Coding Mutations in Vacuolar Protein-Sorting 4 AAA+ ATPase Endosomal Sorting Complexes Required for Transport Protein Homologs Underlie bc-2 and New bc-4 Gene Conferring Resistance to Bean Common Mosaic Virus in Common Bean

Abstract

<i>Bean common mosaic virus</i> (BCMV) is a major disease in common bean (<i>Phaseolus vulgaris</i> L.). Host plant resistance is the most effective strategy to minimize crop damage against BCMV and the related <i>Bean common mosaic necrosis virus</i> (BCMNV). To facilitate breeding for resistance, we sought to identify candidate genes and develop markers for the <i>bc-2</i> gene and the unknown gene with which it interacts. Genome-wide association study (GWAS) of the Durango Diversity Panel (DDP) identified a peak region for <i>bc-2</i> on chromosome Pv11. Haplotype mapping narrowed the <i>bc-2</i> genomic interval and identified Phvul.011G092700, a vacuolar protein-sorting 4 (Vps4) AAA+ ATPase endosomal sorting complexes required for transport (ESCRT) protein, as the <i>bc-2</i> candidate gene. The race Durango Phvul.011G092700 gene model, <i>bc-2</i> ^[UI ^111], contains a 10-kb deletion, while the race Mesoamerican <i>bc-2</i> ^[Robust] consists of a single nucleotide polymorphism (SNP) deletion. Each mutation introduces a premature stop codon, and they exhibit the same interaction with the pathogroups (PGs) tested. Phvul.005G125100, another Vps4 AAA+ ATPase ESCRT protein, was identified as the candidate gene for the new recessive <i>bc-4</i> gene, and the recessive allele is likely an amino acid substitution in the microtubule interacting and transport (MIT) domain. The two Vps4 AAA+ ATPase ESCRT proteins exhibit high similarity to the <i>Zym</i> Cucsa.385040 candidate gene associated with recessive resistance to <i>Zucchini yellow mosaic virus</i> in cucumber. <i>bc-2</i> alone has no resistance effect but, when combined with <i>bc-4</i>, provides resistance to BCMV (except PG-V) but not BCMNV, and, when combined with <i>bc-u</i> ^d, provides resistance to BCMV (except BCMV PG-VII) and BCMNV. So instead of different resistance alleles (i.e., <i>bc-2</i> and <i>bc-2</i> ²), there is only <i>bc-2</i> with a differential reaction based on whether it is combined with <i>bc-4</i> or <i>bc-u</i> <i>^d</i> , which are tightly linked in repulsion. The new tools and enhanced understanding of this host-virus pathogen interaction will facilitate breeding common beans for resistance to BCMV and BCMNV.