Mechanisms of powdery mildew resistance of wheat – a review of molecular breeding

Powdery mildew (Blumeria graminis f. sp. tritici) results in serious economic loss in wheat production. Exploration of plant resistance to wheat powdery mildew over several decades has led to the discovery of a wealth of resistance genes and quantitative trait loci (QTLs). We have provided a comprehensive summary of over 200 powdery mildew genes (permanently and temporarily designated genes) and QTLs reported in common bread wheat. This highlights the diverse and rich resistance sources that exist across all 21 chromosomes. To manage different data for breeders, here we also present a bridged mapping result from previously reported powdery mildew resistance genes and QTLs with the application of a published integrated wheat map. This will provide important insights to empower further breeding of powdery mildew resistant wheat via marker-assisted selection (MAS).     

Expression of the yeast Δ-9 desaturase gene in tomato enhances its resistance to powdery mildew

Tomato plants (Lycopersicon esculentumMill.) transformed with the yeast Δ-9 desaturase gene were found to display enhanced resistance to powdery mildew (Erysiphe polygoniDC. edmund. Salm.) and to possess higher levels of 16:1, 16:2 and 18:1 fatty acids. Lipid peroxides also increased. The improved resistance of the transgenic plants was apparently associated with the increases in 16:1 and 16:2 fatty acids.     

Variation in the nrDNA ITS sequences of some powdery mildew species: do routine molecular identification procedures hide valuable information?

During the past years, nrDNA ITS sequences have supported the identification of many powdery mildew fungi because comprehensive analyses showed that differences in these sequences have always correlated with the delimitation of different species and formae speciales of the Erysiphales. Published data, obtained using direct sequencing of the PCR products, suggested that even one to five nucleotide differences in the ITS sequences delimit different, albeit closely related, species, and/or indicate differences in host range patterns. Here we show that such differences in the ITS sequences can be detected even in a single sample of a powdery mildew fungus. We sequenced the ITS region in 17 samples, representing six powdery mildew species, both directly and after cloning the PCR products. Among these, samples of O. longipes exhibited two or three, samples of O. neolycopersici three or four, those of an Oidium sp. from Chelidonium majus up to seven, and a sample of another Oidium sp. from Passiflora caerulea two different ITS types determined after cloning. No ITS nucleotide polymorphisms were found in samples of O. lycopersici and Erysiphe aquilegiae. This suggests that some powdery mildew taxa are more variable at the ITS level than others. Thus, although the ITS sequences determined by direct sequencing represent robust data useful in delimitation and phylogenetic analysis of distinct species of the Erysiphales, these need to be used with precaution, and preferably determined after cloning, especially when dealing with closely related taxa at species and sub-species levels. With this method a hitherto undetected genetic diversity of powdery mildews can be revealed.     

Global incidence of wheat rusts and powdery mildew during 1969–2010 and durability of resistance of winter wheat variety Bezostaya 1

Disease incidence and severity was studied for winter wheat variety Bezostaya 1 and susceptible checks based on data from international nurseries from 1969 to 2010 and from 51 countries across major winter wheat production regions totalling 1,047 reports. The frequency of leaf rust and stripe rust occurrence was stable over time with marked increases in severity in 2001–2010 especially in Europe and Central and West Asia. Substantial global reductions in stem rust occurrence were recorded and attributed primarily to use of resistance genes although the recent emergence of race Ug99 makes wheat more vulnerable. The occurrence of powdery mildew remained globally stable over time. It was the most important foliar disease in Western and Southern Europe, where the frequency was very high for all time periods coupled with slight increases in severity during 2001–2010. The durable resistance of variety Bezostaya 1 to all four diseases was demonstrated in the study using comparisons of disease severities of Bezostaya 1 and the most susceptible entries. The Lr34/Yr18/Pm38 pleiotrophic set possessed by Bezostaya 1 is currently an important target for selection because it is now amenable to molecular selection. Increased use of genes like Lr34 combined with strategies to minimize cultivation of extremely susceptible varieties will contribute to long term maintenance of low and non-damaging disease levels. The durable disease resistance of Bezostaya 1, combined with its adaptability and good end-use quality, was a significant reason for its huge impact in agriculture over the last 50?years.     

Spectral signatures in the UV range can be combined with secondary plant metabolites by deep learning to characterize barley–powdery mildew interaction

In recent studies, the potential of hyperspectral sensors for the analysis of plant–pathogen interactions was expanded to the ultraviolet range (UV; 200–380 nm) to monitor stress processes in plants. A hyperspectral imaging set-up was established to highlight the influence of early plant–pathogen interactions on secondary plant metabolites. In this study, the plant–pathogen interactions of three different barley lines inoculated with Blumeria graminis f. sp. hordei (Bgh, powdery mildew) were investigated. One susceptible genotype (cv. Ingrid, wild type) and two resistant genotypes (Pallas 01, Mla1- and Mla12-based resistance and Pallas 22, mlo5-based resistance) were used. During the first 5 days after inoculation (dai) the plant reflectance patterns were recorded and plant metabolites relevant in host–pathogen interactions were studied in parallel. Hyperspectral measurements in the UV range revealed that a differentiation between barley genotypes inoculated with Bgh is possible, and distinct reflectance patterns were recorded for each genotype. The extracted and analysed pigments and flavonoids correlated with the spectral data recorded. A classification of noninoculated and inoculated samples with deep learning revealed that a high performance can be achieved with self-attention networks. The subsequent feature importance identified wavelengths as the most important for the classification, and these were linked to pigments and flavonoids. Hyperspectral imaging in the UV range allows the characterization of different resistance reactions, can be linked to changes in secondary plant metabolites, and has the advantage of being a non-invasive method. It therefore enables a greater understanding of plant reactions to biotic stress, as well as resistance reactions.     

Occurrence of boscalid resistance in cucumber powdery mildew in Japan and molecular characterization of the iron–sulfur protein of succinate dehydrogenase of the causal fungus

A total of 74 mass isolates of cucumber powdery mildew fungus (Podosphaera xanthii) were collected from commercial greenhouses with a history of boscalid use in Ibaraki Prefecture, Japan, and tested in a leaf disk assay for their sensitivity to boscalid. The mildew development of 40 of 74 isolates and five sensitive reference isolates on the disks was completely suppressed at 5 μg boscalid/ml. The minimum inhibitory concentrations (MIC) for the remaining 34 isolates were 50 μg/ml or higher, and 21 of these isolates also grew well at 500 μg/ml. Six single-spore isolates were resistant to boscalid with MIC values higher than 500 μg/ml; four of these were moderately resistant (MR), and two were very highly resistant (VHR) isolates. The growth of MR isolates was almost completely suppressed at 500 μg/ml, whereas two VHR isolates grew vigorously at 500 μg/ml. In foliar inoculation tests of potted cucumber plants, the efficacy of boscalid (500 μg/ml) against both MR and VHR isolates was very low. Partial DNA fragment of the iron–sulphur protein subunit (SdhB) gene of succinate dehydrogenase was PCR-amplified from five sensitive and five resistant isolates and directly sequenced, revealing that VHR isolates possess a substitution from a highly conserved histidine (CAT) to tyrosine (TAT) in a third cysteine-rich center of a putative SdhB, whereas MR isolates so far have not been found to have such substitution in SdhB.     

What can pest management learn from laboratory animal ethics?

There remains a lack of a clear overarching policy framework for decision‐making in pest control programmes. In comparison, ethical principles have been extensively developed for scientific procedures, such as those underlying the UK's Animals (Scientific Procedures) Act 1986. This paper assesses the extent to which the principles and methodology underlying the act and secondary guidance could be used to provide principles of rodent management. Useful principles include that any programme has a legitimate purpose; that methods are used only if the harms are outweighed by the benefits; that harms are minimised by refinement, replacement and reduction and that there is personal responsibility. The usefulness and implications for pest control of each principle and the overall approach are discussed. Copyright © 2009 Society of Chemical Industry     

What causes flag smut of wheat?

The causal agent of flag smut of wheat is currently subject to strict quarantine regulations in many countries and is believed to have a wide host range on wild and cultivated grasses. This fungus has been classified as both Urocystis agropyri and Urocystis tritici. Urocystis agropyri was first described from Elymus repens in Germany and U. tritici was first described from Triticum vulgare (=T. aestivum). In 1953, G. W. Fischer placed U. tritici and a large number of other Urocystis species in synonymy with U. agropyri. The present study is the first attempt to clarify the taxonomy and phylogeny of flag smut pathogens of grasses using molecular analyses. Three loci, the internal transcribed spacer (ITS) region of rDNA, the RNA polymerase II subunit 2 (RPB2), and translation elongation factor (TEF) protein‐coding regions were used for phylogenetic reconstruction to determine the species boundaries of 24 Urocystis specimens from triticoid hosts. Results indicate that there are several distinct lineages of flag smut pathogens, including the causal agent of flag smut of wheat, which is supported as a separate species, U. tritici. Sequences from specimens on E. repens, which are retained as U. agropyri, grouped in a clade distinct from those on wheat and rye. The closest relatives of U. tritici were found to be U. hispanica from Aegilops and Urocystis sp. from Thinopyrum junceiforme and Elymus trachycaulis. Recognition that U. tritici is genetically distinct from U. agropyri sensu stricto will impact regulatory policy and facilitate the development of diagnostic tests.     

Structure of populations of wheat powdery mildew (Erysiphe graminis DC f.sp. tritici Marchal) in Central Europe in 1993–1996: I. Dynamics of virulence

In 1993–1996, the virulence of regional populations of the wheat powdery mildew pathogen (Erysiphe graminis DC f. sp. tritici Marchal) from the Czech Republic, Austria, Hungary and Slovakia against 13 resistance genes was investigated. The populations differed mainly at the regional level. Populations from the Czech Republic, mainly from the western regions, showed higher values of virulence against the Pm4b gene. Lower frequency of virulence against Pm4b was found in Austria, and the lowest value was observed in Hungary. The differences in frequencies of virulence against Pm4a and Pm4b showed a similar geographic pattern across the four countries: a continuous decline from west to east and from north to south. Virulence against Pm2 decreased in all countries considered; virulence to pm5, Pm6, Pm8 and Mli was high throughout. Genes and gene combinations that can ensure a relatively effective biological protection against this pathogen across Central Europe at present are Pm3b, Pm2+Mld and Pm1+2+9. Czech and Slovak populations were the most complex: virulence complexity reached a maximum in Slovakia in 1994. A similar evolution, though less significant, was observed in the Czech Republic. Data on complexity of isolates suggest that Central European populations of wheat powdery mildew tend to reach an intermediate level representing the optimal number of virulence genes. This process is probably a consequence of stabilizing selection.     

How low can you go? Estimating impacts of reduced pesticide use

Recent research has suggested that a high proportion of farms can dramatically reduce pesticide applications without reducing crop yields or farm profits. Yet this research has made estimation choices that may systematically bias downwards estimates of the productivity and profitability of pesticides. Fifty years of agricultural economics research provides lessons about how to avoid pitfalls in estimating pesticide productivity. Carefully executed econometric studies have found evidence of overuse, underuse, and near‐optimal use of pesticides in different cropping systems. There are now standard methods to test and correct for sources of biases (either upward or downward) in estimates of pesticide productivity. Ignoring these lessons and methods can seriously bias estimates of the potential for reducing pesticide use at little or no economic cost. © 2018 Society of Chemical Industry     

What have the mechanisms of resistance to glyphosate taught us?

The intensive use of glyphosate alone to manage weeds has selected populations that are glyphosate resistant. The three mechanisms of glyphosate resistance that have been elucidated are (1) target-site mutations, (2) gene amplification and (3) altered translocation due to sequestration. What have we learned from the selection of these mechanisms, and how can we apply those lessons to future herbicide-resistant crops and new mechanisms of action? First, the diversity of glyphosate resistance mechanisms has helped further our understanding of the mechanism of action of glyphosate and advanced our knowledge of plant physiology. Second, the relatively rapid evolution of glyphosate-resistant weed populations provides further evidence that no herbicide is invulnerable to resistance. Third, as new herbicide-resistant crops are developed and new mechanisms of action are discovered, the weed science community needs to ensure that we apply the lessons we have learned on resistance management from the experience with glyphosate. Every new weed management system must be evaluated during development for its potential to select for resistance, and stewardship programs should be in place when the new program is introduced. Copyright © 2011 Society of Chemical Industry     

Breakdown of plant virus resistance: can we predict and extend the durability of virus resistance?

Cultivars with introgressed natural resistance genes have been widely used for plant disease control, especially in the control of virus diseases, for which no effective chemical control agent is available. However, we often encounter virus mutants that break down or overcome the resistance. In this review, recent studies will be discussed with respect to breakdown of plant virus resistance.     

How much of seed dormancy in weeds can be related to seed traits?

Seed dormancy contributes to species persistence in unpredictable environments and is a key process to be taken into account in weed dynamics models. As the level of seed dormancy, photosensitivity and the dates of dormancy induction and release are difficult to measure, our objective was to relate weed seed dormancy with morphological, chemical or physiological seed traits and with expert knowledge. Dormancy of four species was studied experimentally during a 2‐year seed burial experiment. Experiments were supplemented with data from the literature to increase the number of species analysed, resulting in a data set of 29 species. Proportions of non–dormant seeds were higher for elongated than spherical seeds, even when accounting for phylogenetic relatedness between species. Elongated seeds, which tend to remain on the soil surface in undisturbed habitats, may have been selected for lack of dormancy and immediate germination to limit mortality due to predation. Dormancy increased with seed coat thickness, which can act as a chemical and physical barrier to germination, while no relation was found with seed lipid or protein content. No correlation was found between photosensitivity parameters and any of the species traits analysed. Variations in dormancy dates (induction and release) were highly correlated with average field emergence season estimated from expert knowledge. The observed correlations suggest that the level of dormancy results both from direct and from indirect effects of traits being involved in trade‐offs together with seed mortality.     

What is the evidence for sexual reproduction of Phytophthora infestans in Europe?

The biology of late blight of potato and tomato, caused by Phytophthora infestans, changed when sexual reproduction by the pathogen became possible in many parts of the world, including Europe. In northern Europe, especially Scandinavia, there is increasing evidence that the pathogen is reproducing sexually on a regular basis, although in other regions further south or to the west it appears to reproduce primarily in a clonal manner. The presence of both mating types, the production of viable oospores, and observations of fields with soilborne sources of inoculum are consistent with sexual reproduction. Studies with different marker systems have revealed a population structure without any dominating clonal lineages in Scandinavia, and that is most easily explained by sexual reproduction. Phytophthora infestans recovered from the soil can also be linked to parental genotypes using likelihood‐based methods when codominant markers are used. A synthesis of all the available data points to a second centre of sexual reproduction in northern Europe.     

Biological control of plant diseases – What has been achieved and what is the direction?

The global sustainability agenda is increasing the demand for reduction in inputs into agricultural production while maintaining profitable yield of quality products. Plant diseases are a major constraint for both yield and product quality, but often tools for their control are ineffective or lacking. Biological control using antagonistic microorganisms has long been a subject of research resulting in a wide range of products that are now available and marketed in specific territories around the world. These preparations are often niche products with narrow uses. The research effort is intense both to develop new biological control agents (BCAs) and to obtain knowledge of the mechanisms underlying biological disease control. The prospects for biological control are promising. As a minimum, BCAs supplement other sustainable disease management practices such as disease resistance, and present opportunities for controlling diseases for which other approaches are ineffective or unavailable. We can realistically expect increasing use of BCAs to control crop diseases in ways that will benefit the environment. This review paper arose from a webinar held by the British Society for Plant Pathology as part of the International Year of Plant Heath (IYPH2020), at which many of the 300 participants posed or discussed interesting questions. This review is based on that input and the panel members at the webinar are all included as co-authors in this review.     

Fractal dimension and shape parameters of asexual Fusarium spores from selected species: Which species can be distinguished?

Journal of Plant Diseases and Protection - Fungi of the genus Fusarium are prominent plant pathogens producing various toxic secondary metabolites. Digital microscopic images were taken from the...     

The spread of the fall armyworm Spodoptera frugiperda in Africa—What should be done next?

Journal of Plant Diseases and Protection - The following text summarizes the different perspectives of presenters participating in the section Plant Protection in the Tropics and Subtropics, 61st...     

The debate on a loss of biodiversity: can we derive evidence from the monitoring of major plant pests and diseases in major crops?

Journal of Plant Diseases and Protection - The European commission directive EC 128/2009 calls for monitoring pests and pathogens of major crops. The monitoring data may be analysed for trends over...