Three cultivars of winter bread wheat (Gene, Madsen and Stephens) were each inoculated as seedlings in the greenhouse with seven or eight individual isolates of Mycosphaerella graminicola collected in 1997 from each of the same cultivars in the field. Isolates collected from Gene were virulent to all three cultivars, while isolates obtained from Madsen and Stephens were virulent to those two cultivars and, in all but one case, avirulent to Gene. At its release in 1992, Gene was resistant to M. graminicola, as indicated by both field observations and greenhouse tests, but by 1995 its resistance had substantially deteriorated. This indicated that its resistance was vertical (sensu Vanderplank) or race-specific, and that commercial cultivation of Gene rapidly selected for strains in the local M. graminicola population that were specifically adapted to overcome its resistance.
Classic approaches to modeling biological invasions predict a "traveling wave" of constant velocity determined by the invading organism's reproductive capacity, generation time, and dispersal ability. Traveling wave models may not apply, however, for organisms that exhibit long-distance dispersal. Here we use simple empirical relationships for accelerating waves, based on inverse power law dispersal, and apply them to diseases caused by pathogens that are wind dispersed or vectored by birds: the within-season spread of a plant disease at spatial scales of <100 m in experimental plots, historical plant disease epidemics at the continental scale, the unexpectedly rapid spread of West Nile virus across North America, and the transcontinental spread of avian influenza strain H5N1 in Eurasia and Africa. In all cases, the position of the epidemic front advanced exponentially with time, and epidemic velocity increased linearly with distance; regression slopes varied over a relatively narrow range among data sets. Estimates of the inverse power law exponent for dispersal that would be required to attain the rates of disease spread observed in the field also varied relatively little (1.74-2.36), despite more than a fivefold range of spatial scale among the data sets.
Current models for forecasting Fusarium head blight (FHB) and deoxynivalenol (DON) levels in wheat are based on weather near anthesis, and breeding for resistance to FHB pathogens often relies on irrigation before and shortly after anthesis to encourage disease development. The effects of post-anthesis environmental conditions on FHB are poorly understood. We performed a field experiment at Kinston, NC, to explore the effects of increasing duration of post-anthesis moisture on disease incidence, disease severity, Fusarium-damaged kernels (FDK), percent infected kernels, and DON. The experiment had a split-plot design, and one trial was conducted in each of two successive years. Main plots consisted of post-anthesis mist durations of 0, 10, 20, or 30 days. Subplots were of eight cultivars in the first year and seven in the second year, two being susceptible to FHB and the remainder each with varying degrees of apparent type I and type II resistance. Plots were inoculated by spraying Fusarium graminearum macroconidia at mid-anthesis. Averaging across years and cultivars, 10 or 20 days of post-anthesis mist had the same effect (P > or = 0.198) and were associated with an approximately fourfold increase in mean disease incidence and eightfold increase in disease severity compared with 0 days of mist (P < or = 0.0002). In both years, mean FDK percentages at 0 and 10 days post-anthesis mist were the same and significantly lower than FDK percentages under 20 or 30 days of post-anthesis mist. Mist duration had a significant effect on percent kernels infected with Fusarium spp. as detected by a selective medium assay of 2007 samples. Averaging across all cultivars, in both years, DON levels increased significantly for 10 days compared with 0 days of mist, and increased again with 20 days of mist (P < or = 0.04). This is the first investigation to show that extended post-flowering moisture can have a significant enhancing effect on FHB, FDK, DON, and percent infected kernels of wheat. For all disease and toxin assays, cultivar rankings were significantly noncorrelated among mist durations in at least 1 year, suggesting that FHB screening programs might rank genotypes differently under extended post-anthesis moisture than without it. Our findings also imply that accurate forecasts of DON in small grains must take account of post-anthesis weather conditions.
Filamentous fungi rapidly evolve in response to environmental selection pressures in part due to their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of virulence determinants, known as effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. 1,026,859 SNPs/InDels were used to identify novel loci, as well as SnToxA and SnTox3 as factors in disease. Genes displaying presence/absence variation, predicted effector genes, and genes localized on an accessory chromosome had significantly higher pN/pS ratios, indicating a higher rate of sequence evolution. Population structure analyses indicated two P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1 in the most prevalent cultivars in the corresponding regions. Additionally, 12 and 5 candidate effector genes were observed to be under diversifying selection among isolates from Population 1 and 2, respectively, but under purifying selection or neutrally evolving in the opposite population. Selective sweep analysis revealed 10 and 19 regions that had recently undergone positive selection in Population 1 and 2, respectively, involving 92 genes in total. When comparing genes with and without presence/absence variation, those genes exhibiting this variation were significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection pressures unique to spring and winter wheat production regions by rapid adaptive evolution and various routes of genomic diversification, potentially facilitated through transposable element activity.
Quantitative resistance (QR) to crop diseases has usually been much more durable than major-gene, effector-triggered resistance. It has been observed that the effectiveness of some QR has eroded as pathogens adapt to it, especially when deployment is extensive and epidemics occur regularly, but it generally declines more slowly than effector-triggered resistance. Changes in aggressiveness and specificity of diverse pathogens on cultivars with QR have been recorded, along with experimental data on fitness costs of pathogen adaptation to QR, but there is little information about molecular mechanisms of adaptation. Some QR has correlated or antagonistic effects on multiple diseases. Longitudinal data on cultivars’ disease ratings in trials over several years can be used to assess the significance of QR for durable resistance in crops. It is argued that published data likely underreport the durability of QR, owing to publication bias. The implications of research on QR for plant breeding are discussed.
Little is known about the population structure of wheat powdery mildew in the eastern United States, and the most recent report on virulence in this population involved isolates collected in 1993–94. In the present study, wheat leaves naturally infected with powdery mildew were collected from 10 locations in the southeastern United States in 2003 and 2005 and a collection of 207 isolates was derived from single ascospores. Frequencies of virulence to 16 mildew resistance (Pm) genes were determined by inoculating the isolates individually on replicated plates of detached leaves of differential wheat lines. These virulence frequencies were used to infer local effectiveness of Pm genes, estimate virulence complexity, detect significant associations between pairs of pathogen avirulence loci, and assess whether phenotypic differences between pathogen subpopulations increased with geographic distance. In both years, virulence to Pm3a, Pm3c, Pm5a, and Pm7 was present in more than 90% of sampled isolates and virulence to Pm1a, Pm16, Pm17, and Pm25 was present in fewer than 10% of isolates. In each year, 71 to 88% of all sampled isolates possessed one of a few multilocus virulence phenotypes, although there were significant differences among locations in frequencies of virulence to individual Pm genes. Several significant associations were detected between alleles for avirulence to pairs of Pm genes. Genetic (phenotypic) distance between isolate subpopulations increased significantly (R2 = 0.40, P < 0.001) with increasing geographic separation; possible explanations include different commercial deployment of Pm genes and restricted gene flow in the pathogen population.
Fusarium graminearum and 21 related species comprising the F. sambucinum species complex lineage 1 (FSAMSC-1) are the most important Fusarium Head Blight pathogens of cereal crops world-wide. FSAMSC-1 species typically produce type B trichothecenes. However, some F. graminearum strains were recently found to produce a novel type A trichothecene (NX-2) resulting from functional variation in the trichothecene biosynthetic enzyme Tri1. We used a PCR-RFLP assay targeting the TRI1 gene to identify the NX-2 allele among a global collection of 2515 F. graminearum. NX-2 isolates were only found in southern Canada and the northern U.S., where they were observed at low frequency (1.8%), but over a broader geographic range and set of cereal hosts than previously recognized. Phylogenetic analyses of TRI1 and adjacent genes produced gene trees that were incongruent with the history of species divergence within FSAMSC-1, indicating trans-species evolution of ancestral polymorphism. In addition, placement of NX-2 strains in the TRI1 gene tree was influenced by the accumulation of nonsynonymous substitutions associated with the evolution of the NX-2 chemotype, and a significant (P<0.001) change in selection pressure was observed along the NX-2 branch (ω=1.16) in comparison to other branches (ω=0.17) in the TRI1 phylogeny. Parameter estimates were consistent with positive selection for specific amino-acid changes during the evolution of NX-2, but direct tests of positive selection were not significant. Phylogenetic analyses of fourfold degenerate sites and intron sequences in TRI1 indicated the NX-2 chemotype had a single evolutionary origin and evolved recently from a type B ancestor. Our results indicate the NX-2 chemotype may be indigenous, and possibly endemic, to southern Canada and the northern U.S. In addition, we demonstrate that the evolution of TRI1 within FSAMSC-1 has been complex, with evidence of trans-species evolution and chemotype-specific shifts in selective constraint.
The selective effect of quantitative host resistance on pathogen aggressiveness is poorly understood. Because two previous experiments with a small number of bread wheat cultivars and isolates of Mycosphaerella graminicola had indicated that more susceptible hosts selected for more aggressive isolates, we conducted a larger experiment to test that hypothesis. In each of 2 years, six cultivars differing in their levels of partial resistance were planted in field plots, and isolates were collected from each cultivar early and late in the growing season. The isolates were inoculated as populations bulked by cultivar of origin, field replicate, and collection date on seedlings of the same six cultivars in the greenhouse. The selective impact of a cultivar on aggressiveness was measured as the difference in aggressiveness between early and late isolates from that cultivar. Regression of those differences on disease severity in the field yielded significance values of 0.0531 and 0.0037 for the 2 years, with moderately resistant cultivars selecting for more aggressive isolates. In a related experiment, the protectant fungicide chlorothalonil was applied to plots of two susceptible cultivars to retard epidemic development. When tested in the greenhouse, isolates of M. graminicola from those plots were significantly more aggressive than isolates from the same cultivars unprotected by fungicide.
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