Synteny analysis in Rosids with a walnut physical map reveals slow genome evolution in long-lived woody perennials

Authors: LOU, MING-CHENG - University Of California; YOU, FRANK - Agriculture And Agri-Food Canada; LI, PINGCHUAN - Agriculture And Agri-Food Canada; WANG, JI-RUI - Sichuan Agricultural University; ZHUE, TINGTING - University Of California; DANDEKAR, ABHAYA - University Of California; LESLIE, CHARLES - University Of California; Aradhya, Mallikarjuna; MCGUIRE, PATRICK - University Of California; DVORAK, JAN - University Of California

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/9/2015
Publication Date: 9/17/2015
Publication URL: http://www.ars-grin.gov/dav
Citation: Lou, M., You, F.M., Li, P., Wang, J., Zhue, T., Dandekar, A.M., Leslie, C.A., Aradhya, M.K., Mcguire, P.E., Dvorak, J. 2015. Synteny analysis in Rosids with a walnut physical map reveals slow genome evolution in long-lived woody perennials. Biomed Central (BMC) Genomics. 16:707. doi: 10.1186/s12864-015-1906-5.

Interpretive Summary: Mutations often accompany DNA replication. Since there may be fewer cell cycles per year in the germlines of long-lived than short-lived angiosperms, the genomes of long-lived angiosperms may be diverging more slowly than those of short-lived angiosperms. Here we test this hypothesis. We first constructed a genetic map for walnut, a woody perennial. All linkage groups were short, and recombination rates were greatly reduced in the centromeric regions. We then used the genetic map to construct a walnut bacterial artificial chromosome (BAC) clone-based physical map, which contained 15,203 exonic BAC-end sequences, and quantified with it synteny between the walnut genome and genomes of three long-lived woody perennials, Vitis vinifera, Populus trichocarpa, and Malus domestica, and three short-lived herbs, Cucumis sativus, Medicago truncatula, and Fragaria vesca. Each measure of synteny we used showed that the genomes of woody perennials were less diverged from the walnut genome than those of herbs. We also estimated the nucleotide substitution rate at silent codon positions in the walnut lineage. It was one-fifth and one-sixth of published nucleotide substitution rates in the Medicago and Arabidopsis lineages, respectively. We uncovered a whole-genome duplication in the walnut lineage, dated it to the neighborhood of the Cretaceous-Tertiary boundary, and allocated the 16 walnut chromosomes into eight homoeologous pairs. We pointed out that during Polyploidydysploidy cycles, the dominant tendency is to reduce the chromosome number. Slow rates of nucleotide substitution are accompanied by slow rates of synteny erosion during genome divergence in woody perennials.

Technical Abstract: Mutations often accompany DNA replication. Since there may be fewer cell cycles per year in the germlines of long-lived than short-lived angiosperms, the genomes of long-lived angiosperms may be diverging more slowly than those of short-lived angiosperms. Here we test this hypothesis. We first constructed a genetic map for walnut, a woody perennial. All linkage groups were short, and recombination rates were greatly reduced in the centromeric regions. We then used the genetic map to construct a walnut bacterial artificial chromosome (BAC) clone-based physical map, which contained 15,203 exonic BAC-end sequences, and quantified with it synteny between the walnut genome and genomes of three long-lived woody perennials, Vitis vinifera, Populus trichocarpa, and Malus domestica, and three short-lived herbs, Cucumis sativus, Medicago truncatula, and Fragaria vesca. Each measure of synteny we used showed that the genomes of woody perennials were less diverged from the walnut genome than those of herbs. We also estimated the nucleotide substitution rate at silent codon positions in the walnut lineage. It was one-fifth and one-sixth of published nucleotide substitution rates in the Medicago and Arabidopsis lineages, respectively. We uncovered a whole-genome duplication in the walnut lineage, dated it to the neighborhood of the Cretaceous-Tertiary boundary, and allocated the 16 walnut chromosomes into eight homoeologous pairs. We pointed out that during Polyploidydysploidy cycles, the dominant tendency is to reduce the chromosome number. Slow rates of nucleotide substitution are accompanied by slow rates of synteny erosion during genome divergence in woody perennials.