COEVOLUTION OF VIRUS RESISTANCE AND VIRAL AVIRULENCE GENES

Avirulence genes in plant pathogens have been defined by their requirement for disease resistance in hosts containing corresponding R genes. Plant viruses evolve very rapidly owing to very short replication cycles, large numbers of genomes within each cell across many cells per host, and many hosts. For RNA viruses, the absence of a proofreading function in viral replicases may result in mutation rates as high as 104 per replication cycle per base. Viral genetic variation can result from several major genetic processes including mutation, recombination, and the acquisition of additional genomic sequence. As a consequence, resistance breaking viral genotypes are known for most host resistance, especially for genes showing HR. Avirulence determinants are typically identified by creating chimeric clones derived from viral genotypes with contrasting virulence and then testing for infectivity. Once an avirulence domain is identified, site-directed mutagenesis allows identification of specific point mutations responsible for virulence.

 Virtually any part of the viral genome can define an avirulence determinant. With respect to R genes that confer HR, avirulence factors include viral RNA polymerase subunits, movement protein, and CP. Several potyviral avirulence genes have been identified for dominant R genes that do not show HR. The CI and P3 proteins of Turnip mosaic virus serve as avirulence determinants for the Brassica napus R genes, TuRBO1 and TuRBO4/5 (96–98), while SMV HC-Pro and P3 are involved in overcoming Rsv1 in soybean. In contrast to the case for dominant genes where many different viral components have been identified as avirulence determinants, a pronounced trend is apparent viral factors that serve as the determinant for pathogenicity in resistance systems controlled by recessively inherited R genes. Of nine R gene studies to date, seven identify potyviral VPg as the pathogenicity determinant for recessive resistance, although the systems in question show diverse resistance phenotypes: Capsicum pvr1/pvr12 resistance to PVY is cellular, tobacco va resistance impairs the cell-to-cell movement, and Nicandra physaloides and Solanum commersonii affect long-distance movement. The eighth study, also focused on a potyviral system, PsbMV/pea, identified the P3-6K1 cistron as the pathogenicity determinant. Only one study to date has focused outside the Potyviridae. In this case, the 3_ untranslated region of the carmovirus Melon necrotic spotvirus (MNSV) genomic RNA defined the location of the viral determinant in the by interaction of MNSV with melon. In the eight cases where the viral elicitor is protein, host recognition of these viral proteins that serve as pathogenicity determinants is altered by amino acid substitutions that do not appear to significantly compromise the function of the protein in pathogenesis. For other microbial pathogens, there often appears to be a fitness penalty association with mutations from avirulence to virulence. Although this type of fitness/avirulence tradeoff has not been noted generally for plant viruses, there are specific examples where this occurs. Isolates of ToMV capable of overcoming Tm22 gene were found to multiply poorly on resistant plants. If the Tm22 resistant protein targets a domain of the viral MP such that this protein is mutated to overcome resistance, these mutations could result in diminished fitness.