Temperature and the evolution of core meiosis proteins
Temperature extremes are known in a wide range of species of fungi, plants and animals to cause problems with fertility. In at least some cases, these have been shown to be due to failures in meiotic prophase, specifically of the chromosome axes and synaptonemal complexes (both are fragmented and SC accumulates in large self-assembling foci) (Bomblies et al 2015).
Figure 1: Meiotic failure at high temperature. (A) Normal zygotene spread of A. arenosa grown in cool temperatures. Chromosome axes, which form along the length of aligned sister chromatids (replicated copies of the same chromosome), are marked by ASY1 (yellow-green). Synaptonemal complexes, which form between the axes of homologous chromosomes, are marked by ZYP1 (red). AE = axial element. SC = synaptonemal complex. (B) At high temperature, axes are often fragmented, ASY1 material builds up in “foci” (ASY1(Foc)) and ZYP1 fails to form linear structures. Instead ZYP1 forms only short extensions and self-polymerizes to form stacked “polycomplexes” (ZYP1(PC)). Images: J Higgins (U Leicester) & C Morgan (Franklin lab, U Birmingham).
The threshold at which axis and SC failure occurs, however, varies among species, and not surprisingly, tracks habitat of origin to at least some degree (Bomblies et al. 2015). The important point about this is that the temperature tolerance of meiosis is evolvable - it can be modified! The genes and mechanisms involved in the evolution of meiotic thermostability are entirely unknown.
In Arabidopsis arenosa we found that populations that colonised a warmer habitat have increased temperature tolerance for fertility relative to mountain populations. In our conditions, mountain populations have low fertility at 19C, but lowland plants have high fertility. We are currently using mapping approaches to understand the molecular basis of this. Based on the observation that two axis-associated proteins (ASY3 and SYN1; Wright et al 2015) and a difference in axis stability at different temperatures (K Wright, K Bomblies, unpublished), we suspect that temperature stabilisation is achieved in these populations through modifications of the core axis and synaptonemal complex proteins that also seem to be important in polyploid evolution. How are these proteins modified? Is it their thermostability that is directly altered? Is it their interactions that are stabilised? Are they involved at all, or are the signatures of selection in these proteins caused by something else? Can we transfer thermostability among species? Are there costs in terms of other meiotic functions to high temperature tolerance?
Bomblies, K., Higgins, J.D., Yant, L. (2015) Meiosis evolves: Adaptation to external and internal environments. New Phytologist 208: 306-323.
Wright, K.M., Arnold, B., Xue, K., Šurinová, M., O’Connell, J., Bomblies, K. (2015) Selection on meiosis genes in diploid and tetraploid Arabidopsis arenosa. Mol Biol Evol 32: 944-955.