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Title: Multiple polyploidy events in the early radiation of nodulating and non-nodulating legumes

Author
item Cannon, Steven
item MCKAIN, MICHAEL - University Of Georgia
item HARKESS, ALEX - University Of Georgia
item NELSON, MATTHEW - University Of Western Australia
item DASH, SUDHANSU - Iowa State University
item DEYHOLOS, MICHAEL - University Of Alberta
item PENG, YANHUI - University Of Tennessee
item JOYCE, BLAKE - University Of Tennessee
item STEWART, CHARLES - University Of Tennessee
item ROLF, MEGAN - Danforth Plant Science Center

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/17/2014
Publication Date: 11/6/2014
Citation: Cannon, S.B., McKain, M.R., Harkess, A., Nelson, M.N., Dash, S., Deyholos, M.K., Peng, Y., Joyce, B., Stewart, C.N., Rolf, M., Kutchan, T., Xuemei, T., Chen, C., Zhang, Y., Carpenter, E., Wong, G., Doyle, J., Leebens-Mack, J. 2014. Multiple polyploidy events in the early radiation of nodulating and non-nodulating legumes. Molecular Biology and Evolution. 32(1):193-210. DOI: 10.1093/molbev/msu296.

Interpretive Summary: The legume plant family, which contains soybeans, common beans, peas, lentils, clovers and many other crop species, derives much of its value from the ability of these plants to create (or "fix") their own nitrogen fertilizer through association with nitrogen-fixing soil bacteria. Not all species in this large plant family have this capacity, however. To better understand how this special ability arose, this project derived and analyzed the nearly complete set of gene sequences from 20 diverse legume species: 12 that do fix nitrogen and 8 that do not -- and also from 19 more distant relatives outside the legume family. A major finding is that four separate, early-diverging lineages in the legumes were independently affected by whole-genome doublings (genetic events that result in twice as many chromosomes as the progenitors). This is interesting in that it helps explain the chromosome numbers observed across the whole plant family. Further, the ability to fix nitrogen appears to have arisen independently twice, in two of the four lineages that experienced the chromosome doublings. This work provides a partial explanation for the evolution of this complex and important capacity: the ability that some plants have (along with a few of their bacterial "friends"), to produce their own nitrogen fertilizer.

Technical Abstract: Unresolved questions about evolution of the large and diverse legume family include the timing of polyploidy (whole-genome duplication; WGDs) relative to the origin of the major lineages within the Fabaceae and to the origin of symbiotic nitrogen fixation. Previous work has established that a WGD affects most lineages in the Papilionoideae and occurred sometime after the divergence of the papilionoid and mimosoid clades, but the exact timing has been unknown. The history of WGD has also not been established for legume lineages outside the Papilionoideae. We investigated the presence and timing of WGDs in the legumes by querying thousands of phylogenetic trees constructed from transcriptome and genome data from 20 diverse legumes and 16 outgroup species. The timing of duplications in the gene trees indicates that the papilionoid WGD occurred in the common ancestor of all papilionoids. The earliest diverging lineages of the Papilionoideae include both nodulating taxa such as the genistoids (e.g. lupin), dalbergioids (e.g. peanut), phaseoloids (e.g. beans), and galegoids (= Hologalegina, e.g. clovers), and clades with non-nodulating taxa including Xanthocercis and Cladrastis (evaluated in this study). We also found evidence for several independent WGDs near the base of other major legume lineages, including the Mimosoid-Cassiinae-Caesalpinieae (MCC), Detarieae, and Cercideae clades. Nodulation is found in the MCC and papilionoid clades, both of which experienced ancestral WGDs. However, there are numerous non-nodulating lineages in both clades, making it unclear whether the phylogenetic distribution of nodulation is due to independent gains or a single origin followed by multiple losses.