A population genomics approach to accelerating the domestication of the energy grass Miscanthus

The global demands for food and renewable energy are increasing at currently unsustainable rates that are expected to accelerate in the future. A major challenge for plant breeders is therefore to develop bioenergy crops that ideally (1) are highly productive, but carbon negative; (2) can be grown under a wide range of environmental conditions, including marginal lands, but with minimal agronomic inputs (e.g., fertilisers, pesticides, irrigation); (3) produce biomass that can efficiently be converted to biofuels; and (4) can be deployed very rapidly. However, most existing energy crops fail to meet at least one of these requirements. Furthermore, traditional breeding approaches, while certain to be effective, tend to be relatively slow. One way to accelerate breeding cycles is to use diagnostic molecular markers (DNA polymorphisms) to select superior plants at a juvenile age, instead of having to wait for years before direct evaluations can be made. However, an emerging consensus from studies that aim to identify such marker-trait correlations is that genetic variation for most phenotypic traits is underpinned by hundreds of DNA polymorphisms, making it impossible to cherry-pick superior germplasm based on a handful of markers. A more practical approach is therefore to use very large numbers of molecular markers, or even entire genome sequences, to predict phenotypes. This approach, known as genomic selection, is becoming increasingly affordable because of recent breakthroughs in sequencing technology and is believed to have great potential for accelerating crop development and optimisation.

Our project will take advantage of an extensive germplasm collection and apply marker-assisted approaches to accelerate a world-leading breeding programme for the promising energy crop Miscanthus. To achieve this goal, we will first acquire prerequisite information on genome-wide patterns of DNA polymorphism. Then, we will characterise the genomic architectures of phenotypic traits targeted by breeders (i.e., determine the approximate number of DNA polymorphisms underlying genetic variation for each trait and quantify the phenotypic effect of each polymorphism) using state of the art statistical models. Finally, we will apply the genomic selection approach described above to Miscanthus, potentially accelerating breeding cycles 2-3 times and benefitting not only plant scientists and breeders, but also farmers and the general public.

Lignocellulosic biomass is expected to become the most important source of renewable energy in the EU, thereby significantly reducing dependence on fossil fuels and contributing to the mitigation of climate change. Because of their high productivity and low requirements for agricultural inputs, C4 grasses from the tropical genus Miscanthus are believed to have great potential as a bioenergy crop. However, Miscanthus species are essentially undomesticated, and their accelerated breeding is hampered by their primarily outcrossing mating systems and perennial life cycles. To help overcome these challenges, we are proposing to take advantage of a world-leading collection of Miscanthus germplasm (>1500 accessions) that is available at the Institute of Biological, Environmental and Rural Sciences and use high-density molecular marker data and state of the art population genomics approaches to complete three research objectives. First, we will use both model-based and assumption-free analytical approaches to characterise population genetic structure and genome-wide patterns of linkage disequilibrium in a broad collection of Miscanthus germplasm. This will provide the foundation for bridging the gap between phenotype and genotype using genome-wide association studies (GWAS) and genomic selection (i.e., phenotype prediction from a genome-wide set of molecular marker genotypes). Second, we will design and implement large-scale GWAS in multiple species of Miscanthus, elucidating the genomic architectures of important phenotypic traits. Finally, we will assess the feasibility of genomic selection in Miscanthus, potentially accelerating breeding cycles 2-3 times. In addition to Miscanthus biologists and breeders, this research will benefit other scientists from the fundamental fields of plant ecology, genetics and genomics, as well as applied breeders of other perennial crops, farmers and the general public.

Beneficiaries
The key outcomes of this project will be:
1. Detailed and specific information about population genetic structure and genome-wide patterns of allele frequency variation, linkage disequilibrium and recombination in three species of the promising energy crop Miscanthus (Objective 1);
2. Marker-phenotype associations for a number of traits related to phenology, biomass productivity and cell wall composition (Objective 2);
3. Experimental populations, molecular markers and analytical methods that can be used for the accelerated domestication of Miscanthus through genomic selection (Objective 3).
These outcomes will directly impact plant breeders (both publicly and privately funded). Indirectly, this research will also benefit farmers and the wider society. Impacts on each of these groups of beneficiaries are summarised below, and a detailed plan for disseminating our research findings is described in the Pathways to Impact document.

Impact
Outcomes from the proposed research will have a substantial influence on Miscanthus breeding programmes. For example, the detailed molecular genetic characterisation of a broad germplasm collection (Objective 1) will improve the interpretation of results from previous and ongoing crossing and testing operations and will enable the optimisation of these operations in the future. Furthermore, dissecting the genetic and genomic architectures of key phenotypic traits (Objective 2) will inform selection strategies. Most importantly, the ability to predict phenotypes from high-density marker data through genomic selection (Objective 3) could potentially accelerate the breeding cycle 2-3 times, thereby greatly increasing genetic gains per unit of time.

The successful development of high-yielding Miscanthus varieties that require minimal agronomic input would also benefit farmers in the UK and worldwide by diversifying energy crop portfolios and potentially expanding the agricultural land base. The proposed research would contribute to this process in two ways. First, in the short term, genomic selection (Objective 3) could possibly be used to predict the performance of hybrids resulting from crossing accessions that are currently considered superior, as well as potentially from crossing phenotypically uncharacterised (but molecularly fingerprinted) germplasm. This could focus crossing and testing efforts, thereby substantially reducing the time needed to develop first-generation varieties. Second, in the longer term, genomic selection has the potential to greatly increase the rate and reduce the cost of development of later-generation varieties relative to what is possible using traditional breeding approaches.

Finally, the acceleration in energy crop development and improvement through genomic selection (Objective 3) would have a substantial impact on the wider society. More specifically, time- and cost-effective production of biomass with reduced recalcitrance to fuel conversion can contribute to reducing dependency on fossil fuels and mitigating climate change. Furthermore, the effective dissemination of this research can increase the public awareness and improve confidence in green biotechnology, thereby laying the foundation for a future knowledge-based bioeconomy.