Unraveling the evolutionary dynamics of ancient and recent polyploidization events in Avena (Poaceae)

Abstract

Understanding the diversification of polyploid crops in the circum-Mediterranean region is a challenging issue in evolutionary biology. Sequence data of three nuclear genes and three plastid DNA fragments from 109 accessions of Avena L. (Poaceae) and the outgroups were used for maximum likelihood and Bayesian analyses. The evolution of cultivated oat (Avena sativa L.) and its close relatives was inferred to have involved ancient allotetraploidy and subsequent recent allohexaploidy events. The crown ages of two infrageneric lineages (Avena sect. Ventricosa Baum ex Romero-Zarco and Avena sect. Avena) were estimated to be in the early to middle Miocene, and the A. sativa lineages were dated to the late Miocene to Pliocene. These periods coincided with the mild seasonal climatic contrasts and the Mediterranean climate established in the Mediterranean Basin. Our results suggest that polyploidy, lineage divergence, and complex reticulate evolution have occurred in Avena, exemplifying the long-term persistence of tetraploids and the multiple origins of hexaploids related to paleoclimatic oscillations during the Miocene-Pliocene interval in the circum-Mediterranean region. This newly-resolved infrageneric phylogenetic framework represents a major step forward in understanding the origin of the cultivated oat.

Figure 1. The diversification centre for 28 species of Avena (only A. abyssinica in eastern Africa and western Asia) in the Mediterranean Basin using software Adobe Photoshop CS6.

The background map was downloaded from http://www.ngdc.noaa.gov/mgg/global/global.html (Amante C, Eakins BW. ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis. NOAA Technical Memorandum NESDIS NGDC-24. National Geophysical Data Center, NOAA. Doi:10.7289/V5C8276M, March 2009).

Figure 2. Maximum likelihood tree of Avena inferred from nuclear ppcB1 data including three clades (A-PPI in red, A’C-PPI in green, and A’C-PPIII in light green) and two nodes (AB-PPI in blue and A’C-PPII in dark green).

Branch thickness indicate maximum likelihood bootstrap support/Bayesian posterior probability (MLBS/PP): thickest solid = MLBS ≥ 90% and PP ≥ 0.90; thickest shadow = MLBS ≥ 90% or PP ≥ 0.90; thick solid = 89% ≥ MLBS ≥ 70% and 0.89 ≥ PP ≥ 0.70; thick shadow = 89% ≥ MLBS ≥ 70% or 0.89 ≥ PP ≥ 0.70; and thin solid = 69% ≥ MLBS ≥ 50% and 0.69 ≥ PP ≥ 0.50). Red, orange, and black of terminal symbols (circle, square, and star for different accessions) represent thrice, twice, and once clade/node appearance of the cultivated oat. Terminal taxon names and branch support values are shown in Figs S1–S3.

Figure 3. Maximum likelihood tree of Avena inferred from nuclear GBSSI data including three clades (AB-GBI in blue, A’C-GBI in green, and AB&A’C-GBI in brown) plus eight polyploids in unmarked black.

Explanation of branch thickness and colorful terminal symbols refer to Fig. 2. Terminal taxon names and branch support values are shown in Figs S4–S6.

Figure 4. Bayesian inference phylogram of Avena inferred from nuclear GBSSI data including four clades (AB-GBI in light blue, AB-GBII in blue, A’C-GBI in green, and A’C-GBII in green) plus eight polyploids in unmarked black.

Explanation of branch thickness and colorful terminal symbols refer to Fig. 2. Taxon names and branch support value are shown in Figs S7–S10.

Figure 5. Maximum likelihood tree of Avena inferred from nuclear gpa1 data including seven clades (A-GPI in red, C-GPI in brown, AB-GPI in light blue, AB-GPII in blue, A’C-GPI in green, A’C-GPII in dark green, and A’C-GPIII in light green).

Explanation of branch thickness and colorful terminal symbols refer to Fig. 2. Taxon names and branch support value are shown in Fig. S11.

Figure 6. Chronogram of Avena and its close relatives based on plastid (ndhA intron, rpl32-trnL, and rps16 intron) data including two clades (C-NRR and A’C-NRR + AB-NRR) inferred from BEAST. Numbers above the branches are MLBS/PP.

Taxon labels are in the format: Avena vaviloviana-Liu351 (4x), where Avena vaviloviana indicates that the sequence belongs to the species; Liu351 indicates voucher; (4x) indicates that the species is tetraploid. Coloured taxon labels correspond to sections. Node number indicates the lineages of interest (Table S4).