Meiotic recombination heats up

Meiotic recombination is essential for the production of viable haploid gametes in sexually-reproducing organisms, and creates new allelic combinations, whichmay facilitate evolution by natural selection and genetic drift (Barton & Charlesworth, 1998). Crossovers between homologous chromosomes establish physical connections (chiasmata) which enable proper chromosome segregation. In the absence of chiasmata, homologous chromosomes align as univalents on the metaphase plate and segregate randomly, leading to aneuploidy and inviable gametes; in mammals this also leads to pregnancy loss or severe mental and developmental defects in the surviving fetus. Proper meiotic chromosome disjunction is affected not only by the presence or absence of chiasmata, but also by their placement along the chromosome. Crossovers that are too distal or too proximal relative to the centromere contribute to missegregation and aneuploidy in plants, fungi and animals including humans (Hunt, 2006). Because growth anddevelopment in plants is more robust to chromosomal abnormalities, plants represent uniquely powerful tools to understand the regulation of crossover frequency and placement; these insights also offer practical applications in plant breeding. Precision genetic engineering technologies such as the CRISPR/CAS9 system hold enormous potential but are currently limited primarily to gene disruption in plants. Harnessing the molecular factors that control crossovers may enable routine targeted gene replacement. Moreover, the genes underlying traits of interest are not always known. In these cases, manipulation of crossover frequency and distribution would be exceedingly useful in traditional plant breeding efforts, which require recombination between elite genetic backgrounds to enhance the agronomic value of crops. Understanding how environmental conditions – particularly field conditions – influence these systems will be a critical aspect of tapping into this potential. Although it has long been known that the frequency of crossovers can be modulated by genetic and environmental factors such as temperature (e.g. Stern, 1926), and that mammalian recombination hotspots are regulated by the PRDM9 protein (Baudat et al., 2010), we have only recently begun to discover phenomenon that explain the placement of crossovers in plants (Higgins et al., 2012; Choi et al., 2013; Hellsten et al., 2013). In this issue of New Phytologist, Phillips et al. (pp. 421–429) take an important first step towards understanding the underlying mechanics of a temperature-induced increase in crossover frequency and shift in crossover distribution in barley (Hordeum vulgare). Crossovers in plants, fungi, and most animals are formed through two pathways, interference-sensitive (Type I) and interference-insensitive (Type II). Type I crossovers are mediated by ZMMproteins, and are inhibited from occurring near one another (Shinohara et al., 2008), while Type II crossovers are mediated by MUS81 and are unconstrained by the presence of adjacent crossovers (Berchowitz et al., 2007). In order to assess how temperature affects both the frequency and placement of crossovers, Phillips et al. use immunofluorescent staining ofMLH3 foci to examine the distribution and number of Type I crossovers at elevated and control temperatures, as well as genetic mapping to tease apart differences between male and female meioses. The authors find that increases in temperature result in an increase in total crossovers, as measured bymap distance. Curiously, there was not a corresponding increase in MLH3 foci, instead Type I crossovers shifted fromdistal to proximal and interstitial placement (Fig. 1). Furthermore, they find that this shift and the increase in total crossovers occurs only in male meioses. As in Arabidopsis, male and female meioses in barley and other cereals exhibit differences in the frequency and placement of crossovers (heterochiasmy; Drouaud et al., 2007). Their results suggest that in barley, temperature-dependent crossovers are derived from the Type II pathway, and that crossover homeostasis in male and female meiosis is perhaps differentially regulated. More importantly, their findings demonstrate that not only the frequency, but also the distribution of meiotic recombination events can be regulated by external factors, such as temperature.