Comparative phylogenomics of lateral gene transfers among grasses

Natural selection acting on the genetic variation existing among individuals within a species is a major driving force in evolution. In multicellular organisms, such as animals and plants, novel genetic variants were assumed until recently to exclusively arise through random mutations in the genetic material passed from parents to offsprings. However, recent years have seen the accumulation of reports of gene transfers between distinct multicellular species in a process called lateral gene transfer (LGT). LGT can spread functional genes for adaptive traits among distant lineages, and in plants, it has facilitated the colonisation of low-light environments, improved efficiency of photosynthesis in high temperatures, and the ability to thrive on different soil types. LGT can therefore lead to big evolutionary leaps, allowing plants to rapidly evolve beyond their inherent potential. However, a high frequency of LGT would also suggest that genetic material might 'escape' from GM crops and be transferred to wild species. This could lead to the emergence of superweeds that would decrease crop yields and damage natural ecosystems. The evolutionary importance and frequency of LGT remain largely unknown due to a lack of dedicated efforts and sparse species sampling in previous studies.
In this project, we will establish the importance of LGT for plant evolution by quantifying the phenomenon in various groups and establishing the factors that promote such gene transfers. Firstly, we will scan the genomes of numerous flowering plants capturing the diversity of the group to test the hypothesis that some lineages of plants are more likely to exchange genes than others. Secondly, we will analyse the LGT in multiple individuals of some grass species, the most important group of flowering plants ecologically and economically. From the distribution of LGT among individuals within each species our innovative approach will calculate the rates of gains of LGT independently from the rates of subsequent losses. This will allow us to test the hypothesis that the rate of random LGT gains is high in all species, but that the rate of subsequent losses varies because of different selection regimes. Thirdly, we will analyse the variation in the number of LGT donated by diverse grass species to determine whether the probability of being the source of the transfers depends on the evolutionary history, morphological characters or the geographic origin of the species.
Our multidimensional project will provide a precise quantification of the amount of LGT gained and lost through time by diverse groups of plants. In addition, our innovative approach will establish the factors that increase the probability of transferring genes to distant relatives. This fundamental knowledge will be pivotal in establishing the importance of genetic exchanges between species on the ecological and functional diversification of plants, potentially leading to a reappraisal of the tree-of-life nature of evolution in multicellular organisms. In addition, the identification of the factors that promote LGT among grasses will help estimate the risk of gene escape from GM crops and develop mitigating strategies.

Our fundamental research project will provide new knowledge about plant evolution, but we have also identified short-term, medium-term and long-term societal impacts for the public, policy makers and industrial parties.

# Members of the public - short term

The application of GM technology is increasingly cited as the best avenue to guarantee food security for a growing human population in a changing climate. However, there is a general public aversion to GM crops, urging for a need for research to ally these fears. By establishing the natural rate of gene transfers among plants, our project will make key contributions to this debate. First, proving that genes are frequently transferred among wild plants will demonstrate that the phenomenon occurs without human interventions, so that GM technology should not be seen as unnatural. Second, the discovery of plant-to-plant exchanges means that there is a genuine risk of gene escape from GM crops, but establishing which groups of plants can be involved in such transfers will directly determine those GM crops that are safe in this respect. We therefore anticipate that the dissemination of our results will lead to a wider acceptance of GM technology.

# Policy makers - medium term

In addition to contributing to the public understanding of risks associated with GM technology, our research will establish which conditions favour gene movements across species boundaries. This knowledge is crucial to determine which species are safe to grow as GM crops, but also to design mitigating strategies. Such mitigation strategies can involve restricting the type of GM crops that are allowed or regulating the conditions in which they can be grown. Policy makers in the UK and the EU will consequently benefit from our research outputs to inform the decision process surrounding the regulation of current and future GM crops.

# Industrial actors - long term

On the longer term, the identification of the factors that promote genetic exchanges among plant species can help develop GM crops with a reduced risk of gene escape. For example, if our analyses reveal that some morphological traits promote LGT, GM technology can be restricted in the future to those varieties that lack such properties. Because we estimate that our large-scale evolutionary studies will need to be followed by applied research on specific crops, we anticipate that our results will serve to channel industrial efforts and their impact will materialize on the long term.