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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.

SUBMITTER: Liu Q

PROVIDER: S-EPMC5291219 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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

Liu Qing Q Lin Lei L Zhou Xiangying X Peterson Paul M PM Wen Jun J

Scientific reports 20170203

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 cr ...[more]

PMID: 28157193

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Project description:BACKGROUND:Oat (Avena sativa L.) is a recognized health-food, and the contributions of its different candidate A-genome progenitor species remain inconclusive. Here, we report chloroplast genome sequences of eleven Avena species, to examine the plastome evolutionary dynamics and analyze phylogenetic relationships between oat and its congeneric wild related species. RESULTS:The chloroplast genomes of eleven Avena species (size range of 135,889-135,998?bp) share quadripartite structure, comprising of a large single copy (LSC; 80,014-80,132?bp), a small single copy (SSC; 12,575-12,679?bp) and a pair of inverted repeats (IRs; 21,603-21,614?bp). The plastomes contain 131 genes including 84 protein-coding genes, eight ribosomal RNAs and 39 transfer RNAs. The nucleotide sequence diversities (Pi values) range from 0.0036 (rps19) to 0.0093 (rpl32) for ten most polymorphic genes and from 0.0084 (psbH-petB) to 0.0240 (petG-trnW-CCA) for ten most polymorphic intergenic regions. Gene selective pressure analysis shows that all protein-coding genes have been under purifying selection. The adjacent position relationships between tandem repeats, insertions/deletions and single nucleotide polymorphisms support the evolutionary importance of tandem repeats in causing plastome mutations in Avena. Phylogenomic analyses, based on the complete plastome sequences and the LSC intermolecular recombination sequences, support the monophyly of Avena with two clades in the genus. CONCLUSIONS:Diversification of Avena plastomes is explained by the presence of highly diverse genes and intergenic regions, LSC intermolecular recombination, and the co-occurrence of tandem repeat and indels or single nucleotide polymorphisms. The study demonstrates that the A-genome diploid-polyploid lineage maintains two subclades derived from different maternal ancestors, with A. longiglumis as the first diverging species in clade I. These genome resources will be helpful in elucidating the chloroplast genome structure, understanding the evolutionary dynamics at genus Avena and family Poaceae levels, and are potentially useful to exploit plastome variation in making hybrids for plant breeding.

Project description:BACKGROUND AND AIMS:Natural hybridization was investigated between two predominantly allohexaploid wheatgrasses, weedy Elytrigia repens and steppic E. intermedia, with respect to habitats characterized by different degrees of anthropogenic disturbance. METHODS:Using flow cytometry (relative DNA content), 269 plants from three localities were analysed. Hybrids were further analysed using nuclear ribosomal (ITS1-5.8S-ITS2 region) and chloroplast (trnT-F region) DNA markers in addition to absolute DNA content and chromosome numbers. KEY RESULTS:Weedy E. repens was rare in a steppic locality whereas E. intermedia was almost absent at two sites of agricultural land-use. Nevertheless, hybrids were common there whereas none were found at the steppic locality, underlining the importance of different ecological conditions for hybrid formation or establishment. At one highly disturbed site, > 16 % of randomly collected plants were hybrids. Hexaploid hybrids showed intermediate genome size compared with the parents and additive patterns of parental ITS copies. Some evidence of backcrosses was found. The direction of hybridization was highly asymmetric as cpDNA identified E. intermedia as the maternal parent in 61 out of 63 cases. Out of nine nonaploid cytotypes (2n = 9x = 63) which likely originated by fusion of unreduced and reduced gametes of hexaploids, eight were hybrids whereas one was a nonaploid cytotype of E. repens. The progeny of one nonaploid hybrid demonstrated gene flow between hexaploid and nonaploid cytotypes. CONCLUSIONS:The results show that E. repens and E. intermedia frequently cross at places where they co-occur. Hybrid frequency is likely influenced by habitat type; sites disturbed by human influence sustain hybrid formation and/or establishment. Hexaploid and nonaploid hybrid fertility is not negligible, backcrossing is possible, and the progeny is variable. The frequent production of new at least partially fertile cyto- and genotypes provides ample raw material for evolution and adaptation.

Dataset Information

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

Publications

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

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