|DVORAK, JAN - University Of California, Davis|
|WANG, LE - University Of California, Davis|
|ZHU, TINGTING - University Of California, Davis|
|JORGENSEN, CHAD - University Of California, Davis|
|DAI, XIONGTAO - University Of California, Davis|
|MULLER, HANS-GEORG - University Of California, Davis|
|LUO, MING-CHENG - University Of California, Davis|
|DEHGHANI, HAMID - University Of California, Davis|
|SALZBERG, STEVEN - Johns Hopkins University School Of Medicine|
|GILL, BIKRAM - Kansas State University|
|DISTELFELD, ASSAF - Tel Aviv University|
|DEVOS, KATRIEN - University Of Georgia|
|BENNETZEN, JEFFREY - University Of Georgia|
|YOU, FRANK - Agriculture And Agri-Food Canada|
|MCGUIRE, PATRICK - University Of California, Davis|
Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/8/2018
Publication Date: 5/16/2018
Citation: Dvorak, J., Wang, L., Zhu, T., Jorgensen, C.M., Dai, X., Muller, H., Luo, M., Dehghani, H., Gu, Y.Q., Salzberg, S., Gill, B.S., Distelfeld, A., Devos, K.M., Bennetzen, J.L., You, F.M., McGuire, P.E. 2018. Structural variation and rates of genome evolution in the grass family seen through comparison of sequences of genomes greatly differing in size. Plant Journal. 95(3):487-503. https://doi.org/10.1111/tpj.13964.
Interpretive Summary: Genome sizes in flowering plants vary greatly, often within a single family. In the grass family, tropical and subtropical grasses tend to have small genomes whereas temperate grasses including wheat and barley tend to have large genomes with high contents of repetitive DNA. It has been hypothesized that the large content of repeated sequences in the large genomes is accompanied by rapid genomic/sequence changes, such as rearrangement of gene order, gene duplication and deletions, and evolution of genes with new functions. In this study, recently published genome sequences of wild emmer wheat, the wild progenitor of the wheat A and B genomes, and Tausch’s goatgrass (Aegilop tauschii), the wild progenitor of the wheat D genome, were employed to study the sequence evolution in three highly related large genomes. Our results suggest that in addition to the mechanisms associated with the large amounts of highly repetitive sequences in the large genomes, the acceleration in the rate of their evolution can also be attributed to the shortening of generation times when the ancestors of wild emmer and Ae. tauschii transitioned from perennial to annual growth habits.
Technical Abstract: Most temperate grasses in the subfamily Pooideae have large genomes with large quantities of transposable elements, leading to the speculation that this makes the genomes prone to rapid evolution. Recently published genome sequences of wild emmer, the wild progenitor of the wheat A and B genomes, and Aegilops tauschii, the wild progenitor of the wheat D genome, made it possible for the first time to compare the structure and evolution of grass genomes greatly differing in size. High-confidence genes annotated in the large Ae. tauschii genome were used as queries in homology searches against genes annotated in the pseudomolecules of the large and complex A and B genomes of wild emmer, and the pseudomolecules of the small genomes of Brachypodium distachyon, rice, and sorghum. A total of 2,275 rearrangements in gene order, primarily paracentric inversions, was discovered. In all six genomes, the densities of paracentric inversion lengths were approximated by negative exponential functions. The rates of genome evolution in terms of the numbers of rearrangements per million years (MY) were estimated for each branch of a grass phylogenetic tree. The rates were low in the rice and sorghum branches and elevated in all Pooideae branches, including that of B. distachyon, which has a small genome. The rates accelerated further in the tribe Triticeae. Paracentric inversions were employed in testing the hypothesis that the Ae. tauschii lineage is a hybrid of the A- and B-genome lineages. The hypothesis was rejected in favor of evolution of the three genomes by bifurcations. Two of the three breakpoints in the rearranged wheat chromosome 4A that produced pericentric and paracentric inversions and interchange T(4AL;7BS) contain satellite DNA. We suggest that three of the four breakpoints or all four breakpoints in 4A and 7B occurred simultaneously. The precipitous increase in the rate of evolution of the three large Triticeae genomes is of a recent origin. We attribute this acceleration in the rate of genome evolution to the shortening of generation time due to evolution of the annual growth habit in wild emmer and Ae. tauschii. The annual growth habit may also account for the moderately fast evolution of the small B. distachyon genome.