Are the effects of elevated temperature on meiotic recombination and thermotolerance linked via the axis and synaptonemal complex?

Abstract

Meiosis is unusual among cell divisions in shuffling genetic material by crossovers among homologous chromosomes and partitioning the genome into haploid gametes. Crossovers are critical for chromosome segregation in most eukaryotes, but are also an important factor in evolution, as they generate novel genetic combinations. The molecular mechanisms that underpin meiotic recombination and chromosome segregation are well conserved across kingdoms, but are also sensitive to perturbation by environment, especially temperature. Even subtle shifts in temperature can alter the number and placement of crossovers, while at greater extremes, structural failures can occur in the linear axis and synaptonemal complex structures which are essential for recombination and chromosome segregation. Understanding the effects of temperature on these processes is important for its implications in evolution and breeding, especially in the context of global warming. In this review, we first summarize the process of meiotic recombination and its reliance on axis and synaptonemal complex structures, and then discuss effects of temperature on these processes and structures. We hypothesize that some consistent effects of temperature on recombination and meiotic thermotolerance may commonly be two sides of the same coin, driven by effects of temperature on the folding or interaction of key meiotic proteins.This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

Meiotic chromosome stability of a newly formed allohexaploid wheat is facilitated by selection under abiotic stress as a spandrel

“…Both studies suggest that many types of aneuploidies under the polyploid genetic background did not compromise organismal fitness, thus implying stable meiosis was not immediately under selection. Recently, the importance of environmental factors on the evolution of meiosis stability has been emphasized (De Storme & Geelen, 2014;Wright et al, 2015;Morgan et al, 2017), but our results suggest the roles of environments on the evolution of meiosis can be indirect.…”

High temperatures alter cross-over distribution and induce male meiotic restitution in Arabidopsis thaliana

“…However, despite this common response, it is yet unclear whether heat-induced defects in SC result from a direct physical disruption of structural SC components, or instead indirectly originate from aberrations in upstream regulatory processes that are crucial for SC biogenesis. Based on the observation of thickenings in the chromosome axis of heatstressed meiocytes in several plants and other organisms, it has been postulated that heat directly interferes with SC formation 15,33,35,36 . However, cytological analyses in Arabidopsis did not reveal SC polycomplexes or axis thickenings in heatstressed PMCs, suggesting that heat affects SC biogenesis in an indirect manner.…”

Experimental evolution across different thermal regimes yields genetic divergence in recombination fraction but no divergence in temperature associated plastic recombination

“…Stress has long been associated with changes in recombination frequency (for review see Parsons 1988;Modliszewski and Copenhaver 2017). Another possibility is that recombination rates vary in response to temperature because the recombinational machinery is thermosensitive (Morgan et al 2017). Specifically, if the proteins involved in the synaptonemal complex and axis formation function differently at different temperatures, then crossover number may vary according to temperature (Morgan et al 2017).…”

“…Another possibility is that recombination rates vary in response to temperature because the recombinational machinery is thermosensitive (Morgan et al 2017). Specifically, if the proteins involved in the synaptonemal complex and axis formation function differently at different temperatures, then crossover number may vary according to temperature (Morgan et al 2017). Note that this hypothesis is not at odds with the stress-associated recombination hypothesis; selection may shape thermotolerance of meiotic proteins directly or indirectly, and environments outside of the range to which individuals have adapted may lead to meiotic dysfunction (Morgan et al 2017).…”

“…Specifically, if the proteins involved in the synaptonemal complex and axis formation function differently at different temperatures, then crossover number may vary according to temperature (Morgan et al 2017). Note that this hypothesis is not at odds with the stress-associated recombination hypothesis; selection may shape thermotolerance of meiotic proteins directly or indirectly, and environments outside of the range to which individuals have adapted may lead to meiotic dysfunction (Morgan et al 2017). If thermotolerance plays a role in temperature-associated recombination, then we might expect to see different thermostability of the meiotic axis and/or synaptonemal complex in our C versus H lines, as they have evolved distinct recombination rates.…”