Understanding and ameliorating the impact of climate change on plant meiosis

Increasing temperatures associated with climate change are expected to impact food security by causing reductions in the global yield of many major crops. The reproductive phase of plant development is acutely sensitive to temperature stress and exposure to high temperature extremes during this phase is the primary cause of reduced fertility (and yield) in many crops. Meiosis, a special cell division that produces the cells required for sexual reproduction (pollen and eggs in plants, sperm and eggs in humans), represents an important 'weak-link' in the plant reproductive cycle and is known to fail at high temperatures in a variety of plant species, leading to losses of fertility. However, what actually causes meiosis to fail under temperature extremes, and how this might be prevented, remains almost completely mysterious.

I have preliminary evidence that meiotic failure at extreme high temperature (33 degrees) occurs as a consequence of the misassembly and aggregation of multi-protein complexes (the meiotic axis and synaptonemal complex) that orchestrate dynamic chromosomal interactions during the early stages of meiosis. My first objective in this project will progress these initial observations to further characterise the problems that are faced by cells undergoing meiosis at extreme temperatures and to assess the contribution of these problems to overall reductions in plant fertility. To achieve this, I will systematically analyse the effects of a range of high temperatures on meiosis in the model plant species Arabidopsis thaliana using state-of-the-art microscopy. Arabidopsis is a small weed-like plant and is widely used by plant scientists as it possesses numerous features that make it highly amenable for research, allowing meaningful biological conclusions to be drawn from experiments in this species much more rapidly than they could from other non-model crop species.

For my second objective, I will assess the impact of extreme temperatures on the expression of genes in Arabidopsis cells undergoing meiosis. This will shed light on how changes in the expression of particular genes in meiotic cells can either increase or decrease the thermal tolerance of meiosis in Arabidopsis.

Wild populations of Arabidopsis thaliana can also be found occupying a range of different habitats, experiencing highly variable maximum and minimum temperatures. The third objective of my project will be to determine if populations of Arabidopsis thaliana that have adapted to undergoing fertilisation in warmer or cooler environments exhibit strong differences in their meiotic thermal stability and, thus, whether these plants have adapted to hotter temperatures by enhancing their meiotic thermal tolerance.

My project's main aims are to uncover the molecular mechanisms that underpin the thermal sensitivity of meiosis and to find ways to overcome these mechanisms to increase meiotic thermal tolerance in plants. As meiosis is a highly conserved process, with meiosis in yeast, humans and plants all occurring via similar mechanisms, it is likely that any discoveries made in Arabidopsis will be translatable to more economically important crop species. As well as shedding light on aspects that control meiotic thermal stability, my project is also likely to offer novel insights into how chromosomes exchange segments of DNA during meiosis (a process that is of great interest to plant breeders) and it will help to answer fundamental questions about how proteins and cellular processes can evolve in the face of extreme abiotic stress. Taken together, the outcomes of my project will be highly beneficial for ensuring future global food security and sustaining high crop yields in the combined face of climate change and an ever-expanding population. My work maps to all of BBSRC's 'Forward Look for UK Bioscience' themes: 'Advancing the frontiers of bioscience discovery,' 'Tackling strategic challenges,' and 'Building strong foundations'.

Although the temperature sensitivity of meiosis has long been recognised, the molecular mechanisms that underpin this sensitivity remain mysterious. Understanding and overcoming the temperature failure thresholds of meiosis in plants will be important for sustaining high crop yields in the face of climate change.

I have preliminary evidence that extreme high temperature (33 degrees) leads to meiotic failure in A. thaliana due to aggregation of meiotic axis and synaptonemal-complex proteins. My first objective will be to build upon these initial observations using a combination of immunocytochemistry, super-resolution microscopy and live-cell imaging to determine the precise thresholds for meiotic failure and the molecular causes and consequences of this. I will also investigate the effect that perturbing the meiotic axis at high temperatures has on crossover interference.

My second objective will be to use RNA-seq to identify differentially expressed genes in A. thaliana meiocytes that have been exposed to either modest or extreme high-temperatures. This will help to identify candidate genes whose changes in expression will be tested for either strengthening or weakening meiotic stability in response to high temperatures.

Given the thermosensitivity of meiosis, I also expect that A. thaliana accessions that undergo fertilization in regions that experience higher average temperatures will have increased meiotic thermal tolerance compared to accessions that are found in cooler habitats. Therefore, my third objective will be to determine the temperature tolerance of meiosis for accessions collected from diverse habitats, including extreme habitats collected in Africa (collaboration with Dr Angela Hancock, MPIPZ Cologne). I will also take advantage of existing sequencing information to identify sequence variants in candidate genes (cohesins and axis proteins) and test carrier accessions for differences in thermotolerance and other meiotic features.