Cultivated oat (Avena sativa L.) is an allohexaploid (AACCDD, 2n = 6x = 42) thought to have been domesticated more than 3,000 years ago while growing as a weed in wheat, emmer and barley fields in Anatolia1,2. Oat has a low carbon footprint, substantial health benefits and the potential to replace animal-based food products. However, the lack of a fully annotated reference genome has hampered efforts to deconvolute its complex evolutionary history and functional gene dynamics. Here we present a high-quality reference genome of A. sativa and close relatives of its diploid (Avena longiglumis, AA, 2n = 14) and tetraploid (Avena insularis, CCDD, 2n = 4x = 28) progenitors. We reveal the mosaic structure of the oat genome, trace large-scale genomic reorganizations in the polyploidization history of oat and illustrate a breeding barrier associated with the genome architecture of oat. We showcase detailed analyses of gene families implicated in human health and nutrition, which adds to the evidence supporting oat safety in gluten-free diets, and we perform mapping-by-sequencing of an agronomic trait related to water-use efficiency. This resource for the Avena genus will help to leverage knowledge from other cereal genomes, improve understanding of basic oat biology and accelerate genomics-assisted breeding and reanalysis of quantitative trait studies.

Oat (Avena sativa L.) is an important and nutritious cereal crop, and there is a growing need to identify genes that contribute to improved oat varieties. Here we utilize a newly sequenced and annotated oat reference genome to locate and characterize quantitative trait loci (QTLs) affecting agronomic and grain-quality traits in five oat populations. We find strong and significant associations between the positions of candidate genes and QTL that affect heading date, as well as those that influence the concentrations of oil and β-glucan in the grain. We examine genome-wide recombination profiles to confirm the presence of a large, unbalanced translocation from chromosome 1 C to 1 A, and a possible inversion on chromosome 7D. Such chromosome rearrangements appear to be common in oat, where they cause pseudo-linkage and recombination suppression, affecting the segregation, localization, and deployment of QTLs in breeding programs.

Oat is susceptible to several Fusarium species that cause contamination with different trichothecene mycotoxins. The molecular mechanisms behind Fusarium resistance in oat have yet to be elucidated. In the present work, we identified and characterised two oat UDP-glucosyltransferases orthologous to barley HvUGT13248. Overexpression of the latter in wheat had been shown previously to increase resistance to deoxynivalenol (DON) and nivalenol (NIV) and to decrease disease the severity of both Fusarium head blight and Fusarium crown rot. Both oat genes are highly inducible by the application of DON and during infection with Fusarium graminearum. Heterologous expression of these genes in a toxin-sensitive strain of Saccharomyces cerevisiae conferred high levels of resistance to DON, NIV and HT-2 toxins, but not C4-acetylated trichothecenes (T-2, diacetoxyscirpenol). Recombinant enzymes AsUGT1 and AsUGT2 expressed in Escherichia coli rapidly lost activity upon purification, but the treatment of whole cells with the toxin clearly demonstrated the ability to convert DON into DON-3-O-glucoside. The two UGTs could therefore play an important role in counteracting the Fusarium virulence factor DON in oat.

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SUMMARYWind, rain, herbivores, obstacles, neighbouring plants, etc. provide important mechanical cues to steer plant growth and survival. Mechanostimulation to stimulate yield and stress resistance of crops is of significant research interest, yet a molecular understanding of transcriptional responses to touch is largely absent in cereals. To address this, we performed whole‐genome transcriptomics following mechanostimulation of wheat, barley, and the recent genome‐sequenced oat. The largest transcriptome changes occurred ±25 min after touching, with most of the genes being upregulated. While most genes returned to basal expression level by 1–2 h in oat, many genes retained high expression even 4 h post‐treatment in barley and wheat. Functional categories such as transcription factors, kinases, phytohormones, and Ca2+ regulation were affected. In addition, cell wall‐related genes involved in (hemi)cellulose, lignin, suberin, and callose biosynthesis were touch‐responsive, providing molecular insight into mechanically induced changes in cell wall composition. Furthermore, several cereal‐specific transcriptomic footprints were identified that were not observed in Arabidopsis. In oat and barley, we found evidence for systemic spreading of touch‐induced signalling. Finally, we provide evidence that both the jasmonic acid‐dependent and the jasmonic acid‐independent pathways underlie touch‐signalling in cereals, providing a detailed framework and marker genes for further study of (a)biotic stress responses in cereals.