Abstract
Changes in environmental temperature influence cellular processes and their dynamics, and thus affect the life cycle of organisms that are unable to control their cell/body temperature. Meiotic recombination is the cellular process essential for producing healthy haploid gametes by providing physical links (chiasmata) between homologous chromosomes to guide their accurate segregation. Additionally, meiotic recombination—initiated by programmed DNA double-strand breaks (DSBs)—can generate genetic diversity and, therefore, is a driving force of evolution. Environmental temperature influencing meiotic recombination outcome thus may be a crucial determinant of reproductive success and genetic diversity. Indeed, meiotic recombination frequency in fungi, plants and invertebrates changes with temperature. In most organisms, these temperature-induced changes in meiotic recombination seem to be mediated through the meiosis-specific chromosome axis organization, the synaptonemal complex in particular. The fission yeast Schizosaccharomyces pombe does not possess a synaptonemal complex. Thus, we tested how environmental temperature modulates meiotic recombination frequency in the absence of a fully-fledged synaptonemal complex. We show that intragenic recombination (gene conversion) positively correlates with temperature within a certain range, especially at meiotic recombination hotspots. In contrast, crossover recombination, which manifests itself as chiasmata, is less affected. Based on our observations, we suggest that, in addition to changes in DSB frequency, DSB processing could be another temperature-sensitive step causing temperature-induced recombination rate alterations.
Highlights
Single-celled organisms, such as yeasts, and other organisms unable to control their internal temperature are at the mercy of the environmental temperature, which can fluctuate considerably between seasons and during day-night cycles
Temperature effects on recombination are largely species-specific and can manifest in different ways: (I) CO frequencies follow a U-shaped distribution in Drosophila or Arabidopsis (Plough 1917; Lloyd et al 2018), where CO recombination is highest at the more extreme temperatures within the fertile range, (II) CO frequency increases with increasing temperature in C. elegans (Rose and Baillie 1979), (III) in grasshoppers CO frequency decreases with increasing temperature (Church and Wimber 1969) and (IV) in S. cerevisiae, Hordeum vulgare and Secale cereale overall CO frequency is maintained (De La Peña et al 1980; Higgins et al 2012; Zhang et al 2017)
Changes in environmental temperature during sexual reproduction affect the duration of mating, meiosis and sporulation (Fig. 1), as well as the meiotic recombination outcome tested at several versions of a genetic interval containing multiple different ade6 heteroalleles (Fig. 3)
Summary
Single-celled organisms, such as yeasts, and other organisms unable to control their internal temperature are at the mercy of the environmental temperature, which can fluctuate considerably between seasons and during day-night cycles. Environmental temperature has been suggested to be a major driver in the evolutionary adaptation of the meiotic machinery (Bomblies et al 2015). The main function of meiotic recombination is to ensure correct chromosome segregation, as it establishes physical connections between the homologous chromosomes (homologues). This is achieved through the repair of programmed DNA double-strand breaks (DSBs) from the homologue rather than the sister chromatid, and the processing of recombination intermediates between the homologues as crossovers (COs) (de Massy 2013; Hunter 2015). The DSB ends are resected to enable homologous recombination, which leads to COs and non-crossovers (NCOs) depending on the repair pathway (de Massy 2013; Gray and Cohen 2016)
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