Oat evolution revealed in the maternal lineages of 25 Avena species

Abstract

Cultivated hexaploid oat has three different sets of nuclear genomes (A, C, D), but its evolutionary history remains elusive. A multiplexed shotgun sequencing procedure was explored to acquire maternal phylogenetic signals from chloroplast and mitochondria genomes of 25 Avena species. Phylogenetic analyses of the acquired organelle SNP data revealed a new maternal pathway towards hexaploids of oat genome evolution involving three diploid species (A. ventricosa, A. canariensis and A. longiglumis) and two tetraploid species (A. insularis and A. agadiriana). Cultivated hexaploid A. sativa acquired its maternal genome from an AC genome tetraploid close to A. insularis. Both AC genome A. insularis and AB genome A. agadiriana obtained a maternal genome from an ancient A, not C, genome diploid close to A. longiglumis. Divergence dating showed the major divergences of C genome species 19.9-21.2 million years ago (Mya), of the oldest A genome A. canariensis 13-15 Mya, and of the clade with hexaploids 8.5-9.5 Mya. These findings not only advance our knowledge on oat genome evolution, but also have implications for oat germplasm conservation and utilization in breeding.

Figure 1

Phylogenetic trees of 25 oat species with branch length and support and with wheat as an outgroup. They were inferred using BEAST software based on 6329 chloroplast (cp) (A) and 6343 mitochondrial (mt) (B) SNP data sets. The branch lengths are shown above the branches and branch supports at nodes are posterior probability. Three major clades (I, II, III) are highlighted and labeled on each tree. The branch for A. agadiriana and A. longiglumis closest to Clades II and III is also highlighted.

Figure 2

Oat genome relationships as revealed with the Bayesian density trees for three specific groups of oat species. They were inferred using BEAST software based on 6329 chloroplast (cp), 6343 mitochondrial (mt) and 12,672 combined (cpmt) SNP data sets. The major concerned species are highlighted in red bar among three data sets for each set of oat samples for ease of comparisons.

Figure 3

Phylogenetic trees of 25 oat species with branch support, node age and an outgroup of wheat. These MCC trees were obtained using BEAST software based on 12,672 combined cp and mt SNP data set. The values above the branch are posterior probability and the node ages are calibrated with the wheat-oat divergence of 25 Mya. Three major clades (I, II, III) are highlighted and labelled. The branch for A. agadiriana and A. longiglumis closest to Clade II is also highlighted.

Figure 4

Proposed scenario for the maternal origins of hexaploid oat with the extant Avena species based on the organelle phylogenetic signals. Cultivated hexaploid A. sativa acquired its maternal genome from an AC genome tetraploid close to A. insularis, highlighted in red. Both AC genome A. insularis and AB genome A. agadiriana obtained a maternal genome from an ancient A genome diploid close to A. longiglumis in red. Ac genome A. canariensis and AB genome A. agadiriana, highlighted in blue, are the oldest living species also likely contributing to the maternal genome of tetraploid and hexaploid, respectively. The paternal genome contributors of diploids to tetraploid and hexaploid are also reasoned based on existing literature in oat evolution in combination with the revealed oat genome relationships. Note that AC or AB genome designations may be renamed as CD genome based on the findings of Yan et al. to minimize the confusion on oat genome evolution. Multiple tetraploidziation and hexaploidization events occurred and are shown with the upper limits of age inferred from the divergence of A. ventricosa and the clade II leading to hexaploid oat, respectively (see Fig. 3).