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'.

Keywords: evolution; meiosis; recombination; temperature.

Figure 1.

Mechanisms of meiotic recombination. The various stages of recombination that occur during prophase I are illustrated and include global interactions across entire chromosomes as well as more intricate interactions at the single molecule level. Blue and red strands represent homologous chromosomes, and the meiotic axis and synaptonemal complex are coloured green and orange, respectively. The 5′ ends of DNA molecules are represented with an arrowhead.

Figure 2.

A model for meiotic failure at high temperature. (a) Meiotic axis formation and synapsis are compromised at temperatures exceeding the physiological optimum, leading to aggregation of axis proteins and SC polycomplex formation. Perturbation of axis and SC formation leads to downstream effects such as altered crossover frequency and localization or crossover failure leading to univalent formation. (b,c) Prophase I cells from tetraploid Arabidopsis arenosa grown at 22°C (optimal) and 33°C (>optimal) temperatures and stained for the axis-associated protein ASY1 (green), the SC transverse filament protein ZYP1 (red) and DNA (stained with DAPI, blue). (b) At 22°C a linear axis is formed and the cell undergoes full synapsis via the formation of a continuous SC. (c) At 33°C discontinuous ASY1 staining is observed along with axis-associated ASY1 aggregate formation (white arrowheads) and ZYP1 polycomplexes (white arrows) form in regions that are both linked and unlinked to the axis. Scale bars, 10 µm.