Proximal and ultimate causes of adaptive lateral gene transfers in land plants

In multicellular organisms, evolution is classically thought to proceed exclusively through natural selection on mutations occurring within genes present in the genome of a single species. This paradigm has been challenged by recent reports of lateral gene transfers among multicellular animals and plants. In particular, we have recently shown that laterally acquired genes were integrated into the basic metabolism of some grasses and contributed to the adaptation of their photosynthetic apparatus through the optimization of a novel photosynthetic pathway, namely C4 photosynthesis. This trait increases the productivity of plants living in warm and dry conditions and would consequently lead to an increase of yield if introduced into crops using the ancestral C3 photosynthetic pathway, including rice and wheat. Elucidating the mechanisms behind naturally occurring adaptive transfers of genes for C4 photosynthesis among grasses would open new potential strategies for this endeavour. We currently do not understand how or why these gene transfers occurred. We propose to tackle these issues by sequencing and comparing the genomes of closely related grasses that differ in their photosynthetic types and in the number of laterally acquired genes they possess.
This project will capitalize on the availability of high-throughput sequencing, using comparative genomics to address a key question in evolutionary biology. Complete genomes will be generated de novo for four closely related taxa of the grass genus Alloteropsis, two of which belong to the same species complex but use C3 and C4 photosynthesis, respectively. Thirty additional individuals from the same species complex, sampled from different continents and with different laterally acquired genes, will be selected for re-sequencing, and their genomes will be assembled using the de novo assemblies as a reference. All markers generated for Alloteropsis will be analysed within a phylogenetic framework that will incorporate publicly available complete genomes for model grasses, two of which are closely related to the donors of laterally transferred genes. All Alloteropsis genes that are statistically more closely related to their equivalents in species outside Alloteropsis will be identified as laterally acquired genes. The genomic regions surrounding them will be investigated to test alternative hypotheses about the mechanism responsible for the transfer. Finally, the evolutionary history of key C4 genes, including gradual C4-adaptive changes and loss of function, will be used to infer the photosynthetic type of the plants that received the gene transfers, shedding new light on the adaptive significance of the foreign genetic material incorporated.
This multifaceted project will determine how and why adaptive lateral gene transfers occurred in grasses, enabling new understanding of the conditions that allow the lateral spread of functional traits among distantly related species. In addition, this fundamental research project will have a direct impact on the efforts to engineer rice using C4 photosynthesis to feed the growing human population, by elucidating the conditions that allowed successful transfers in the wild. Finally, the proposed project will generate the first genomes for closely related taxa that use different photosynthetic types, providing new and valuable resources for the identification of the fine-scale genetic (especially regulatory) changes that allow photosynthetic adaptation in grasses, the ecologically and economically most important group of plants.

The results of our projects are likely to be of the greatest interest for crop scientists working on engineering C4 photosynthesis in C3 crops, such as rice. This is especially the case for the C4rice project funded partially by the Bill & Melinda Gates foundation (http://c4rice.irri.org/) and partially by the UK Government via UK Aid, and the 3to4 project funded by the European Union (http://www.3to4.org/). These two international consortia aim at translating the knowledge from academic research to engineer commercially viable crops with an increased yield in tropical countries. Besides academics from numerous institutions worldwide (including the University of Sheffield), they include multiple industrial partners, which have the financial means to translate fundamental research into agronomical outputs.

The efforts to improve C3 crops by the human-directed introgression of C4 photosynthesis would directly benefit from the elucidation of the mechanisms involved in the successful transfer of C4 genes among grass species in the wild, which is one of the primary goals of the proposed research. Indeed, if the transfers can be reproduced by breeders, they would lead to the incorporation of C4-optimized genes in the basic metabolism of C3 crops. In addition, the genomic resources that will be generated in this project can be used to identify new candidate genes for aspects of C4 photosynthesis for which the genetic determinism is unknown. This is particularly important for C4 anatomical characters, metabolite transporters, and regulators. These characters are variable within Alloteropsis, and genomic data for multiple individuals that vary for these traits can be used to detect new candidate genes through association mapping, or similar approaches. Genes for these C4 characters could then be introduced in C3 crops (e.g. by replacing them with genes from C4 species) to generate the C4 anatomy that is necessary for engineering C4 photosynthesis.