Oat domestication - understanding the origin of a European cereal

Oats can claim to be the only 'European' cereal. Previous work indicated that its closest wild relatives are found around Turkey near sites where wheat and barley were first domesticated, but archaeological evidence points to first use as a crop only late in the development of agriculture and then in Central Europe, rather than in its original environment. A plausible explanation for this transfer is that a population of the wild relative (Avena sterilis), which colonises broken ground, had become adapted to life as an agricultural weed. The new weed (A. fatua) is less able to spread in the wild but is very successful at colonising tilled fields of cereals such as barley. A. fatua could have spread across Europe with those crops and then become a crop in its own right in hard times where others failed. Indeed, oats have traditionally been grown on poor ground and at the end of rotations when soil fertility is low, a possible legacy of this secondary domestication. At some stage completely non-shattering oats would have been selected for easier grain harvest and storage, and greater pressure would have been applied for full domestication (loss of awns, larger grain size and so on).
A complication for this model is that oats appear to have been domesticated twice. Most cultivars now resemble 'white' oats (A. sativa), sown in the spring and most closely related to wild populations in central Turkey. However, around the Mediterranean, traditional landraces are often 'red' oats (A. byzantina), sown in autumn and most closely related to wild populations in south western Turkey. Modern breeding programmes are largely based on crosses between these two types, and the UK's unique winter oat cultivars may be particularly dependent on A. byzantina traits. We have a strong interest in understanding the origin of both red and white oats, and the role of A. fatua. This is not only driven by curiosity about the development of agriculture but also by the need to add new variation to the modern crop. Each domestication step has created genetic bottlenecks where potentially valuable germplasm has been lost. Better understanding of these bottlenecks, and of natural variation in wild populations, will help find useful variation to incorporate into breeding programmes.
Genotyping-by-sequence (GbS) is a recent high throughput method to reveal genetic variation across entire genomes. It samples short sequences adjacent to specific restriction enzyme sites, and does not require prior knowledge of which variants are present. Hundreds of samples may be processed, making it ideal for diversity screens. We have panels of over 500 weedy, wild and landrace accessions already screened by GbS. Unfortunately, the oat genome is almost as large and complex as that of wheat, and no reference is yet available to associate GbS tags with neighbouring genes. Even when the first references become available (expected in 2018), they will have been derived from modern cultivars which may differ from the ancestral stocks we are studying. In this project we will bridge the gap between GbS and genome references to assess gene variation either directly or by improving the references available. In the first step we will use a newly developed sequencing approach to cut the cost of building a red oat reference. In the second we will work with a German barley expert who developed exome capture, a method that samples and sequences only targeted gene regions, and with a Canadian partner who has created an exome capture for oats, based in part on our genome data. We will use an improved design to recover comprehensive collections of gene sequences from 220 key GbS panel accessions. Finally we will obtain sequence from progenitors that will allow comparisons of gene content and order with modern cultivars, and will enhance analysis of exome and GbS data. Working with a Polish partner who has created hybrid populations, we will identify key genes underpinning domestication.

The project will establish a reliable reference genome for Avena byzantina, one of the two major lineages of cultivated oats, and will use exome capture to identify the most significant changes in genetic diversity that have occurred during the development of modern elite cultivars from wild hexaploids. Capture panels will include wild, weedy, landrace and early cultivar accessions. The data will clarify the origins of the two cultivated oat lineages (A. sativa ss and A. byzantina) and the role of the weed species A. fatua in the emergence of the oat crop in late Neolithic Europe. Resequencing of A. sterilis and A. fatua accessions will provide a full spectrum of gene content across the primary gene pool available for oat breeding.

We will work as part of an international consortium which will provide an exceptional combination of in-kind expertise and resources. An open source bioinformatics pipeline will be used to reduce the cost of assembling the complex (13Gb) hexaploid Avena genome, and increase the accessibility of pan-genome approaches for minor crops. Our exome capture panel is intended to complement work carried out in other public good programmes, and will inform strategies to recover the most valuable germplasm for use in current oat breeding programmes, while characterisation of the secondary domestication process(es) will be of interest to other temperate cereal programmes seeking to improve resilience in modern highly inbred crops.

Oats have played a significant role in British agriculture for hundreds of years, and are traditionally grown on poorer land or at the end of rotations. As such they have also traditionally been seen as a low value crop. However, it is now widely appreciated that they may form a beneficial component of human diets, having positive effects on satiety, so reducing calorie intake, and providing significant intake of fibre including beta-glucans, which improve gut health and contribute to a lowering of blood cholesterol. Health claims have been approved by the FDA and EFSA and are widely promoted by producers. As a consequence the proportion of oats grown for milling and human use has increased greatly in recent years, and now forms the main use of the crop. This has also contributed to a significant reversal in the decline of the crop that had inevitably followed the loss of animal feed markets wth the introduction of mechanisation in the last century.

There is now an urgent need to revitalise oat breeding as the crop is struggling to maintain production even in the face of this increasing demand for profitable human consumption as food or in cosmetics. It is widely grown across Europe, although frequently on more traditional farms or by older generations of farmers, leading to fears that major producers such as Spain or Poland will abandon oats rather than adapt to more efficient methods. Loss of expertise and infrastructure such as mills is then difficult to reverse, as is being found in North America. Oats are a valuable part of rotations, however, with much unrealised potential both for human and animal use, and the UK leads the way in reversing the historic decline in oat production. The outputs from this proposal would contribute to the critical mass of research needed to introduce methods such as genomic selection into oat breeding, and to accelerate the (re-)introduction of unused variation from the very large numbers of landraces preserved in genebanks. We therefore believe that the project will have long term beneficial impacts (ie through improvements in new variety production) that will include more diverse and lower input agriculture, more sustainable animal feed production as oats substitute imported components and healthier functional foods as beneficial components become additional breeding targets.