Meiotic recombination: how has this adaptive and evolutionary force been influenced by domestication and selective breeding?

Lead Research Organisation: Rothamsted Research
Department Name: Sustainable Soils and Crops

Abstract

Plant domestication and the origin of agriculture date from ca. 10,000 years ago and have had profound effects on genome evolution demonstrated in the dramatic phenotypic differences between wild progenitors and domesticated crops. The transition from wild to domesticated plants followed by selective breeding has led to a reduction of genetic diversity. In this proposal we propose that meiotic recombination has played a key role in the reduction of genetic diversity in crops and the difference in genetic diversification between wild and crop species. Meiotic recombination is the basic process of sexual reproduction in germs cells that exchanges genetic information between chromosomes breaking the linkage between genes to form new allelic combinations. Meiotic recombination is a powerful force for plant genome evolution and adaptation to local environment as well as during breeding.

Meiotic recombination and the intense selection during breeding have highly influenced plant genome evolution, but it remains unclear how these two processes are connected. In this project, we will evaluate how meiotic processes have diverged during breeding to effectively reduce genetic variation in crops. We will use advanced genomic technologies to sequence the DNA molecules bound to meiotic recombination proteins and profile the landscape of meiotic recombination genome-wide in wild and domesticated wheat. These new datasets will be unique due to their high-resolution and will allow us to explore local recombination rate over genes to test the genetic effects of domestication and to understand the differing evolutionary trajectories between natural and agricultural environments.

This project will also address an essential knowledge gap as it will determine if genes of agricultural relevance that have been under strong selection during breeding have retained recombinational properties for further genetic improvements. Initial investigations will be carried out on trehalose phosphate synthase (TPS) and trehalose phosphate phosphatase (TPP). TPSs and TPPs determine the way sugars in plants are allocated which strongly affects plant adaptation to environment, growth and development and crop yields; they are important targets in crop improvement. With the knowledge generated in this project it will be possible to understand how some of the genetic variation in TPSs and TPPs has been lost during the crop selection process. We will also investigate local recombination rate over meiotic genes to test whether they too have been fixed by selective breeding. This will enable us to understand how loss of genetic diversity for important genes has reduced the adaptive potential to create novel genetic diversity.

Overall, this project will generate high resolution and genome-wide recombination data to gain key insights in gene evolution between natural and agricultural environments. Our research initially focuses on three gene families but could be extended to any gene families in future studies. Hence, this project addresses a key fundamental question in evolutionary biology with the potential to establish new concepts on the genetic effects of domestication and to promote the strategic mission of NERC in "Population genetics and evolution".

Publications

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Description This project evaluated the extend to which meiotic recombination differs between wild and domesticated and between tetraploid and hexaploid wheat lines. Using cytological approaches, we found that the number of crossovers per chromosome is relatively stable between lines but that the positioning of crossovers along the chromosomes substantially varies. For instance, we found a wild wheat variety with crossovers occurring at high frequency in centromere-proximal regions. This is very interesting as these regions are generally repressed for recombination in wheat elite lines. Identification of lines with unusual crossover landscape can provide fundamental knowledge on the molecular mechanisms controlling crossover position and valuable information to design tools to reposition crossovers in elite lines to create novel genetic variation.
During this project, we developed a collaboration with members of the Genetics, Reproduction and Development Institute, CNRS, University Clermont Auvergne (France) and optimised methods to isolate meiocytes for genomic work across a range of wheat lines. We also developed a semi-automated system to rapidly and accurately count recombination foci on meiotic chromosomes immunostained for recombination proteins. These new techniques will benefit the wheat scientific community and advance our study of meiosis in wheat.
We also identified several meiotic genes with signature of evolution in tetraploid and hexaploidy lines. Some proteins essential for meiotic recombination seem to have evolved and gained or lost motifs with putative roles in meiosis. These observations raise important fundamental questions in evolutionary biology and follow-up studies to evaluate if certain meiotic proteins have gained/lost functions and the consequences on crossover positioning will be evaluated. As part of this research outcome, we developed fruitful collaboration with members of INRAE, Genetics, Diversity & Ecophysiology of Cereals, France to further investigate the evolution of meiotic genes.
Exploitation Route It is estimated that 80% of the wheat genome doesn't recombine because recombination is restricted at the end of the chromosomes. Our finding of a line with centromere-proximal recombination has high value for breeding as it can unlock the genetic potential of some of the recombination-repressed regions and create novel genetic variation not currently possible through conventional breeding. Our data also has high value for academic as it provides opportunities to study the mechanisms of crossover position in wheat by comparing different lines. For example, follow-up studies could focus on the identification of the gene(s) responsible for the observed unusual crossover positioning in the wild wheat line.
Sectors Agriculture

Food and Drink

 
Description Educational developments in the form of a course and course material
Geographic Reach Local/Municipal/Regional 
Policy Influence Type Influenced training of practitioners or researchers
Impact This course increased student awareness on the importance of meiotic recombination in breeding programmes to improve crop genetics. The course also improved the student knowledge on the evolution of plant genome, population genetics and aspects of meiotic processes.
 
Description Evolution of meiotic genes in wheat 
Organisation Genetics, Diversity and Ecophysiology of Cereals
Country France 
Sector Public 
PI Contribution We identified several meiotic genes with signature of evolution in tetraploid and hexaploid wheat lines. We have strong expertise in genetics and meiotic recombination but needed some insights from experts in wheat genome evolution. We decided to contact members of INRAE, UCA Genetics, Diversity & Ecophysiology of Cereals (France) and shared our finding to collaborate with them on this project. Members of INRAE have expertise in the field of plant genome evolution having published some work on the "evolution of recombination landscapes in diverging populations of bread wheat". We are continuing our analysis on the change of function of meiotic genes during evolution and are benefiting from this collaboration.
Collaborator Contribution Members of INRAE have extensive knowledge and technical expertise in the study of wheat meiosis. They shared information on their unpublished work, biological material (wheat mutant lines), and genomic expertise that we can use to further study the evolution of meiotic genes in wheat and experimentally test hypotheses. We are particularly interested to understand if and how meiotic genes have changed function to adapt to ploidy change. To further stimulate discussion and strengthen the collaboration, they invited me to visit their department and give a talk.
Impact The collaboration lead to an invitation by members of INRAE for me to visit their department and give a seminar in 2023. We also submitted a joint PhD project to an INRAE funding call (pending). The research work is ongoing and will lead to a publication upon completion of the experiments.
Start Year 2022
 
Description Invited seminar 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Invited seminar at INRAE, UMR 1095 INRAE - UCA Genetics, Diversity & Ecophysiology of cereals, Clermont-Ferrand, France. The title of my seminar was "The control of meiotic recombination for crop genetic improvement".
The aim of this activity was to update a scientific audience on my group research activities and recent findings. There was a high interest in the audience about my group research activities leading to questions and discussion afterwards and the start of new collaborative work between my group and members of the INRAE institute.
Year(s) Of Engagement Activity 2023