Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis

During meiosis, homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double-strand breaks (DSBs), which are processed into single-stranded DNA that can invade a homologous chromosome....

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Published in:Proceedings of the National Academy of Sciences - PNAS 2018-03, Vol.115 (10), p.2437-2442
Main Authors: Serra, Heïdi, Lambing, Christophe, Griffin, Catherine H., Topp, Stephanie D., Nageswaran, Divyashree C., Underwood, Charles J., Ziolkowski, Piotr A., Séguéla-Arnaud, Mathilde, Fernandes, Joiselle B., Mercier, Raphaël, Henderson, Ian R.
Format: Article
Language:English
Subjects:
Arabidopsis
Biological Sciences
Cell division
Centromeres
Chromosomes
Crop improvement
Crossovers
Deoxyribonucleic acid
DNA
DNA damage
DNA helicase
Dosage
Genes
Genetic diversity
Genomes
Heterochromatin
Homology
Life Sciences
Meiosis
Mutation
Polymorphism
Recombination
Repair
Single-stranded DNA
Ubiquitin-protein ligase
Vegetal Biology
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creator Serra, Heïdi
Lambing, Christophe
Griffin, Catherine H.
Topp, Stephanie D.
Nageswaran, Divyashree C.
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Ziolkowski, Piotr A.
Séguéla-Arnaud, Mathilde
Fernandes, Joiselle B.
Mercier, Raphaël
Henderson, Ian R.
description During meiosis, homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double-strand breaks (DSBs), which are processed into single-stranded DNA that can invade a homologous chromosome. The resulting joint molecules can ultimately be resolved as crossovers. In Arabidopsis, competing pathways balance the repair of ∼100–200 meiotic DSBs into ∼10 crossovers per meiosis, with the excess DSBs repaired as noncrossovers. To bias DSB repair toward crossovers, we simultaneously increased dosage of the procrossover E3 ligase gene HEI10 and introduced mutations in the anticrossovers helicase genes RECQ4A and RECQ4B. As HEI10 and recq4a recq4b increase interfering and noninterfering crossover pathways, respectively, they combine additively to yield a massive meiotic recombination increase. Interestingly, we also show that increased HEI10 dosage increases crossover coincidence, which indicates an effect on interference. We also show that patterns of interhomolog polymorphism and heterochromatin drive recombination increases distally towards the subtelomeres in both HEI10 and recq4a recq4b backgrounds, while the centromeres remain crossover suppressed. These results provide a genetic framework for engineering meiotic recombination landscapes in plant genomes.
doi_str_mv 10.1073/pnas.1713071115
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Scott Hawley, Stowers Institute for Medical Research, Kansas City, MO, and approved January 26, 2018 (received for review July 24, 2017)</notes><notes>Author contributions: H.S., C.L., C.H.G., D.C.N., R.M., and I.R.H. designed research; H.S., C.L., C.H.G., S.D.T., and D.C.N. performed research; C.J.U., P.A.Z., M.S.-A., and J.B.F. contributed new reagents/analytic tools; H.S., C.L., C.H.G., S.D.T., D.C.N., and I.R.H. analyzed data; and H.S., C.L., C.H.G., R.M., and I.R.H. wrote the paper.</notes><notes>2Present address: Department of Genome Biology, Adam Mickiewicz University in Poznan, 61-614 Poznan, Poland.</notes><notes>1Present address: Vegetable Crop Research, KeyGene, 6708 PW Wageningen, The Netherlands.</notes><abstract>During meiosis, homologous chromosomes undergo reciprocal crossovers, which generate genetic diversity and underpin classical crop improvement. Meiotic recombination initiates from DNA double-strand breaks (DSBs), which are processed into single-stranded DNA that can invade a homologous chromosome. The resulting joint molecules can ultimately be resolved as crossovers. In Arabidopsis, competing pathways balance the repair of ∼100–200 meiotic DSBs into ∼10 crossovers per meiosis, with the excess DSBs repaired as noncrossovers. To bias DSB repair toward crossovers, we simultaneously increased dosage of the procrossover E3 ligase gene HEI10 and introduced mutations in the anticrossovers helicase genes RECQ4A and RECQ4B. As HEI10 and recq4a recq4b increase interfering and noninterfering crossover pathways, respectively, they combine additively to yield a massive meiotic recombination increase. Interestingly, we also show that increased HEI10 dosage increases crossover coincidence, which indicates an effect on interference. 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subjects Arabidopsis
Biological Sciences
Cell division
Centromeres
Chromosomes
Crop improvement
Crossovers
Deoxyribonucleic acid
DNA
DNA damage
DNA helicase
Dosage
Genes
Genetic diversity
Genomes
Heterochromatin
Homology
Life Sciences
Meiosis
Mutation
Polymorphism
Recombination
Repair
Single-stranded DNA
Ubiquitin-protein ligase
Vegetal Biology
title Massive crossover elevation via combination of HEI10 and recq4a recq4b during Arabidopsis meiosis
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