 2013;Wijnker et al 2013;Shilo et al 2015;Choi et al 2016). To evaluate the existence of recombinationassociated motifs in wheat, we searched for DNA motifs overrepresented in Rec intervals without a priori using MEME Suite and the base frequency of the chromosome (see Materials and Methods for details).…”

Section: Recombinogenic Regions Have Different Composition In Tes Andmentioning

confidence: 99%

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

et al. 2017

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During meiosis, crossovers (COs) create new allele associations by reciprocal exchange of DNA. In bread wheat (Triticum aestivum L.), COs are mostly limited to subtelomeric regions of chromosomes, resulting in a substantial loss of breeding efficiency in the proximal regions, though these regions carry 60-70% of the genes. Identifying sequence and/or chromosome features affecting recombination occurrence is thus relevant to improve and drive recombination. Using the recent release of a reference sequence of chromosome 3B and of the draft assemblies of the 20 other wheat chromosomes, we performed fine-scale mapping of COs and revealed that 82% of COs located in the distal ends of chromosome 3B representing 19% of the chromosome length. We used 774 SNPs to genotype 180 varieties representative of the Asian and European genetic pools and a segregating population of 1270 F 6 lines. We observed a common location for ancestral COs (predicted through linkage disequilibrium) and the COs derived from the segregating population. We delineated 73 small intervals (,26 kb) on chromosome 3B that contained 252 COs. We observed a significant association of COs with genic features (73 and 54% in recombinant and nonrecombinant intervals, respectively) and with those expressed during meiosis (67% in recombinant intervals and 48% in nonrecombinant intervals). Moreover, while the recombinant intervals contained similar amounts of retrotransposons and DNA transposons (42 and 53%), nonrecombinant intervals had a higher level of retrotransposons (63%) and lower levels of DNA transposons (28%). Consistent with this, we observed a higher frequency of a DNA motif specific to the TIR-Mariner DNA transposon in recombinant intervals. KEYWORDS recombination; meiosis; bread wheat; linkage disequilibrium; transposon; hotspot; sequence motif M EIOTIC recombination is a process that allows reshuffling of diversity by the reciprocal exchange of DNA called a crossover (CO). This phenomenon is conserved in most eukaryotes (for a review see Mercier et al. 2015) and follows the formation of a double-strand break (DSB) of DNA generated by the topoisomerase SPO11 complex. However, the number of DSBs is at least 10-to 50-fold greater than the number of COs which rarely exceeds three per bivalent chromosome per meiosis (Mercier et al. 2015). This paucity of COs per meiosis with regards to the number of DSBs suggests the existence of a tight control and regulation of recombination in plants that promote DSB repair in a manner that does not lead to COs. For example, the study of the two helicases AtFANCM and RECQ4 (AtRECQ4A and AtRECQ4B) (Crismani et al. 2012;Knoll et al. 2012;Girard et al. 2014;Séguéla-Arnaud et al. 2015) revealed three-and sixfold CO frequency increases in the Atfancm single mutant and the Atrecq4a/Atrecq4b double mutant, respectively, compared to the wild type. These increases result from additional COs from the class-II pathway which suggests that FANCM and RECQ4 prevent CO formation and direct recombination intermediates towar...

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