Christina Cowger

Post-anthesis moisture increased Fusarium head blight and deoxynivalenol levels in North Carolina winter wheat.

ABSTRACT 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.

Relevance of integrated disease management to resistance durability

Three aspects of integrated disease management are considered. The first is the epidemiological synergism that can be derived through combining management tactics, and through disease management at regional scales. Field studies with potato late blight are used to demonstrate epidemiological impacts of integrating host resistance, fungicides, host density, and host genetic diversity. The importance of considering spatial scale and regional disease management are demonstrated with examples of cultivar mixtures in three different pathosystems. The second aspect is the potential for integrated management to increase the durability of resistance, e.g., through reduction of pathogen population size and imposition of disruptive selection. At this point in time, most information on this topic is limited to arguments of logic and to the results of mathematical models; empirical data are largely lacking. We suggest that current theoretical approaches need to be supplemented with inclusion of more complex processes, such as the effect of fitness modifiers in pathogen populations and the influence of quantitative adaptation of pathogens to their hosts. The third aspect is integration of resistance into overall crop management, including factors such as the balance between yield potential and disease resistance and the management of genotype x environment interaction. Such integration will increase the likelihood that farmers will utilize durable resistance, and will be demonstrated with examples from wheat production in the Pacific Northwest region of the USA.

Long-distance dispersal and accelerating waves of disease: empirical relationships.

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.

Virulence Structure of the Eastern U.S. Wheat Powdery Mildew Population

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.

Molecular characterization of a new powdery mildew resistance gene Pm54 in soft red winter wheat

Key messageA new powdery mildew resistance genePm54was identified on chromosome 6BL in soft red winter wheat.AbstractPowdery mildew is causing increasing damage to wheat production in the southeastern USA. To combat the disease, a continuing need exists to discover new genes for powdery mildew resistance and to incorporate those genes into breeding programs. Pioneer® variety 26R61 (shortened as 26R61) and AGS 2000 have been used as checks in the Uniform Southern Soft Red Winter Wheat Nursery for a decade, and both have provided good resistance across regions during that time. In the present study, a genetic analysis of mildew resistance was conducted on a RIL population developed from a cross of 26R61 and AGS 2000. Phenotypic evaluation was conducted in the field at Plains, GA, and Raleigh, NC, in 2012 and 2013, a total of four environments. Three quantitative trait loci (QTL) with major effect were consistently detected on wheat chromosomes 2BL, 4A and 6BL. The 2BL QTL contributed by 26R61 was different from Pm6, a widely used gene in the southeastern USA. The other two QTL were identified from AGS 2000. The 6BL QTL was subsequently characterized as a simple Mendelian factor when the population was inoculated with a single Blumeria graminis f. sp. tritici (Bgt) isolate in controlled environments. Since there is no known powdery mildew resistance gene (Pm) on this particular location of common wheat, the gene was designated Pm54. The closely linked marker Xbarc134 was highly polymorphic in a set of mildew differentials, indicating that the marker should be useful for pyramiding Pm54 with other Pm genes by marker-assisted selection.

Rye-derived powdery mildew resistance gene Pm8 in wheat is suppressed by the Pm3 locus

Genetic suppression of disease resistance is occasionally observed in hexaploid wheat or in its interspecific crosses. The phenotypic effects of genes moved to wheat from relatives with lower ploidy are often smaller than in the original sources, suggesting the presence of modifiers or partial inhibitors in wheat, especially dilution effects caused by possible variation at orthologous loci. However, there is little current understanding of the underlying genetics of suppression. The discovery of suppression in some wheat genotypes of the cereal rye chromosome 1RS-derived gene Pm8 for powdery mildew resistance offered an opportunity for analysis. A single gene for suppression was identified at or near the closely linked storage protein genes Gli-A1 and Glu-A3, which are also closely associated with the Pm3 locus on chromosome 1AS. The Pm3 locus is a complex of expressed alleles and pseudogenes embedded among Glu-A3 repeats. In the current report, we explain why earlier work indicated that the mildew suppressor was closely associated with specific Gli-A1 and Glu-A3 alleles, and predict that suppression of Pm8 involves translated gene products from the Pm3 locus.

Velocity of Spread of Wheat Stripe Rust Epidemics

ABSTRACT Controversy has long existed over whether plant disease epidemics spread with constant or with increasing velocity. We conducted largescale field experiments with wheat stripe rust at Madras and Hermiston, Oregon, where natural stripe rust epidemics were rare, to test these competing models. Data from three location-years were available for analysis. A susceptible winter wheat cultivar was planted in pure stand and also in a 1:4 or 1:1 mixture with a cultivar immune to the stripe rust race utilized in the experiments. Plots were 6.1 m wide and varied from 73 to 171 m in length. A 1.5 by 1.5-m focus was inoculated in either the center (2001) or upwind of the center (2002 and 2003) of each plot. Disease severity was evaluated weekly throughout the epidemics in each plot at the same points along a transect running upwind and downwind from the focus. Velocity of spread was calculated from the severity data and regressed separately on time and on distance from the focus. In all location-years and treatments, and at all levels of disease severity, velocity consistently increased linearly with distance, at an average rate of 0.59 m/week per m, and exponentially with time. Further, across epidemics there was a significant positive relationship between the apparent infection rate, r, and the rate of velocity increase in both space and time. These findings have important implications for plant diseases with a focal or partially focal character, and in particular for the effectiveness of ratereducing disease management strategies at different spatial scales.

Fusarium graminearum infection and deoxynivalenol concentrations during development of wheat spikes.

Fusarium head blight (FHB) affects whole spikes of small grain plants, yet little is known about how FHB develops following infection, or about the concentration or progression of the mycotoxin deoxynivalenol (DON) in non-grain spike tissues. Fusarium mycotoxin levels in whole small-grain spikes are of concern to producers of whole-crop silage, as well as users of straw containing chaff for animal bedding or winter livestock rations. A 2-year field experiment was performed in Kinston, NC to reveal the time course of FHB development. Eight winter wheat cultivars with varying levels of FHB resistance were used in the 2006 experiment, and four of them were used in 2007. Plots were spray-inoculated with Fusarium graminearum macroconidia at mid-anthesis. Four durations of post-anthesis mist were applied: 0, 10, 20, or 30 days. Spike samples were collected and bulked by plot at 15, 25, 35, 45, 55, and 65 days after anthesis (daa); samples were separated into grain, glume, and rachis fractions. Increasing durations of post-anthesis moisture elevated grain DON and reduced the effect of cultivar on DON, presumably by affecting the expression of resistance, in all spike tissues. Fusarium-damaged kernels increased from early kernel-hard to harvest-ripe in both years. Percent infected kernels increased from medium-milk to harvest-ripe. During grainfill, DON concentrations declined in grain but increased in rachises and glumes, peaking at early kernel-hard, before declining. Higher mean and maximum DON levels were observed in rachises and glumes than in grain. Estimated whole-spike DON peaked at early kernel-hard. In a high-FHB year, whole-plant harvest for forage should be conducted as early as possible. Straw that may be consumed by livestock could contain significant amounts of DON in chaff, and DON can be minimized if straw is sourced from low-symptom crops. Cultivar FHB resistance ratings and disease data should be useful in predicting whole-spike DON levels. Overall, associations between grain DON levels in harvest-ripe and prior samples were stronger the later the prior samples were collected, suggesting limits to the possibility of predicting harvest-ripe grain DON from earlier levels.

Frequency of Sexual Reproduction by Mycosphaerella graminicola on Partially Resistant Wheat Cultivars

ABSTRACT The frequency of sexual reproduction has a profound effect on the population structure and the adaptive potential of a facultatively sexual parasite. Little is known about the relationship of quantitative host resistance to the frequency of sex in pathogens. We sampled over 5,000 fungal fruiting bodies from eight different wheat cultivars over a 3-year period. The cultivars possessed varying degrees of susceptibility to Mycosphaerella graminicola, a facultatively sexual pathogen that is hetero-thallic and bipolar. The fruiting bodies were classified as M. graminicola pycnidia or ascocarps (asexual and sexual fruiting bodies, respectively), other identifiable fungi, or unidentified. In all 3 years, area under the disease progress curve (AUDPC) explained a significant proportion of the variation in ascocarps as a percentage of M. graminicola fruiting bodies (P < 0.0005). The mean percentage of M. graminicola ascocarps from all cultivars was 63% in 1998, when the epidemic was intense, and 14% in 1999, a year of low disease levels. In 2000, samples were taken at 7-day intervals from 6 June to 27 June from two cultivars with substantially different AUDPCs (788 and 2,185 percentage-days). The less diseased cultivar yielded its first M. graminicola ascocarps 1 week later than the more diseased cultivar, and respective means of ascocarps as a percentage of M. graminicola fruiting bodies across sampling dates were 20.2 and 59.3%. The ratio of sexual to asexual reproduction by M. graminicola is likely to be strongly conditioned by infection density.

Appearance of Powdery Mildew of Wheat Caused by Blumeria graminis f. sp. tritici on Pm17-Bearing Cultivars in North Carolina

Pm17 is a gene for resistance to powdery mildew caused by Blumeria graminis (DC.) E.O. Speer f. sp. tritici. The gene was first confirmed in the wheat-rye translocation cultivar Amigo (1). In Amigo, the translocation is T1AL-1RS and the 1RS arm has the gene Pm17. In the mid-Atlantic United States, at least two widely deployed soft red winter wheat (Triticum aestivum L.) cultivars, McCormick (2) and Tribute (3), possess Pm17 inherited from Amigo. Before 2009, low frequencies of mostly intermediate virulence to Pm17 were detected among isolates from research plots of highly susceptible cultivars (4), but Pm17-bearing cultivars remained immune to mildew in the field. In April 2009, moderately severe powdery mildew was observed for the first time throughout plots of McCormick, Tribute, and other cultivars in both Kinston and Raleigh, NC. At Kinston, Pm17 virulence was observed at two research sites, separated by approximately 10 km, throughout plots of Amigo, McCormick, Tribute, and the hard red winter wheat cultivar TAM 303, which also contains Pm17. In the same month, virulence to Pm17 was observed in Raleigh throughout rows and plots of Amigo and TAM 303. In Kinston and Raleigh, ratings of powdery mildew severity on the Pm17-containing cultivars were 4 or 5 on a scale of 0 to 9, with 0 being the absence of mildew pustules and 9 the most severe mildew infection. Mildew was observed on leaves of all ages. Mildewed leaves were collected from field plots of all four Pm17-bearing cultivars, and an assay to confirm Pm17 virulence was conducted in the laboratory. Mixed-isolate cultures were derived from the leaves and a detached-leaf assay was performed using Amigo, which is the standard Pm17 differential (4). All tested cultures were fully to moderately virulent on Pm17 and all were fully virulent on the susceptible control Chancellor. In the field, chasmothecia (sexual fruiting bodies) were observed on Pm17-bearing cultivars. Together with the quantitatively varying Pm17 virulence detected in the laboratory assay, this suggests that multiple strains of Pm17-virulent B. graminis f. sp. tritici may be present in the field, although that has not yet been demonstrated. Pm17 has protected wheat from powdery mildew over a substantial area in the mid-Atlantic United States. The loss of Pm17 is the most important virulence shift in the U.S. wheat powdery mildew population since Pm4a became ineffective around 2002. Isolates virulent to Pm17 can be expected to appear and multiply in wheat-producing states of the mid-Atlantic United States, including Delaware, Maryland, Virginia, North Carolina, South Carolina, and Georgia. Thus, the urgency of developing and releasing wheat cultivars with other sources of effective mildew resistance is heightened. References: (1) B. Friebe et al. Euphytica 91:59, 1996. (2) C. A. Griffey et al. Crop Sci. 45:416, 2005. (3) C. A. Griffey et al. Crop Sci. 45:419, 2005. (4) R. Parks et al. Plant Dis. 92:1074, 2008.