The estimated potential yield losses caused by plant pathogens is up to 16% globally and most research in plant pathology aims to reduce yield loss in our crops directly or indirectly. Yield losses caused by a certain disease depend not only on disease severity, but also on the weather factors, the pathogen’s aggressiveness, and the ability of the crop to compensate for reduced photosynthetic area. The yield loss-disease relationship in a certain host-pathogen system might therefore change from year to year, making predictions for yield loss very difficult at the regional or even at the farmer’s level. However, estimating yield losses is essential to determine disease management thresholds at which acute control measures such as fungicide applications, or strategic measures such as crop rotation or use of resistant cultivars are economically and environmentally sensible. Legislation in many countries enforces implementation of integrated pest management (IPM), based on economic thresholds at which the costs due to a disease justify the costs for its management. Without a better understanding of the relationship between disease epidemiology and yield loss, we remain insufficiently equipped to design adequate IPM strategies that will be widely adapted in agriculture. Crop loss studies are resource demanding and difficult to interpret for one particular disease, as crops are usually not invaded by only one pest or pathogen at a time. Combining our knowledge on disease epidemiology, crop physiology, yield development, damage mechanisms involved, and the effect of management practices can help us to increase our understanding of the disease-crop loss relationship. The main aim of this paper is to review and analyze the literature on a representative host-pathogen relationship in an important staple food crop to identify knowledge gaps and research areas to better assess yield loss and design management strategies based on economic thresholds.

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.

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. Parastagonospora nodorum is an economically important pathogen of wheat, employing proteinaceous effectors to cause disease. Recognition of effectors by host susceptibility genes often leads to the elicitation of programmed cell death. However, little is known on the correlation between effector diversity and the spatial distribution of host resistance/susceptibility or the genomic mechanisms of diversification. This research presents the genome resequencing of 197 P. nodorum isolates collected from spring, winter, and durum wheat production regions of the United States, enabling the investigation of genome dynamics and evolution. Results illustrate local adaptation to host resistance or susceptibility, as evidenced by population-specific evolution of predicted effector genes and positively selected selective sweeps. Predicted effector genes, genes exhibiting presence/absence variation, and genes residing on an accessory chromosome, were found to be diversifying more rapidly. Additionally, transposable elements were predicted to play a role in the maintenance or elimination of genes. A GWAS approach identified the previously reported SnToxA and SnTox3 as well as novel virulence candidates as major elicitors of disease. These results highlight the flexibility of the P. nodorum genome in response to population-specific selection pressures and illustrate the utility of whole genome resequencing for the identification of putative virulence mechanisms.

Wheat powdery mildew is a disease of global importance that occurs across a wide geographic area in the United States. A virulence survey of Blumeria graminis f. sp. tritici, the causal agent, was conducted by sampling 36 wheat fields in 15 U.S. states in the years 2013 and 2014. Using a hierarchical sampling protocol, isolates were derived from three separated plants at each of five separated sites within each field in order to assess the spatial distribution of pathotypes. In total, 1,017 isolates from those fields were tested individually on single-gene differential cultivars containing a total of 21 powdery mildew resistance (Pm) genes. Several recently introgressed mildew resistance genes from wild wheat relatives (Pm37, Pm53, MlAG12, NCAG13, and MlUM15) exhibited complete or nearly complete resistance to all local B. graminis f. sp. tritici populations from across the sampled area. One older gene, Pm4b, also retained at least some efficacy across the sampled area. The B. graminis f. sp. tritici population sampled from Arkansas and Missouri, on the western edge of the eastern soft red winter wheat region, had virulence profiles more similar to other soft wheat mildew populations than to the geographically closer population from hard wheat fields in the Plains states of Oklahoma, Nebraska, and Kansas. The Plains population differed in that it was avirulent to several Pm genes long defeated in the soft-wheat-growing areas. Virulence complexity was greatest east of the Mississippi River, and diminished toward the west. Several recently introgressed Pm genes (Pm25, Pm34, Pm35, and NCA6) that are highly effective against mildew in the field in North Carolina were unexpectedly susceptible to eastern-U.S. B. graminis f. sp. tritici populations in detached-leaf tests. Sampled fields displayed a wide range of pathotype diversity and spatial distribution, suggesting that epidemics are caused by varying numbers of pathotypes in all regions. The research confirmed that most long-used Pm genes are defeated in the eastern United States, and the U.S. B. graminis f. sp. tritici population has different virulence profiles in the hard- and soft-wheat regions, which are likely maintained by host selection, isolation by distance, and west-to-east gene flow.

Deoxynivalenol (DON) concentrations in mature wheat grain are usually correlated with symptoms produced by Gibberella zeae infection. However, there have been numerous observations of unacceptably high DON in asymptomatic crops, which can lead to lower-than-expected milling reductions in DON. We conducted a field experiment with winter wheat to examine the effect of infection timing and postanthesis moisture on grain quality and DON accumulation. Seven to eight soft red winter wheat cultivars were grown in three successive years in a misted nursery in Kinston, NC. Spikes were randomly selected for individual spray inoculation at 0, 10, or 20 days after anthesis (daa). Starting at anthesis, plots were subjected to 0, 10, 20, or 30 days of mist. Inoculated spikes and noninoculated controls were collected at harvest-ripeness, and the threshed grain was assayed for Fusarium-damaged kernels (FDK) and DON. In 2 of 3 years, percentages of FDK were significantly lower from 10-daa infections than from those at 0 daa, although DON concentrations were the same at the two inoculation timings in 2 of the 3 years. Those results indicate that the period of maximum susceptibility to wheat spike infections by G. zeae is close to or slightly less than 10 daa in North Carolina. In 2 of 3 years, FDK–DON correlation was greater for 0- and 10-daa inoculations and for 0- to 20-daa misted treatments than for the later-inoculated or longer-misted treatments, respectively. The percentage of “low-FDK, high DON” (LFHD) observations (defined as FDK ≤ 4.0%, DON ≥ 2 μg g^–1) was higher in 2007 than in 2005 or 2006 (41, 14, and 18%, respectively). In both 2006 and 2007, high percentages of LFHD observations (≥60%) occurred under marginal disease conditions involving late infection. We conclude that late infection is an important factor leading to LFHD grain. Periods of rain soon after anthesis likely favor the low-symptom, high-DON scenario, and conditions that create greater within-crop variability of anthesis timing may also be important.