Hot Regions of Noninterfering Crossovers Coexist with a Nonuniformly Interfering Pathway inArabidopsis thaliana

Abstract

In most organisms that have been studied, crossovers formed during meiosis exhibit interference: nearby crossovers are rare. Here we provide an in-depth study of crossover interference in Arabidopsis thaliana, examining crossovers genome-wide in .1500 backcrosses for both male and female meiosis. This unique data set allows us to take a two-pathway modeling approach based on superposing a fraction p of noninterfering crossovers and a fraction (1 2 p) of interfering crossovers generated using the gamma model characterized by its interference strength nu. Within this framework, we fit the two-pathway model to the data and compare crossover interference strength between chromosomes and then along chromosomes. We find that the interfering pathway has markedly higher interference strength nu in female than in male meiosis and also that male meiosis has a higher proportion p of noninterfering crossovers. Furthermore, we test for possible intrachromosomal variations of nu and p. Our conclusion is that there are clear differences between left and right arms as well as between central and peripheral regions. Finally, statistical tests unveil a genome-wide picture of small-scale heterogeneities, pointing to the existence of hot regions in the genome where crossovers form preferentially without interference. SEXUALLY reproducing organisms undergo meiosis, thereby producing gametes having a level of ploidy equal to half that of the parental cells. This reduction in ploidy emerges from a complex and tightly controlled sequence of events. In most organisms, prophase I of meiosis begins by the active formation of double-strand breaks (DSBs) mediated by Spo11, a topoisomerase-like transesterase (Keeney et al. 1997). Then homologous chromosomes align and pair as the DSBs are repaired, typically using a homolog as template. Such DSB repairs can lead to either a crossover (CO), a reciprocal exchange of large chromosomal fragments between homologs), or to a noncrossover (NCO), a nonreciprocal exchange of small chromosomal segments between homologs, detected through associated gene conversions (Bishop and Zickler 2004)). COs mediate intrachromosomal rearrangement of parental alleles, giving rise to novel haplotypes in the gametes and thus driving genetic diversity. They also provide a physical connection between the homologs, holding them in a stable pair (bivalent) and allowing their correct segregation during anaphase I (Page and Hawley 2004;Jones and Franklin 2006). Studies in several plants and animals have shown that the average number of COs in meiosis may vary between male and female meiosis (see review by Lenormand and Dutheil 2005), but there is no general rule that governs the direction or degree of CO number variation. Similarly, the distribution of COs along chromosomes can also differ when comparing male and female meiosis (Drouaud et al. 2007). Such distributions are generally nonuniform: some portions of the physical chromosome seem more likely to recombine while others hardly ever do (e.g., close to the cent...

High‐throughput measurement of recombination rates and genetic interference in Saccharomyces cerevisiae

“…Also, we always observed significant positive CO interference for diploids SK1 × SK1, which is in accordance with previous studies reporting positive interference in S. cerevisiae (Chen et al, ; de los Santos et al, ; Malkova et al, ; Stahl et al, ). We also observed significant variation of CoC values along chromosomes, which may reflect a variation of the CO/NCO ratio, as already reported in S. cerevisiae (Mancera et al, ; Zhao, Speed, & McPeek, ) and would be compatible with the data in A. thaliana (Basu‐Roy et al, ). However, CoC values of SK1 × W303 hybrids showed apparent negative (or absence of) CO interference (CoC > 1), especially on chromosome VI.…”

Role ofcis,trans, and inbreeding effects on meiotic recombination inSaccharomyces cerevisiae

“…[8] reported significant differences among 23 hybrids based on the gamma model. We also measured variations of interference intensity along and between chromosomes, as already reported in S. cerevisiae [6,49] and in Arabidopsis [50]. Our results showed significant positive correlations (averaged across seven testers) between recombination rate and interference strength, whereas in maize, Bauer et al .…”

Modelling Sex-Specific Crossover Patterning inArabidopsis

“…In each round of each analysis, 30,000 bivalents were simulated for a range of parameter values. In the first round, to ensure the full parameter space was sampled, relatively broad value ranges of optimized parameters (Smax: 2-10 L: 0.4-1.7; T2Prob: 0.002-0.008; cL: 0.3-1.3, and cR: 0.3-1.3) were chosen based on values described in Zhang et al (2014a) and comparison of ad hoc simulations with analysis of experimental data sets (Basu-Roy et al 2013). Parameters N, B, E, Bs/Be/Bd, A, and M were set at appropriate default values (see below).…”