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Chloroplast Phylogenomic Analyses Resolve Multiple Origins of the Kengyilia Species (Poaceae: Triticeae) via Independent Polyploidization Events.

ABSTRACT: Kengyilia is a group of allohexaploid species that arose from two hybridization events followed by genome doubling of three ancestral diploid species with different genomes St, Y, and P in the Triticeae. Estimating the phylogenetic relationship in resolution of the maternal lineages has been difficult, owing to the extremely low rate of sequence divergence. Here, phylogenetic reconstructions based on the plastome sequences were used to explore the role of maternal progenitors in the establishment of Kengyilia polyploid species. The plastome sequences of 11 Kengyilia species were analyzed together with 12 tetraploid species (PP, StP, and StY) and 33 diploid taxa representing 20 basic genomes in the Triticeae. Phylogenomic analysis and genetic divergence patterns suggested that (1) Kengyilia is closely related to Roegneria, Pseudoroegneria, Agropyron, Lophopyrum, Thinopyrum, and Dasypyrum; (2) both the StY genome Roegneria tetraploids and the PP genome Agropyron tetraploids served as the maternal donors during the speciation of Kengyilia species; (3) the different Kengyilia species derived their StY genome from different Roegneria species. Multiple origins of species via independent polyploidization events have occurred in the genus Kengyilia, resulting in a maternal haplotype polymorphism. This helps explain the rich diversity and wide adaptation of polyploid species in the genus Kengyilia.

SUBMITTER: Chen S

PROVIDER: S-EPMC8377392 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Introgressive events (e.g., hybridization, gene flow, horizontal gene transfer) and incomplete lineage sorting of ancestral polymorphisms are a challenge for phylogenetic analyses since different genes may exhibit conflicting genealogical histories. Grasses of the Triticeae tribe provide a particularly striking example of incongruence among gene trees. Previous phylogenies, mostly inferred with one gene, are in conflict for several taxon positions. Therefore, obtaining a resolved picture of relationships among genera and species of this tribe has been a challenging task. Here, we obtain the most comprehensive molecular dataset to date in Triticeae, including one chloroplastic and 26 nuclear genes. We aim to test whether it is possible to infer phylogenetic relationships in the face of (potentially) large-scale introgressive events and/or incomplete lineage sorting; to identify parts of the evolutionary history that have not evolved in a tree-like manner; and to decipher the biological causes of gene-tree conflicts in this tribe. RESULTS:We obtain resolved phylogenetic hypotheses using the supermatrix and Bayesian Concordance Factors (BCF) approaches despite numerous incongruences among gene trees. These phylogenies suggest the existence of 4-5 major clades within Triticeae, with Psathyrostachys and Hordeum being the deepest genera. In addition, we construct a multigenic network that highlights parts of the Triticeae history that have not evolved in a tree-like manner. Dasypyrum, Heteranthelium and genera of clade V, grouping Secale, Taeniatherum, Triticum and Aegilops, have evolved in a reticulated manner. Their relationships are thus better represented by the multigenic network than by the supermatrix or BCF trees. Noteworthy, we demonstrate that gene-tree incongruences increase with genetic distance and are greater in telomeric than centromeric genes. Together, our results suggest that recombination is the main factor decoupling gene trees from multigenic trees. CONCLUSIONS:Our study is the first to propose a comprehensive, multigenic phylogeny of Triticeae. It clarifies several aspects of the relationships among genera and species of this tribe, and pinpoints biological groups with likely reticulate evolution. Importantly, this study extends previous results obtained in Drosophila by demonstrating that recombination can exacerbate gene-tree conflicts in phylogenetic reconstructions.

Dataset Information

Chloroplast Phylogenomic Analyses Resolve Multiple Origins of the Kengyilia Species (Poaceae: Triticeae) via Independent Polyploidization Events.

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