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Background Avena longiglumis Durieu (2n = 2x = 14) is a wild relative of cultivated oat (Avena sativa, 2n = 6x = 42) with good agronomic and nutritional traits. The plant mitochondrial genome has a complex organization and carries genetic traits of value in exploiting genetic resources, not least male sterility alleles used to generate F1 hybrid seeds. Therefore, we aim to complement the chromosomal-level nuclear and chloroplast genome assemblies of A. longiglumis with the complete assembly of the mitochondrial genome (mitogenome) based on Illumina and ONT long reads, comparing its structure with Poaceae species. Results The complete mitochondrial genome of A. longiglumis can be represented by one master circular genome being 548,445 bp long with a GC content of 44.05%. It can be represented by linear or circular DNA molecules (isoforms or contigs), with multiple alternative configurations mediated by long (4,100–31,235 bp) and medium (144–792 bp) size repeats. Thirty-five unique protein-coding genes, three unique rRNA genes, and 11 unique tRNA genes are identified. The mitogenome is rich in duplications (up to 233 kb long) and multiple tandem or simple sequence repeats, together accounting for more than 42.5% of the total length. We identify homologous sequences between the mitochondrial, plastid and nuclear genomes, including the exchange of eight plastid-derived tRNA genes, and nuclear-derived retroelement fragments. At least 85% of the mitogenome is duplicated in the A. longiglumis nuclear genome. We identify 269 RNA editing sites in mitochondrial protein-coding genes including stop codons truncating ccmFC transcripts. Conclusions Comparative analysis with Poaceae species reveals the dynamic and ongoing evolutionary changes in mitochondrial genome structure and gene content. The complete mitochondrial genome of A. longiglumis completes the last link of the oat reference genome and lays the foundation for oat breeding and exploiting the biodiversity in the genus.

BackgroundOat (Avena sativa, 2n=6x=42) is an important crop, and with its wild relatives including A. longiglumis (ALO, 2n=6x=14), has advantageous agronomic and nutritional traits. A de-novo chromosome-level ALO genome assembly was made to investigate diversity and structural genome variation between Avena species and other Poaceae in an evolutionary context, and develop genomic resources to identify the pangenome and economic traits within Pooideae.ResultsThe 3.85 gigabase ALO genome (seven pseudo-chromosomes), contained 40,845 protein-coding genes and 87% repetitive sequences (84.21% transposable elements). An LTR retrotransposon family was abundant at all chromosome centromeres, and genes were distributed without major terminal clusters. Comparisons of synteny with A. eriantha and A. strigosa showed evolutionary translocations of terminal segments including many genes. Comparison with rice (x=12) and the ancestral grass karyotype showed synteny and features of chromosome evolution including fusions, translocations and insertions of syntenic blocks across Pooideae species. With a genome size 10 times larger than rice, ALO showed relatively uniform expansion along the chromosome arms, with few gene-poor regions along arms, and no major duplications nor deletions. Linked gene networks were identified (mixed-linkage glucans and cellulose synthase genes), and CYP450 genes may be related to salt-tolerance.ConclusionsThe high-continuity genome assembly shows gene, chromosomal structural and copy number variation, providing a reference for the Avena pangenome, defining the full spectrum of diversity. Chromosomal rearrangements and genome expansion demonstrate features of evolution across the genus and grass BOP-clade, contributing to exploitation of gene and genome diversity through precision breeding.