Host effect on the genetic diversification of beet necrotic yellow vein virus single-plant populations.

Theoretical models predict that, under restrictive host conditions, virus populations will exhibit greater genetic variability. This virus response has been experimentally demonstrated in a few cases but its relation with a virus's capability to overcome plant resistance is unknown. To explore the genetic host effects on Beet necrotic yellow vein virus (BNYVV) populations that might be related to resistance durability, a wild-type virus isolate was vector inoculated into partially resistant Rz1, Rz2, and susceptible sugar beet cultivars during a serial planting experiment. Cloning and sequencing a region of the viral RNA-3, involving the pathogenic determinant p25, revealed that virus diversity significantly increased in direct proportion to the strength of host resistance. Thus, whereas virus titers were highest, intermediate, and lowest in susceptible, Rz1, and Rz2 plants, respectively; the average number of nucleotide differences among single-plant populations was 0.8 (±0.1) in susceptible, 1.4 (±0.1) in Rz1, and 2.4 (±0.2) in Rz2 genotypes. A similar relationship between host restriction to BNYVV root accumulation and virus genetic variability was detected in fields of sugar beet where these specific Rz1- and Rz2-mediated resistances have been defeated.

Breakdown of host resistance by independent evolutionary lineages of Beet necrotic yellow vein virus involves a parallel c/u mutation in its p25 gene.

ABSTRACT Breakdown of sugar beet Rz1-mediated resistance against Beet necrotic yellow vein virus (BNYVV) infection was previously found, by reverse genetics, to be caused by a single mutation in its p25 gene. The possibility of alternative breaking mutations, however, has not been discarded. To explore the natural diversity of BNYVV in the field and its effects on overcoming Rz1, wild-type (WT) and resistance-breaking (RB) p25 genes from diverse production regions of North America were characterized. The relative titer of WT p25 was inversely correlated with disease expression in Rz1 plants from Minnesota and California. In Minnesota, the predominant WT p25 encoded the A(67)C(68) amino acid signature whereas, in California, it encoded A(67)L(68). In both locations, these WT signatures were associated with asymptomatic BNYVV infections of Rz1 cultivars. Further analyses of symptomatic resistant plants revealed that, in Minnesota, WT A(67)C(68) was replaced by V(67)C(68) whereas, in California, WT A(67)L(68) was replaced by V(67)L(68). Therefore, V(67) was apparently critical in overcoming Rz1 in both pathosystems. The greater genetic distances between isolates from different geographic regions rather than between WT and RB from the same location indicate that the underlying C to U transition originated independently in both BNYVV lineages.

Intrahost mechanisms governing emergence of resistance-breaking variants of Potato virus Y.

The emergence of resistance breaking (RB) variants starting from the avirulent Potato virus Y NN strain (PVY(NN)) was analyzed after imposing different selective host constraints. Tobacco resistance to PVY(NN) is conferred by va in both NC745 and VAM genotypes, but VAM carries an extra resistance gene, va2. RB-variants emerged only in NC745 and unexpectedly accumulated higher in the original host, tobacco B21, than the parental PVY(NN). However, the recovery of RB-variants was interfered by PVY(NN) in mixed infections. Further analysis indicated that RB-variants also arose in tobacco VAM, but they were limited to subliminal local infections. Their inability to breakout was associated with absence of a mutational adaptation in the viral VPg gene, which implied a loss of fitness in tobacco B21. Altogether, the emergence of RB-variants was conditioned by inherited host constraints, interference by co-infecting avirulent virus genotypes, and fitness tradeoff of virus adaptations.

Complementary functions of two recessive R-genes determine resistance durability of tobacco 'Virgin A Mutant' (VAM) to Potato virus Y.

Tobaccos VAM and NC745 carry the recessive va gene that confers resistance to PVY(NN). However, they exhibit different levels of resistance durability. Upon virus inoculation, only NC745 developed sporadic systemic symptoms caused by emerging resistance-breaking variants that easily infected both NC745 and VAM genotypes. To identify the differential host conditions associated with this phenomenon, cellular accumulation, cell-to-cell movement, vascular translocation, and foliar content of PVY(NN) were comparatively evaluated. Virus cell-to-cell movement was restricted and its transit through the vasculature boundaries was completely blocked in both tobacco varieties. However, an additional defense mechanism operating only in tobacco VAM drastically reduced the in situ cellular virus accumulation. Genetic analyses of hybrid plant progenies indicate that VAM-type resistance was conditioned by at least two recessive genes: va and a newly reported va2 locus. Moreover, segregant plant progenies that restricted virus movement but permitted normal virus accumulation were prone to develop resistance-breaking infections.

Changes in the intraisolate genetic structure of Beet necrotic yellow vein virus populations associated with plant resistance breakdown.

The causal agent of rhizomania disease, Beet necrotic yellow vein virus (BNYVV), typically produces asymptomatic root-limited infections in sugar beets (Beta vulgaris) carrying the Rz1-allele. Unfortunately, this dominant resistance has been recently overcome. Multiple cDNA clones of the viral pathogenic determinant p25, derived from populations infecting susceptible or resistant plants, were sequenced to identify host effects on the viral population structure. Populations isolated from compatible plant-virus interactions (susceptible plant-wild type virus and resistant plant-resistant breaking variants) were large and relatively homogeneous, whereas those from the incompatible interaction (resistant plant-avirulent type virus) were small and highly heterogeneous. All populations from susceptible plants had the same dominant haplotype, whereas those from resistant cultivars had a different haplotype surrounded by a spectrum of mutants. Selection and diversification analyses suggest an evolutionary trajectory of BNYVV with positive selection for changes required to overcome resistance, followed by elimination of hitchhiking mutations through purifying selection.