Unraveling the epistatic interactions of major rust resistance genes in common bean

Authors: VALENTINI, GISELI - North Dakota State University; PASTOR-CORRALES, MARCIAL - Retired ARS Employee; HURTADO-GONZALES, OSCAR - Animal And Plant Health Inspection Service (APHIS); Tamang, Prabin; Song, Qijian

Submitted to: European journal of plant pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/19/2025
Publication Date: 6/30/2025
Citation: Valentini, G., Pastor-Corrales, M., Hurtado-Gonzales, O., Tamang, P., Song, Q. 2025. Unraveling the epistatic interactions of major rust resistance genes in common bean. European journal of plant pathology. https://doi.org/10.1007/s10658-025-03088-z.
DOI: https://doi.org/10.1007/s10658-025-03088-z

Interpretive Summary: Bean rust is a disease caused by a fungus that thrives in cool, moist conditions. It can cause major yield loss of common bean, which is a major food source for millions of people around the world. The best way to protect beans is to breed plants that are naturally resistant to the disease. However, combining multiple resistance genes into one plant to fight disease is not always effective - sometimes one gene can "hide" the effects of another, also making it difficult for breeders to know which genes are at work. Scientists at the USDA Agricultural Research Service, Beltsville, Maryland, and North Dakota State University studied how three major rust resistance genes (Ur-3, Ur-4, and Ur-5) interact with each other. They tested two groups of bean plants, exposing them to the rust-causing fungus and observing their responses. Some plants developed small dead spots (a sign that Ur-3 and Ur-4 were working), while others developed tiny pustules (associated with Ur-5). To confirm how the genes interacted, the researchers also used DNA genetic markers to track these genes. The study shows that these resistance genes don't always work well together. When certain genes are combined, one gene dominates the other, a phenomenon called epistasis. This means that while all three genes provide some level of protection, their interactions can make it difficult for breeders to identify and effectively combine them to control rust. These findings will help scientists and plant breeders comprehend genetic complexity underlying rust resistance in common beans and explore epistatic models that can better withstand rust disease, leading to a healthier crop, and greater food security worldwide in the face of evolving pathogens.

Technical Abstract: Bean rust, caused by Uromyces appendiculatus, threatens common bean (Phaseolus vulgaris) production. Development of resistant varieties is an effective way to prevent and control bean rust. Combining rust resistance genes often results in epistatic interactions, in which the effect of one allele on one gene hides the effect of the allele on another gene. We investigated the interactions between Ur-3 and Ur-5 and Ur-4 and Ur-5 resistance genes. Two populations were inoculated with selected races of U. appendiculatus. The resistant reactions to Ur-3 and Ur-4 were a hypersensitive reaction (HR) characterized by necrotic spots. The resistance response to Ur-5 were tiny pustules (TP) with sporulation. Both populations showed a 12:3:1 segregation associated with epistasis. The HR reaction of Ur-3 was epistatic to the TP reaction of Ur-5 and the TP reaction of Ur-5 was epistatic to the HR reaction of Ur-4. Both epistatic interactions were confirmed by genotyping the populations with tightly linked molecular markers tagging each gene. These results suggest that complete dominant epistasis occurred on both gene pairs, but that one gene is epistatic to the other when dominant. This is the first comprehensive study to demonstrate epistatic interactions between these rust resistant genes in common bean. These findings will help breeder develop strategies to pyramid resistance genes and to develop bean plants with two or more epistatic rust resistance genes.