Recombination patterns in maize reveal limits to crossover homeostasis

Abstract

During meiotic recombination, double-strand breaks (DSBs) are formed in chromosomal DNA and then repaired as either crossovers (COs) or non-crossovers (NCOs). In most taxa, the number of DSBs vastly exceeds the number of COs. COs are required for generating genetic diversity in the progeny, as well as proper chromosome segregation. Their formation is tightly controlled so that there is at least one CO per pair of homologous chromosomes whereas the maximum number of COs per chromosome pair is fairly limited. One of the main mechanisms controlling the number of recombination events per meiosis is CO homeostasis, which maintains a stable CO number even when the DSB number is dramatically altered. The existence of CO homeostasis has been reported in several species, including mouse, yeast, and Caenorhabditis elegans. However, it is not known whether homeostasis exists in the same form in all species. In addition, the studies of homeostasis have been conducted using mutants and/or transgenic lines exhibiting fairly severe meiotic phenotypes, and it is unclear how important homeostasis is under normal physiological conditions. We found that, in maize, CO control is robust only to ensure one CO per chromosome pair. However, once this limit is reached, the CO number is linearly related to the DSB number. We propose that CO control is a multifaceted process whose different aspects have a varying degree of importance in different species.meiosis | recombination | crossing-over | double-strand breaks | crossover homeostasis M eiotic recombination creates genetic diversity by generating new allelic combinations in the progeny. In the first step of the recombination pathway, double-strand breaks (DSBs) are formed in chromosomal DNA by a topoisomerase-like protein, SPO11 (1). The DSBs are subsequently repaired in a process that involves several recombination proteins. First, the MRN complex, which includes MRE11, RAD50, and NBS1, resects the DSB ends, leading to formation of 3′ overhangs (2). The single-stranded DNAs created in this way are then coated by two recA-like proteins, RAD51 and DMC1. These proteins catalyze the invasion of homologous doublestranded DNA regions, resulting in single-end invasion (SEI) events (3). Eventually, DSBs are repaired as either crossovers (COs) or non-crossovers (NCOs). Besides generating genetic diversity, crossing-over creates physical connections between homologous chromosomes, which are essential for accurate segregation of the homologs during the first meiotic division. Defects in this process can lead to aneuploidy. Consequently, CO formation, including the number and distribution of COs, is under stringent control (4, 5).To ensure proper segregation of chromosomes during anaphase I, at least one CO must be formed for each homolog pair (6). Failure to meet this requirement leads to chromosome missegregation. Consequently, nonexchange chromosomes are extremely rare in WT meiosis in most species, including maize (7). Even in Caenorhabditis elegans, which forms only one CO per bivalent, th...

Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation

“…Crossover homeostasis was first described in S. cerevisiae and has since been described in S. pombe , C. elegans , maize, and mouse (50, 108, 147, 202, 231, 232). Crossover homeostasis, as initially defined, is the maintenance of crossover frequency even when precursor DSB numbers are decreased (147).…”

“…In maize, for example, Sidhu et al (202) analyzed strains with varying numbers of meiotic DSBs, as measured by RAD51 foci. Interestingly, they found that crossover numbers increased accordingly, suggesting that perhaps homeostasis mechanisms are different in plants.…”

Understanding and Manipulating Meiotic Recombination in Plants

“…Finally, CO homeostasis, which has been documented in S. cerevisiae and mouse, can maintain a stable number of COs even when DSB numbers are altered (Martini et al, 2006). However, a recent study suggested that, at least in maize (Zea mays), CO homeostasis is not prominent (Sidhu et al, 2015), and this result may argue that plants in general do not exhibit this phenomenon.…”

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

“…Different approaches are used to determine both number and positions of COs along homologous chromosomes (Mézard et al, ): Counts of chiasmata, the cytological signatures of COs at metaphase I (Sidhu et al, ), with the risk of missing some chiasmata and thus COs owing to the highly compacted state of metaphase chromosomes. Analysis of protein complexes associated with COs along the less compacted pachytene chromosomes by electron microscopy (EM; observation of late recombination nodules; Anderson et al, ) or by fluorescence microscopy using immunolocalization (Anderson, Reeves, Webb, & Ashley, ). Measuring distances between COs remains, however, time‐consuming.…”