Genomic insights from the first chromosome-scale assemblies of oat (Avena spp.) diploid species

Abstract

Background: Cultivated hexaploid oat (Common oat; Avena sativa) has held a significant place within the global crop community for centuries; although its cultivation has decreased over the past century, its nutritional benefits have garnered increased interest for human consumption. We report the development of fully annotated, chromosome-scale assemblies for the extant progenitor species of the A_s- and C_p-subgenomes, Avena atlantica and Avena eriantha respectively. The diploid Avena species serve as important genetic resources for improving common oat's adaptive and food quality characteristics.

Results: The A. atlantica and A. eriantha genome assemblies span 3.69 and 3.78 Gb with an N50 of 513 and 535 Mb, respectively. Annotation of the genomes, using sequenced transcriptomes, identified ~ 50,000 gene models in each species-including 2965 resistance gene analogs across both species. Analysis of these assemblies classified much of each genome as repetitive sequence (~ 83%), including species-specific, centromeric-specific, and telomeric-specific repeats. LTR retrotransposons make up most of the classified elements. Genome-wide syntenic comparisons with other members of the Pooideae revealed orthologous relationships, while comparisons with genetic maps from common oat clarified subgenome origins for each of the 21 hexaploid linkage groups. The utility of the diploid genomes was demonstrated by identifying putative candidate genes for flowering time (HD3A) and crown rust resistance (Pc91). We also investigate the phylogenetic relationships among other A- and C-genome Avena species.

Conclusions: The genomes we report here are the first chromosome-scale assemblies for the tribe Poeae, subtribe Aveninae. Our analyses provide important insight into the evolution and complexity of common hexaploid oat, including subgenome origin, homoeologous relationships, and major intra- and intergenomic rearrangements. They also provide the annotation framework needed to accelerate gene discovery and plant breeding.

Keywords: Avena; Aveninae; Crown rust resistance; Flowering time; Hi-C; Oat; Polyploidy.

Fig. 1

Correlation between the physical and linkage map. The genetic position of mapped markers is plotted as a function of physical distance relative to the A. atlantica genome assembly. The linkage position of six unassigned scaffolds with multiple mapping markers is shown

Fig. 2

Genome overview of a A. atlantica and b A. eriantha. Track 1 (outside): Chromosome and sizes; Tracks 2: Annotated gene density; Track 3: Centromeric repeat density; Track 4: Telomeric sub-repeat density; Track 5: C-genome specific repeat (pAm1) density; Track 6: A-genome specific repeat (pAvKB26) density

Fig. 3

Identification of candidate genes putatively underlying heading date in oats. Candidate gene loci were identified using BLAST searches against the A. atlantica genome assembly using maker sequences associated with heading date QTLs located on the homoeologous linkage groups a Mrg12 and b Mrg02 (Bekele et al. [29]). Markers from both QTLs mapped to the same physical position on chromosome AA1, within an interval containing an FT-like protein (HD3A), suggesting that heading date in modern oat is controlled by two functional homoeologs of the flowering time gene

Fig. 4

Identification of candidate genes putatively underlying crown rust resistance in oats. Candidate gene loci were identified using BLAST searches against the A. atlantica genome assembly using maker sequences associated with crown rust QTLs located on hexaploid A. sativa linkage group Mrg18 reported by Klos et al. [30]. Mrg18 was previously shown to be involved with an intergenomic translocation involving 7C and 17A, corresponding to A. eriantha chromosome AE7 (blue) and A. atlantica chromosome AA2 (red)

Fig. 5

Abbreviated maximum likelihood tree generated using a 10,894 SNPs for C-genome diploids rooted to the A. atlantica (AT_Cc7277) reference and b 7221 SNPs for A-genome diploids rooted to the A. eriantha reference (ER_CN 19238). Asterisks denote percentage of 1000 bootstrap replicates that support the topology at 90–100% (gold) and 75–89% (blue). Scale bar represents substitutions per site. Branch labels are based on subgenome composition and, in some cases, diaspore morphology (“floret-shattering,” “spikelet-shattering,” or “cultivated”). Unabbreviated trees are provided as Additional file 15: Figure S7 and Additional file 16: Figure S8