An NBS-LRR protein in the Rpp1 locus negates the dominance of Rpp1-mediated resistance against Phakopsora pachyrhizi in soybean

Authors: WEI, WEI - University Of Illinois; WU, XING - University Of Illinois; GARCIA, ALEXANDRE - Tropical Melhoramento & Genética, Ltda; McCoppin, Nancy; GOMES VIANA, JOAO - University Of Illinois; MURAD, PRAERONA - University Of Illinois; Walker, David; Hartman, Glen; DOMIER, LESLIE - Retired ARS Employee; HUDSON, MATTHEW - University Of Illinois; Clough, Steven

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/14/2022
Publication Date: 11/24/2022
Citation: Wei, W., Wu, X., Garcia, A., McCoppin, N.K., Gomes Viana, J.P., Murad, P.S., Walker, D.R., Hartman, G.L., Domier, L.L., Hudson, M.E., Clough, S.J. 2022. An NBS-LRR protein in the Rpp1 locus negates the dominance of Rpp1-mediated resistance against Phakopsora pachyrhizi in soybean. The Plant Journal. 113(5):915-933. https://doi.org/10.1111/tpj.16038.
DOI: https://doi.org/10.1111/tpj.16038

Interpretive Summary: The ability of plants to adequately defend themselves against microbial attack is essential for survival and for sufficient crop production. At a molecular level, this ability is often conferred by single, specific resistance genes that allow a plant to recognize some factor released by a pathogen. In soybean, the Rpp1 gene provides resistance to specific pathotypes of the soybean rust fungus. In this manuscript we describe how the resistance provided by Rpp1 can be suppressed by a protein produced by a different gene at the Rpp1 location that occurs in a “dominant susceptible” soybean, such that plants from crosses between a resistant parent and a dominant susceptible parent are susceptible to rust. We were able to demonstrate at a molecular level that the repression of resistance is most likely due to the physical binding of a protein from the dominant susceptible parent with a normally functional Rpp1 protein. The results provide more insight into how resistance genes function and highlight the potential effect of susceptible genotypes in breeding for resistance. This information will be useful to soybean breeders, who would normally expect three-fourths of the F2 progeny from a resistant x susceptible cross to be resistant. They may need to use DNA markers to distinguish between heterozygous susceptible plants and susceptible plants that did not inherit a copy of the Rpp1 resistance gene.

Technical Abstract: The soybean Rpp1 locus confers resistance to Phakopsora pachyrhizi, the causal agent of rust, and resistance is usually dominant over susceptibility. Although three genes (all NBS-LRRs) have been identified as candidates for Rpp1, the actual resistance gene within the Rpp1 locus is unknown. The dominance of Rpp1-mediated resistance is lost when a resistant genotype with either Rpp1 or Rpp1b is crossed with the susceptible line TMG06_0011, but the mechanism of this dominant susceptibility (DS) is unknown. Sequencing of the region revealed that the TMG06_0011 Rpp1 locus has a single NBS-LRR gene (DS-R), whereas resistant PI 594760B (Rpp1b) is like PI 200492 (Rpp1) in having three NBS-LRR genes. Evidence that DS-R is the cause of DS was reflected in virus-induced gene silencing of DS-R in Rpp1b/DS-R or Rpp1/DS-R heterozygous plants where resistance was partially restored. In heterozygous Rpp1b/DS-R plants, expression of the Rpp1b candidate genes was not altered, indicating no effect of DS-R on transcription. Physical interaction of the DS-R protein with Rpp1b resistance-associated proteins was supported by yeast two-hybrid studies. We conclude that suppression of resistance most likely occurs at the protein level, with function of the Rpp1 proteins inhibited by binding of the DS-R protein. The DS-R gene was found in other soybean, with an estimated allele frequency of approximately 6%, and in wild soybean (Glycine soja). The identification of a dominant susceptible NBS-LRR gene provides insight into the behavior of NBS-LRR proteins and shows that the dominance of an R gene can be influenced by a susceptibility allele.