SOCLE - SOCial SeLEction in cultivated plants

Project Information

SOCLE

Grant agreement ID: 101030712

DOI

10.3030/101030712

Project terminated on 30 November 2023

EC signature date 7 April 2021

Start date 1 January 2022

End date 31 December 2023

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 191 149,44

EU contribution

€ 191 149,44

Coordinated by

UNIVERSITE DE LAUSANNE
Switzerland

Periodic Reporting for period 1 - SOCLE (SOCLE - SOCial SeLEction in cultivated plants)

Reporting period: 2022-01-01 to 2023-12-31

Summary of the context and overall objectives of the project

Agriculture is facing the need to feed an increasing world population while reducing its impact on the natural environment. A diverse array of solutions ranging from robotics to bioengineering could help solving this dilemma. Besides such technology-based solutions, nature-based solutions could also contribute to the transition towards more resilient and sustainable cultivation practices. Farmers and plant breeders have used the principles of evolution and natural selection for centuries to select crop varieties with improved productivity and quality. However, some evolutionary theories have remained disconnected from plant breeding practices. This is the case of social evolution theories, notably kin selection theory, which have helped us understand the evolution of inter-individual interactions in natural ecosystems. In particular, one great achievement of kin selection is to explain how individuals can evolve costly traits to cooperate with each other and as such achieve a greater collective performance. Applying social evolution theories to crops could thus bring new insights to select less competitive, i.e. more cooperative varieties. The general objective of this project is to apply social evolution theories to plants, using crops as a model in order to better integrate plant-plant interactions in plant breeding programs. First, we aim at quantifying the contribution of plant-plant interactions to the heritable variation in productivity-related traits in plants. Second, we aim to identify the traits that underlie social interactions, as these traits could be used as breeding targets. Finally, we aim to identify the genetic regions associated with social effects, which could also be used as breeding targets (e.g. to select cooperative alleles). Identifying genetic variant associated with greater plant cooperation would also be a first step towards the identification of new molecular and ecophysiological pathways underlying plant-plant interactions.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

I approached plant-plant interactions with the conceptual framework of quantitative genetics, in particular Indirect Genetic Effects (IGEs). These models partition the effect that the genes have on their own bearers (direct genetic effects, DGEs) and the effect that they have on their neighbours (indirect genetic effects, IGEs). They have mostly been applied to animals and perennial plants so far. As a proof-of-concept, I first applied IGE models to the model plant species Arabidopsis thaliana, using experimental data already published by one of my supervisor (Samuel Wuest). This analysis revealed that IGEs models are able to quantify the contribution of plant-plant interaction to heritable phenotypic variation as well as to dissect their genetic architecture and evolutionary history. We notably show that alleles with positive IGE (i.e. cooperative alleles) are maintained in specific ecological habitats found at extremal latitudes in A. thaliana. This work was presented at the 2022 ESEB (European Society for Evolutionary Biology) meeting in Pragues (Poster) and published in Nature Ecology and Evolution in 2023 (see list of publication). I then applied the IGEs approach to crops, using two successive field experiments with binary mixtures of wheat varieties. This work was done in collaboration with Agroscope, the Swiss Federal Centre of Excellence in Agricultural Research. We quantified the contribution of IGEs to different agronomic traits, and identified their underlying genomic basis. We could identify some key genes with Indirect Genetic Effects, notably one of the well-known Rht genes associated with a major effect on plant height. Interestingly, we also identified one IGE locus associated with blumenol concentration, a leaf marker for AMF (Arbuscular Mycorrhizal Fungi) colonization. This result motivated a third confirmatory experiment in more controlled conditions (greenhouse) to check the association between the candidate locus and AMF colonization. This work is still on-going and involves a strong collaboration with Prof. Ian Sanders and his postdoc Erica McGale. Preliminary results have been presented to academics and plant breeders during the annual meeting of the French-speaking Cereal Breeders (mainly coming from Belgium, France, and Switzerland), and they will be published in a scientific journal as soon as the analysis of the results from the follow-up experiments is finished. Besides this work in IGEs in A. thaliana and wheat, I conducted a critical review of kin recognition studies in plants. Social evolution theories indeed predict that cooperation can also evolve when individuals are able to recognize their relatives and preferentially direct their help towards them. Multiple (controversial) studies have already reported evidence of kin recognition in different plant species, including in crops. While going through these studies, I realized that most of their results could also be interpreted as manifestations of greenbeard genes, a form of kin selection where a single gene is able to recognize similar copies of itself in other individuals. This motivated an opinion paper currently in press in New Phytologist.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

The results of the project have allowed to better understand plant-plant interactions and their genetic basis. In A. thaliana, first, our study is the first to report the contribution of Indirect Genetic Effects to phenotypic variation and to dissect their genetic architecture using a representative sample of the natural variation of the species. These results contribute to better understand the evolutionary history of the species in Eurasia, establishing a connection between plant-plant interactions, demographic history, and ecological habitats. The genes and molecular functions associated with IGEs inform us on the eco-physiological mechanisms underlying plant-plant interactions (i.e. shade-avoidance), which certainly apply to other plant species. Our results in wheat have direct implications for plant breeding. Notably, we show that part of the variation of plant-plant interaction in heritable (i.e. driven by IGEs), and so that it is accessible to selection. We identify important traits that could also be used as indirect breeding targets to optimize plant-plant interactions. Results from the follow-up experiment will allow clarifying the role of AMF in driving interactions between wheat genotypes, which could have important implications for both fundamental research, e.g. fuelling the current hot debates about common mycorrhiza networks (CMNs); and applied research, e.g. providing recommendations regarding synergies between crop diversification and inoculation strategies. Finally, the objective of the opinion paper on greenbeard genes in plants was to popularize the greenbeard concepts among plant scientists, and hopefully, to initiate new research fronts in plant biology. We provide guidance for this in the article by pointing to the areas of plant science that are, according to us, the most promising for greenbeard discovery, and also by listing the most important scientific questions to initiate this new field of research.

Wheat field experiment