Fitness penalty in susceptible host is associated with virulence of S oybean mosaic virus on R sv1 ‐genotype soybean: a consequence of perturbation of HC ‐ P ro and not P 3

Summary The multigenic Rsv1 locus in the soybean plant introduction ( PI ) ‘ PI96983 ’ confers extreme resistance against the majority of S oybean mosaic virus ( SMV ) strains, including SMV ‐ N , but not SMV ‐ G7 and SMV ‐ G7d . In contrast, in susceptible soybean cultivars lacking a functional Rsv1 locus, such as ‘ W illiams82’ ( rsv1 ), SMV ‐ N induces severe disease symptoms and accumulates to a high level, whereas both SMV ‐ G7 and SMV ‐ G7d induce mild symptoms and accumulate to a significantly lower level. Gain of virulence by SMV ‐ N on Rsv1 ‐genotype soybean requires concurrent mutations in both the helper‐component proteinase ( HC ‐ P ro) and P3 cistrons. This is because of the presence of at least two resistance ( R ) genes, probably belonging to the nucleotide‐binding leucine‐rich repeat ( NB‐LRR ) class, within the Rsv1 locus, independently mediating the recognition of HC ‐ P ro or P3 . In this study, we show that the majority of experimentally evolved mutational pathways that disrupt the avirulence functions of SMV ‐ N on Rsv1 ‐genotype soybean also result in mild symptoms and reduced accumulation, relative to parental SMV ‐ N , in W illiams82 ( rsv1 ). Furthermore, the evaluation of SMV ‐ N ‐derived HC ‐ P ro and P3 chimeras, containing homologous sequences from virulent SMV ‐ G7 or SMV ‐ G7d strains, as well as SMV ‐ N ‐derived variants containing HC ‐ P ro or P3 point mutation(s) associated with gain of virulence, reveals a direct correlation between the perturbation of HC ‐Pro and a fitness penalty in W illiams82 ( rsv1 ). Collectively, these data demonstrate that gain of virulence by SMV on R sv1 ‐genotype soybean results in fitness loss in a previously susceptible soybean genotype, this being a consequence of mutations in HC ‐ P ro, but not in P3 .