Characterization of natural and induced variation in the LOV1 gene, a CC-NB-LRR gene conferring victorin sensitivity and disease susceptibility in Arabidopsis.

The fungus Cochliobolus victoriae, the causal agent of Victoria blight, produces a compound called victorin that is required for pathogenicity of the fungus. Victorin alone reproduces disease symptoms on sensitive plants. Victorin sensitivity and susceptibility to C. victoriae were originally described on oats but have since been identified on Arabidopsis thaliana. Victorin sensitivity and disease susceptibility in Arabidopsis are conferred by LOV1, a coiled-coil-nucleotide-binding-leucine-rich repeat (CC-NB-LRR) protein. We sequenced the LOV1 gene from 59 victorin-insensitive mutants and found that the spectrum of mutations causing LOV1 loss of function was similar to that found to cause loss of function of RPM1, a CC-NB-LRR resistance protein. Also, many of the mutated residues in LOV1 are in conserved motifs required for resistance protein function. These data indicate that LOV1 may have a mechanism of action similar to resistance proteins. Victorin sensitivity was found to be the prevalent phenotype in a survey of 30 Arabidopsis ecotypes, and we found very little genetic variation among LOV1 alleles. As selection would not be expected to preserve a functional LOV1 gene to confer victorin sensitivity and disease susceptibility, we propose that LOV1 may function as a resistance gene to a naturally-occurring pathogen of Arabidopsis.

Plant disease susceptibility conferred by a "resistance" gene.

The molecular nature of many plant disease resistance (R) genes is known; the largest class encodes nucleotide-binding site-leucine-rich repeat (NBS-LRR) proteins that are structurally related to proteins involved in innate immunity in animals. Few genes conferring disease susceptibility, on the other hand, have been identified. Recent identification of susceptibility to the fungus Cochliobolus victoriae in Arabidopsis thaliana has enabled our cloning of LOV1, a disease susceptibility gene that, paradoxically, is a member of the NBS-LRR resistance gene family. We found LOV1 mediates responses associated with defense, but mutations in known defense response pathways do not prevent susceptibility to C. victoriae. These findings demonstrate that NBS-LRR genes can condition disease susceptibility and resistance and may have implications for R gene deployment.

Identification and characterization of victorin sensitivity in Arabidopsis thaliana.

Cochliobolus victoriae is a necrotrophic fungus that produces a host-selective toxin called victorin. Victorin is considered to be host selective because it has been known to affect only certain allohexaploid oat cultivars containing the dominant Vb gene. Oat cultivars containing Vb are also the only genotypes susceptible to C. victoriae. Assays were developed to screen the "nonhost" plant of C. victoriae, Arabidopsis thaliana, for victorin sensitivity. Sensitivity to victorin was identified in six of 433 bulk populations of Arabidopsis. In crosses of Col-4 (victorin-insensitive) x victorin-sensitive Arabidopsis ecotypes, victorin sensitivity segregated as a single dominant locus, as it does in oats. This Arabidopsis locus was designated LOV, for locus orchestrating victorin effects. Allelism tests indicate that LOV loci are allelic or closely linked in all six victorin-sensitive ecotypes identified. LOV was localized to the north arm of Arabidopsis thaliana chromosome I. The victorin-sensitive Arabidopsis line LOV1 but not the victorin-insensitive line Col-4 was susceptible to C. victoriae infection. Consequently, the LOV gene appears to be a genetically dominant, disease susceptibility gene.