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Title: The impact of polyploidy on the evolution of a complex NB-LRR resistance gene cluster in soybean

item ASHFIELD, TOM - Indiana University
item EGAN, ASHLEY - East Carolina University
item PFEIL, BERNARD - Cornell University - New York
item CHEN, NICHOLAS - University Of Paris
item RATNAPARKHE, MILIND - Virginia Polytechnic Institution & State University
item AMELINE-TORREGROSA, CARINE - University Of Minnesota
item DENNY, R. - University Of Minnesota
item Cannon, Steven
item DOYLE, JEFF - Cornell University - New York
item GEFFROY, VALERIE - University Of Paris
item ROE, BRUCE - University Of Oklahoma
item MAROOF, M.A. - Virginia Polytechnic Institution & State University
item YOUNG, NEVIN - University Of Minnesota
item INNES, ROGER - Indiana University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/22/2012
Publication Date: 3/28/2012
Citation: Ashfield, T., Egan, A.N., Pfeil, B.E., Chen, N.W., Ratnaparkhe, M.B., Ameline-Torregrosa, C., Denny, R., Cannon, S.B., Doyle, J.J., Geffroy, V., Roe, B.A., Maroof, M.S., Young, N.D., Innes, R.W. 2012. The impact of polyploidy on the evolution of a complex NB-LRR resistance gene cluster in soybean. Plant Physiology. DOI:10.1104/CS.112.195040.

Interpretive Summary: A key problem in plant biology is to understand how plants defend against pathogens and pests, and how plants evolve to try to stay ahead in the "arms race" against these foes. The sentinels in the plant immune system are a group of proteins, derived from genes called "NB-LRR disease resistance genes", that can recognize attackers or can recognize the symptoms of those attacks. This paper follows the evolution of a group of NB-LRR genes in soybean and soybean's wild relatives, and in common bean; and reports how these genes have changed over the course of several million years of pathogen pressure. Among the findings are that related genes in the corresponding regions in these plants have recombined within these species to provide new disease resistance capabilities, and that many new copies and variants of the genes have arisen in common bean through gene duplications. Also, in soybean, a whole-genome duplication that occurred several million years ago (but after soybean and common bean diverged), gave rise to two clusters of these disease resistance genes; but only one of these clusters has been expanding, while the other has been decaying and losing genes. These results give plant breeders new tools for breeding soybean and bean varieties that can fend off certain races of bacterial blight and some viral and fungal pathogens.

Technical Abstract: A comparative genomics approach was used to investigate the evolution of a complex NB-LRR gene cluster found in soybean (Glycine max), common bean (Phaseolus vulgaris), and other legumes. In soybean, the cluster is associated with several disease resistance (R) genes of known function including Rpg1b, an R gene effective against some races of bacterial blight. We show that local duplications/deletions, recombination, and positive selection are all driving the evolution of the NB-LRR family in this region. Analysis of different domains of these NB-LRR genes revealed that the N-terminal coiled-coil (CC) domain, central nucleotide binding (NB-ARC), and C-terminal leucine-rich repeat (LRR) domains have undergone distinct evolutionary paths. Sequence exchanges within the NB-ARC domain were rare. In contrast, inter-paralogue exchanges involving the CC and LRR domains were common, consistent with both of these regions co-evolving with pathogens. Residues under positive selection were over-represented within the predicted solvent-exposed face of the LRR domain, although several were also detected within the NB-ARC domain. Superimposition of these residues on a prediction of the tertiary structure of the NB-ARC domain reveals that the majority are located on the surface, suggestive of a role in interactions with other domains or proteins. Following polyploidy in the Glycine lineage, NB-LRR genes have been preferentially lost from one of the duplicated chromosomes (homoeologues), and there appears to have been little to no sequence exchange between NB-LRR genes on separate homoeologues. The NB-LRR cluster in homoeologue 2 resides in a pericentromeric region and contains only three intact paralogues, all belonging to one ancestral NB-ARC lineage, interspersed with many NB-LRR gene fragments. In contrast, the majority of paralogues in homoeologue 1 are intact and several lineages are represented. The single orthologous region in Phaseolus contains at least as many intact paralogues as found in the two Glycine homoeologues combined, at least partially due to an increased rate of local duplications. We conclude that while polyploidization in Glycine has not driven a stable increase in family size for NB-LRR genes derived from the ancestral Rpg1b cluster, it has generated two recombinationally isolated clusters, one of which appears to be in the process of decay.