Natural variation identifies SNI1, the SMC5/6 component, as a modifier of meiotic crossover in Arabidopsis

The frequency and distribution of meiotic crossovers are tightly controlled; however, variation in this process can be observed both within and between species. Using crosses of two natural Arabidopsis thaliana accessions, Col and Ler, we mapped a crossover modifier locus to semidominant polymorphisms in SUPPRESSOR OF NPR1-1 INDUCIBLE 1 (SNI1), which encodes a component of the SMC5/6 complex. The sni1 mutant exhibits a modified pattern of recombination across the genome with crossovers elevated in chromosome distal regions but reduced in pericentromeres. Mutations in SNI1 result in reduced crossover interference and can partially restore the fertility of a Class I crossover pathway mutant, which suggests that the protein affects noninterfering crossover repair. Therefore, we tested genetic interactions between SNI1 and both RECQ4 and FANCM DNA helicases, which showed that additional Class II crossovers observed in the sni1 mutant are FANCM independent. Furthermore, genetic analysis of other SMC5/6 mutants confirms the observations of crossover redistribution made for SNI1. The study reveals the importance of the SMC5/6 complex in ensuring the proper progress of meiotic recombination in plants.

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Diffusion-mediated HEI10 coarsening can explain meiotic crossover positioning in Arabidopsis

Nature Communications ◽

10.1038/s41467-021-24827-w ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Chris Morgan ◽

John A. Fozard ◽

Matthew Hartley ◽

Ian R. Henderson ◽

Kirsten Bomblies ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Ring Finger ◽

Super Resolution ◽

Ring Finger Protein ◽

Wild Type ◽

Crossover Interference ◽

Finger Protein ◽

Meiotic Crossover ◽

Mechanistic Basis

AbstractIn most organisms, the number and distribution of crossovers that occur during meiosis are tightly controlled. All chromosomes must receive at least one ‘obligatory crossover’ and crossovers are prevented from occurring near one another by ‘crossover interference’. However, the mechanistic basis of this phenomenon of crossover interference has remained mostly mysterious. Using quantitative super-resolution cytogenetics and mathematical modelling, we investigate crossover positioning in the Arabidopsis thaliana wild-type, an over-expressor of the conserved E3 ligase HEI10, and a hei10 heterozygous line. We show that crossover positions can be explained by a predictive, diffusion-mediated coarsening model, in which large, approximately evenly-spaced HEI10 foci grow at the expense of smaller, closely-spaced clusters. We propose this coarsening process explains many aspects of Arabidopsis crossover positioning, including crossover interference. Consistent with this model, we also demonstrate that crossover positioning can be predictably modified in vivo simply by altering HEI10 dosage, with higher and lower dosage leading to weaker and stronger crossover interference, respectively. As HEI10 is a conserved member of the RING finger protein family that functions in the interference-sensitive pathway for crossover formation, we anticipate that similar mechanisms may regulate crossover positioning in diverse eukaryotes.

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Mismatch repair impedes meiotic crossover interference

10.1101/480418 ◽

2018 ◽

Cited By ~ 4

Author(s):

Tim J. Cooper ◽

Margaret R. Crawford ◽

Laura J. Hunt ◽

Marie-Claude Marsolier-Kergoat ◽

Bertrand Llorente ◽

...

Keyword(s):

Mismatch Repair ◽

Dna Sequence ◽

Meiotic Recombination ◽

Molecular Level ◽

Computational Modelling ◽

Sequence Divergence ◽

Global Distribution ◽

Crossover Interference ◽

Genome Wide ◽

Meiotic Crossover

SummarySequence divergence, mediated by the anti-recombinogenic activity of mismatch repair (MMR), forms a potent barrier to meiotic recombination and in turn the formation of viable gametes1–5. However, exactly how MMR jeopardizes meiotic success is unclear. Here we utilize a combination ofS. cerevisiaegenetics, genome-wide mapping of recombination and computational modelling to demonstrate that MMR unexpectedly influences the global distribution of recombination through preferential suppression of interfering crossovers (COs) at regions of greater sequence divergence. As a result, inactivation of MMR not only increases the rate of recombination, as previously observed, but also, paradoxically, the strength of CO interference. Our observations reveal a new mechanism by which MMR spatially sculpts the meiotic landscape—linking CO control to the mechanisms that can reproductively isolate a population, and highlighting how genomes may become meiotically incompatible at the molecular level, dependent upon interactions of the primary DNA sequence.

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Faculty Opinions recommendation of Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.13436965.14811068 ◽

2012 ◽

Author(s):

Sheila McCormick

Keyword(s):

Arabidopsis Thaliana ◽

Natural Variation

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Faculty Opinions recommendation of Topoisomerase II mediates meiotic crossover interference.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718499008.793497626 ◽

2014 ◽

Author(s):

Jeff Sekelsky ◽

Talia Hatkevich

Keyword(s):

Topoisomerase Ii ◽

Crossover Interference ◽

Meiotic Crossover

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Crossover Interference in Saccharomyces cerevisiae Requires a TID1/RDH54- and DMC1-Dependent Pathway

Genetics ◽

10.1093/genetics/163.4.1273 ◽

2003 ◽

Vol 163 (4) ◽

pp. 1273-1286 ◽

Cited By ~ 3

Author(s):

Miki Shinohara ◽

Kazuko Sakai ◽

Akira Shinohara ◽

Douglas K Bishop

Keyword(s):

Saccharomyces Cerevisiae ◽

Meiotic Recombination ◽

Strand Break ◽

Tetrad Analysis ◽

Yeast Saccharomyces Cerevisiae ◽

Crossover Interference ◽

Meiotic Progression ◽

Invasion Stage ◽

Strand Invasion ◽

Dependent Pathway

Abstract Two RecA-like recombinases, Rad51 and Dmc1, function together during double-strand break (DSB)-mediated meiotic recombination to promote homologous strand invasion in the budding yeast Saccharomyces cerevisiae. Two partially redundant proteins, Rad54 and Tid1/Rdh54, act as recombinase accessory factors. Here, tetrad analysis shows that mutants lacking Tid1 form four-viable-spore tetrads with levels of interhomolog crossover (CO) and noncrossover recombination similar to, or slightly greater than, those in wild type. Importantly, tid1 mutants show a marked defect in crossover interference, a mechanism that distributes crossover events nonrandomly along chromosomes during meiosis. Previous work showed that dmc1Δ mutants are strongly defective in strand invasion and meiotic progression and that these defects can be partially suppressed by increasing the copy number of RAD54. Tetrad analysis is used to show that meiotic recombination in RAD54-suppressed dmc1Δ cells is similar to that in tid1; the frequency of COs and gene conversions is near normal, but crossover interference is defective. These results support the proposal that crossover interference acts at the strand invasion stage of recombination.

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Crossover Interference in Arabidopsis

Genetics ◽

10.1093/genetics/160.4.1631 ◽

2002 ◽

Vol 160 (4) ◽

pp. 1631-1639 ◽

Cited By ~ 6

Author(s):

G P Copenhaver ◽

E A Housworth ◽

F W Stahl

Keyword(s):

Arabidopsis Thaliana ◽

Degrees Of Freedom ◽

Double Strand Breaks ◽

Crossing Over ◽

Chi Square ◽

Strand Breaks ◽

Crossover Interference

AbstractThe crossover distribution in meiotic tetrads of Arabidopsis thaliana differs from those previously described for Drosophila and Neurospora. Whereas a chi-square distribution with an even number of degrees of freedom provides a good fit for the latter organisms, the fit for Arabidopsis was substantially improved by assuming an additional set of crossovers sprinkled, at random, among those distributed as per chi square. This result is compatible with the view that Arabidopsis has two pathways for meiotic crossing over, only one of which is subject to interference. The results further suggest that Arabidopsis meiosis has >10 times as many double-strand breaks as crossovers.

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Maximal Power Tests for Detecting Defects in Meiotic Recombination

Genetics ◽

10.1093/genetics/161.3.1333 ◽

2002 ◽

Vol 161 (3) ◽

pp. 1333-1337

Author(s):

Thomas I Milac ◽

Frederick R Adler ◽

Gerald R Smith

Keyword(s):

Optimal Design ◽

Design Of Experiments ◽

Meiotic Recombination ◽

Region Of Interest ◽

Genetic Distances ◽

Genomic Region ◽

Maximal Power ◽

Optimal Design Of Experiments ◽

Crossover Interference ◽

Single Interval

Abstract We have determined the marker separations (genetic distances) that maximize the probability, or power, of detecting meiotic recombination deficiency when only a limited number of meiotic progeny can be assayed. We find that the optimal marker separation is as large as 30–100 cM in many cases. Provided the appropriate marker separation is used, small reductions in recombination potential (as little as 50%) can be detected by assaying a single interval in as few as 100 progeny. If recombination is uniformly altered across the genomic region of interest, the same sensitivity can be obtained by assaying multiple independent intervals in correspondingly fewer progeny. A reduction or abolition of crossover interference, with or without a reduction of recombination proficiency, can be detected with similar sensitivity. We present a set of graphs that display the optimal marker separation and the number of meiotic progeny that must be assayed to detect a given recombination deficiency in the presence of various levels of crossover interference. These results will aid the optimal design of experiments to detect meiotic recombination deficiency in any organism.

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Genetic analysis of a Piezo-like protein suppressing systemic movement of plant viruses in Arabidopsis thaliana

Scientific Reports ◽

10.1038/s41598-019-39436-3 ◽

2019 ◽

Vol 9 (1) ◽

Cited By ~ 9

Author(s):

Zhen Zhang ◽

Xin Tong ◽

Song-Yu Liu ◽

Long-Xiang Chai ◽

Fei-Fan Zhu ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Genetic Analysis ◽

Plant Viruses ◽

Systemic Movement

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Molecular and genetic analysis of the yeast early meiotic recombination genes REC102 and REC107/MER2.

Molecular and Cellular Biology ◽

10.1128/mcb.12.3.1248 ◽

1992 ◽

Vol 12 (3) ◽

pp. 1248-1256 ◽

Cited By ~ 23

Author(s):

M Cool ◽

R E Malone

Keyword(s):

Sequence Analysis ◽

Genetic Analysis ◽

Meiotic Recombination ◽

Genetic Recombination ◽

Recombination Process ◽

Genetic Complementation ◽

Rec Genes ◽

Reductional Division

By selecting for mutations which could rescue the meiotic lethality of a rad52 spo13 strain, we isolated several new Rec genes required relatively early in the meiotic recombination process. This paper presents data to confirm that two of them, REC102 and REC107, are general, meiosis-specific recombination genes that have no detectable role during mitosis. Sequence analysis and genetic complementation indicate that REC107 is identical to the MER2 gene. No sequences related to REC102 have been found in the GenBank or EMBL collections. REC102 is expressed only in meiosis, prior to the reductional division, at about the time that genetic recombination occurs. Examination of the REC102 sequence indicates the presence of several sequences which may play a role in the regulation of its expression; however, the URS1 sequence commonly found in genes expressed early in meiosis is not present.

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