FANCM Limits Meiotic Crossovers in Brassica Crops

Blary, Aurélien; Gonzalo, Adrián; Eber, Frédérique; Berard, Aurélie; Bergès, Hélène; Bessoltane, Nadia; Charif, Delphine; Charpentier, Catherine; Cromer, Laurence; Fourment, Joëlle; Genevriez, Camille; Paslier, Marie‐Christine Le; Lodé, Maryse; Lucas, Marie‐Odile; Nési, Nathalie; Lloyd, A. B.; Chèvre, Anne‐Marie; Jenczewski, Eric

doi:10.3389/fpls.2018.00368

Cited by 46 publications

(35 citation statements)

References 70 publications

(102 reference statements)

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“…In comparison with Arabidopsis , crop species have been largely disregarded. So far, knockout of FANCM or RECQ4 orthologs have been tested in the rapeseed, rice, pea and tomato with contrasting results (Blary et al ., ; Mieulet et al ., ). For instance, a mutation of FANCM in Brassica napus leads to a 1.3‐fold increase versus threefold in Arabidopsis and B. rapa (Blary et al ., ), although the B. napus mutation is not necessarily null and showed a limited effect in intraspecific hybrids compared to pure lines (Fernandes et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…So far, knockout of FANCM or RECQ4 orthologs have been tested in the rapeseed, rice, pea and tomato with contrasting results (Blary et al ., ; Mieulet et al ., ). For instance, a mutation of FANCM in Brassica napus leads to a 1.3‐fold increase versus threefold in Arabidopsis and B. rapa (Blary et al ., ), although the B. napus mutation is not necessarily null and showed a limited effect in intraspecific hybrids compared to pure lines (Fernandes et al ., ). On the other hand, the single recq4 mutation increases crossovers approximately threefold in all crops tested (Mieulet et al ., ), suggesting that manipulating RECQ4 may be a universal tool for increasing recombination in plants.…”

Section: Introductionmentioning

confidence: 97%

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CRISPR/Cas inactivation of RECQ4 increases homeologous crossovers in an interspecific tomato hybrid

Maagd

Loonen

Chouaref

et al. 2019

Plant Biotechnology Journal

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Summary Crossover formation during meiosis in plants is required for proper chromosome segregation and is essential for crop breeding as it allows an (optimal) combination of traits by mixing parental alleles on each chromosome. Crossover formation commences with the production of a large number of DNA double‐strand breaks, of which only a few result in crossovers. A small number of genes, which drive the resolution of DNA crossover intermediate structures towards non‐crossovers, have been identified in Arabidopisis thaliana. In order to explore the potential of modification of these genes in interspecific hybrids between crops and their wild relatives towards increased production of crossovers, we have used CRISPR/Cas9‐mutagenesis in an interspecific tomato hybrid to knockout RecQ4. A biallelic recq4 mutant was obtained in the F1 hybrid of Solanum lycopersicum and S. pimpinellifolium. Compared with the wild‐type F1 hybrid, the F1 recq4 mutant was shown to have a significant increase in crossovers: a 1.53‐fold increase when directly observing ring bivalents in male meiocytes microscopically and a 1.8‐fold extension of the genetic map when measured by analysing SNP markers in the progeny (F2) plants. This is one of the first demonstrations of increasing crossover frequency in interspecific hybrids by manipulating genes in crossover intermediate resolution pathways and the first to do so by directed mutagenesis. Significance statement Increasing crossover frequency during meiosis can speed up or simplify crop breeding that relies on meiotic crossovers to introduce favourable alleles controlling important traits from wild relatives into crops. Here we show for the first time that knocking out an inhibitor of crossovers in an interspecific hybrid between tomato and its relative wild species using CRISPR/Cas9‐mutagenesis results in increased recombination between the two genomes.

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Section: Introductionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

CRISPR/Cas inactivation of RECQ4 increases homeologous crossovers in an interspecific tomato hybrid

Maagd

Loonen

Chouaref

et al. 2019

Plant Biotechnology Journal

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“…Mutation of this gene also leads to a large increase in recombination, but only in pure lines (~3-fold) with a very limited effect in hybrids 2,3,5,13 . FANCM was also shown to limit crossovers in a Brassica rapa pure line 14 . The third pathway depends on the AAA-ATPase FIGL1.…”

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confidence: 95%

Unleashing meiotic crossovers in crops

Mieulet

Aubert

Brès

et al. 2018

Preprint

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“…Duplicate gene loss may occur via deletion of the (entire or partial) sequence of one duplicate, a process that is still difficult to repeat experimentally, and/or through accumulation of loss-offunction mutations 3 . In this study, we searched for mutations in BnaA.MSH4 and BnaC.MSH4 across 500 M2 plants from the EMS mutagenized RAPTILL population (described in 35 ). Using separate screens for the two genes, we identified 44 and 43-point mutation alleles within 1 kb of the MutSac domain of BnaA.MSH4 and BnaC.MSH4, respectively (Supplementary Figure 2).…”

Section: Tilling Enables Production Of Msh4 Mutants In Allotetraploidmentioning

confidence: 99%

“…Brassica napus L. cv. Tanto is a double-low spring cultivar obtained at INRA Rennes (France) that was used to develop the RAPTILL EMS population 35 in which we looked for mutations in BnaA.MSH4 and BnaC.MSH4. Microspore culture was performed to isolate allohaploid plants following the protocol described in 61 .…”

Section: Plant Materialsmentioning

confidence: 99%

Meiotic effects ofMSH4copy number variation support an adaptive role for post-polyploidy gene loss

Gonzalo

Lucas

et al. 2018

Preprint

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Many eukaryotes descend from polyploid ancestors that experienced massive duplicate gene loss. This genomic erosion is particularly strong for duplicated (meiotic) recombination genes that return to a single copy more rapidly than genome average following polyploidy. To better understand the evolutionary forces underlying duplicate loss, we analysed how varying copy numbers of MSH4, an essential meiotic recombination gene, influences crossover formation in allotetraploid Brassica napus. We show that faithful chromosome segregation and crossover frequencies between homologous chromosomes are unchanged with MSH4 duplicate loss; by contrast, crossovers between homoeologous chromosomes (which result in genomic rearrangements) decrease with reductions in MSH4 copy number. We also found that inter-homoeologue crossovers originate almost exclusively from the MSH4-dependent crossover pathway. Limiting the efficiency of this pathway by decreasing the copy number of key meiotic recombination genes could therefore contribute to adaptation to polyploidy, by promoting regular chromosome segregation and genomic stability. TextGene duplication and gene loss are two driving forces in evolution 1-3 . These two mechanisms are well illustrated by the evolution of the meiotic recombination machinery. At the outset, the emergence of meiosis required key evolutionary breakthroughs 4-6 that were all made possible through iterative gene duplications followed by acquisition of new functions. These include, among others, the formation of programmed DNA double-strand breaks by SPO11 proteins 7 , the promotion of double-strand break repair using homologous templates by DMC1, RAD51 and some other related proteins 8 or the resolution of recombination intermediates as crossovers by MSH and MLH proteins 9 . After this initial phase, genes involved in meiotic recombination (and DNA repair in general) have tended to return preferentially to single copy following subsequent duplications 10,11 , with some

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FANCM Limits Meiotic Crossovers in Brassica Crops

Cited by 46 publications

References 70 publications

CRISPR/Cas inactivation of RECQ4 increases homeologous crossovers in an interspecific tomato hybrid

CRISPR/Cas inactivation of RECQ4 increases homeologous crossovers in an interspecific tomato hybrid

Unleashing meiotic crossovers in crops

Meiotic effects ofMSH4copy number variation support an adaptive role for post-polyploidy gene loss

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