Search bioRxiv⌕ Search

Biology subjects

McDonald, B. A.

Publications and source records attributed to McDonald, B. A..

36 records · Page 2Linked to original sources

How large and diverse are field populations of fungal plant pathogens? The case of Zymoseptoria tritici

Pathogen populations differ in the amount of genetic diversity they contain. Populations carrying higher genetic diversity are thought to have a greater evolutionary potential than populations carrying less diversity. We used published studies to estimate the range of values associated with two critical components of genetic diversity, the number of unique pathogen genotypes and the number of spores produced during an epidemic, for the septoria tritici blotch pathogen Zymoseptoria tritici. We found that wheat fields experiencing typical levels of infection are likely to carry between 3.2 and 14.9 million pathogen genotypes per hectare and produce at least 2.3 to 10.5 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 x 10-10 substitutions per site per cell division, we estimate that between 28 and 130 million pathogen spores carrying adaptive mutations to counteract fungicides and resistant cultivars will be produced per hectare during a growing season. This suggests that most of the adaptive mutations that have been observed in Z. tritici populations can emerge through local selection from standing genetic variation that already exists within each field. The consequences of these findings for disease management strategies are discussed.

microbiology↗

A transcription factor and a phosphatase regulate temperature-dependent morphogenesis in a fungal plant pathogen

Naturally fluctuating temperatures provide a constant environmental stress that requires adaptation. Some fungal pathogens respond to heat stress by producing new morphotypes that maximize their overall fitness. The fungal wheat pathogen Z. tritici responds to heat stress by switching from its yeast-like blastospore form to hyphae or chlamydospores. The regulatory mechanisms underlying this switch are unknown. Here, we demonstrate that a differential heat stress response is ubiquitous in Z. tritici populations around the world. We used QTL mapping to identify a single locus associated with the temperature-dependent morphogenesis and we found two genes, the transcription factor ZtMsr1 and the protein phosphatase ZtYvh1, regulating this mechanism. We find that ZtMsr1 regulates repression of hyphal growth and induces chlamydospore formation whereas ZtYvh1 is required for hyphal growth. We next pinpointed that chlamydospore formation is a response to the intracellular osmotic stress generated by the heat stress. This intracellular stress stimulates the CWI and HOG MAPK pathways resulting in hyphal growth. If cell wall integrity is however compromised, ZtMsr1 represses the hyphal development program and might induce the chlamydospore-inducing genes as a stress-response survival strategy. Taken together, these results suggest a novel mechanism through which morphological transitions are orchestrated in Z. tritici - a mechanism possibly also present in other pleomorphic fungi. IMPORTANCETemperature is an environmental signal constantly monitored by pleomorphic fungi. Our experiments showed that yeast-to-hyphal or yeast-to-chlamydospore transitions are ubiquitous heat stress responses in Z. tritici. QTL mapping allowed us to identify a transcription factor and a protein phosphatase contributing to temperature-dependent morphogenesis. We showed that intracellular osmolarity is the pivotal signal inducing these transitions. We propose a regulatory network controlling Z. tritici morphogenesis, which may have broad implications for temperature sensing of fungal pathogens.

molecular biology↗

The population genomics of transposable element activation in the highly repressive genome of an agricultural pathogen

The activity of transposable elements (TEs) can be an important driver of genetic diversity with TE-mediated mutations having a wide range of fitness consequences. To avoid deleterious effects of TE activity, some fungi evolved highly sophisticated genomic defences to reduce TE proliferation across the genome. Repeat-induced point (RIP) mutations is a fungal-specific TE defence mechanism efficiently targeting duplicated sequences. The rapid accumulation of RIP mutations is expected to deactivate TEs over the course of a few generations. The evolutionary dynamics of TEs at the population level in a species with highly repressive genome defences is poorly understood. Here, we analyze 366 whole-genome sequences of Parastagonospora nodorum, a fungal pathogen of wheat with efficient RIP. A global population genomics analysis revealed high levels of genetic diversity and signs of frequent sexual recombination. Contrary to expectations for a species with RIP, we identified recent TE activity in multiple populations. The TE composition and copy numbers showed little divergence among global populations regardless of the demographic history. Miniature inverted-repeat transposable elements (MITEs) and terminal repeat retrotransposons in miniature (TRIMs) were largely underlying recent intra-species TE expansions. We inferred RIP footprints in individual TE families and found that recently active, high-copy TEs have possibly evaded genomic defences. We find no evidence that recent positive selection acted on TE-mediated mutations rather that purifying selection maintained new TE insertions at low insertion frequencies in populations. Our findings highlight the complex evolutionary equilibria established by the joint action of TE activity, selection and genomic repression. Data SummaryAll Illumina sequence data is available from the NCBI SRA BioProject numbers PRJNA606320, PRJNA398070 and PRJNA476481 (https://www.ncbi.nlm.nih.gov/bioproject). The Methods and Supplementary Figures S1-S11 and Supplementary Tables S1-S4 provide all information on strain locations and outcomes of genome analyses.

genomics↗

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used multi-trait genome-wide association mapping. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified numerous pleiotropic SNPs with conflicting effects on host colonization and survival in stressful environments. Such genetic constraints are likely limiting the pathogens ability to cause host damage and could be exploited for pathogen control. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.

evolutionary biology↗

A polyetic modelling framework for plant disease emergence

Plant disease emergences have dramatically increased recently as a result of global changes, especially with respect to trade, host genetic uniformity, and climate change. A better understanding of the conditions and processes determining epidemic outbreaks caused by the emergence of a new pathogen, or pathogen strain, is needed to develop strategies and inform decisions to manage emerging diseases. A polyetic process-based model is developed to analyse conditions of disease emergence. This model simulates polycyclic epidemics during successive growing seasons, the yield losses they cause, and the pathogen survival between growing seasons. This framework considers an immigrant strain coming into a system where a resident strain is already established. Outcomes are formulated in terms of probability of emergence, time to emergence, and yield loss, resulting from deterministic and stochastic simulations. An analytical solution to determine a threshold for emergence is also derived. Analyses focus on the effects of two fitness parameters on emergence: the relative rate of reproduction (speed of epidemics), and the relative rate of mortality (decay of population between seasons). Analyses revealed that stochasticity is a critical feature of disease emergence. The simulations suggests that: (1) emergence may require a series of independent immigration events before a successful invasion takes place; (2) an explosion in the population size of the new pathogen (or strain) may be preceded by many successive growing seasons of cryptic presence following an immigration event, and; (3) survival between growing seasons is as important as reproduction during the growing season in determining disease emergence.

ecology↗

Maintenance of variation in virulence and reproduction in populations of an agricultural plant pathogen

Genetic diversity within pathogen populations is critically important for predicting pathogen evolution, disease outcomes and prevalence. However, we lack a good understanding of the processes maintaining genetic variation and constraints on pathogen life-history evolution. Here, we analyzed interactions between 12 wheat host genotypes and 145 strains of Zymoseptoria tritici from five global populations to investigate the evolution and maintenance of variation in pathogen virulence and reproduction. We found a strong positive correlation between virulence and reproduction, with substantial variation in both traits maintained within each pathogen population. On average, highly virulent isolates exhibited higher fecundity, which might increase transmission potential in agricultural fields planted to homogeneous hosts at a high density. We further showed that pathogen strains with a narrow host range (i.e. specialists) for fecundity were on average less virulent, and those with a broader host range (i.e. generalists) for virulence were on average less fecund on a given specific host. These trade-offs costs associated with host specialization might constrain the directional evolution of virulence and fecundity. We conclude that selection favoring pathogen strains that are virulent across diverse hosts, coupled with selection that maximizes fecundity on specific hosts, may explain the maintenance of these pathogenicity traits within and among pathogen populations.

evolutionary biology↗

The genetic architecture of emerging fungicide resistance in populations of a global wheat pathogen

Containing fungal diseases often depends on the application of fungicidal compounds. Fungicides can rapidly lose effectiveness due to the rise of resistant individuals in populations. However, the lack of knowledge about resistance mutations beyond known target genes challenges investigations into pathways to resistance. We used whole-genome sequencing data and association mapping to reveal the multilocus genetic architecture of fungicide resistance in a global panel of 159 isolates of Parastagonospora nodorum, an important fungal pathogen of wheat. We found significant differences in azole resistance among global field populations. The populations evolved distinctive combinations of resistance alleles which can interact synergistically. We identified 34 significantly associated SNPs located in close proximity to genes associated with fungicide resistance in other fungi, including an MFS transporter. Using fungal colony growth rates and melanin production at different temperatures as fitness proxies, we found no evidence that resistance was constrained by genetic trade-offs. Our study demonstrates how genome-wide association studies of a global collection of pathogen strains can recapitulate the emergence of fungicide resistance. The distinct complement of resistance mutations found among populations illustrates how the evolutionary trajectory of fungicide adaptation can be complex and challenging to predict.

genomics↗

SnToxA, SnTox1 and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

The center of origin of the globally distributed wheat pathogen Parastagnospora nodorum has remained uncertain because only a small number of isolates from the Fertile Crescent, a region in the Middle East where wheat was domesticated from wild grasses, were included in earlier population genetic and phylogeographic studies. We isolated and genetically analyzed 193 P. nodorum strains from three naturally infected wheat fields distributed across Iran, a country located within the Fertile Crescent, using eleven neutral microsatellite loci. Compared to previous studies that included populations from North America, Europe, Africa, Australia and China, the populations from Iran had the highest genetic diversity globally and also exhibited greater population structure over smaller spatial scales, patterns typically associated with a species center of origin. Genes encoding the necrotrophic effectors SnToxA, SnTox1 and SnTox3 were found at a high frequency in the Iranian population. By sequencing 96 randomly chosen Iranian strains, we detected new alleles for all three effector genes. Analyses of allele diversity showed that all three effector genes had higher diversity in Iran than in any population included in previous studies, with Iran acting as a hub for the effector diversity that was found in other global populations. Taken together, these findings support the hypothesis that P. nodorum originated either within or nearby the Fertile Crescent with a genome that already encoded all three necrotrophic effectors during its emergence as a pathogen on wheat. Our findings also suggest that P. nodorum was the original source of the ToxA genes discovered in the wheat pathogens Phaeosphaeria avenaria f. sp. tritici 1, Pyrenophora tritici-repentis and Bipolaris sorokiniana.

plant biology↗

Genetic architecture of oxidative stress tolerance in the fungal wheat pathogen Zymoseptoria tritici

Reactive oxygen species are toxic byproducts of aerobic respiration produced during cell growth. They also are an important component of plant defenses to inhibit microbial pathogens. Tolerance to oxidative stress contributes to viability and pathogenicity of plant pathogens. However, the complex molecular network of oxidative stress responses hinders identification of the genes contributing to variation in this trait. Variation in genes affecting responses to oxidative stress is likely to affect the evolutionary potential of pathogen tolerance to host defences. Here, we employed a forward genetic approach to investigate the genetic architecture of oxidative stress tolerance in the fungal wheat pathogen Zymoseptoria tritici. By performing quantitative trait locus (QTL) mapping in two crosses, we identified several genomic regions associated with tolerance to oxidative stress, including a QTL having a large effect on growth under oxidative stress. We found evidence for a significant trade-off between growth under non-stressful conditions and growth inhibition under oxidative stress. We identified a large QTL associated with this trade-off and with growth under non-stressful conditions, suggesting that differences in fungal growth could result in different sensitivities to oxidative stress. Our results suggest that genes related to fungal growth could also contribute to variation in oxidative stress tolerance among fungal strains.

genetics↗

A population-level invasion by transposable elements in a fungal pathogen

AO_SCPLOWBSTRACTC_SCPLOWGenome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici, a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2,456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogens center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.

genomics↗

A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici

BackgroundThe gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. ResultsHere, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only [~]60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable elements content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species. ConclusionsTaken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.

genomics↗

Differential morphological changes in response to environmental stimuli in a fungal plant pathogen

During their life cycles, pathogens have to adapt to many biotic and abiotic environmental stresses to maximize their overall fitness. Morphological transitions are one of the least understood of the many strategies employed by fungal plant pathogens to adapt to constantly changing environments, even though different morphotypes may play important biological roles. We characterized the responses of the wheat pathogen Zymoseptoria tritici to a series of environmental stresses in order to understand the effects of changing environments on fungal morphology and adaptation. We found that all tested stresses induced morphological changes, but different responses were found among four different strains. A transcription analysis showed that morphogenesis and virulence factors are co-regulated. We discovered that Z. tritici forms chlamydospores and demonstrated that these structures are better able to survive extreme cold, heat and drought than other cell types. We also show that blastospores (the \"yeast-like\" form of the pathogen typically found only in laboratory conditions) can form from germinated pycnidiospores on the surface of wheat leaves, suggesting that this morphotype can play an important role in the natural history of Z. tritici. Our findings illustrate how changing environmental conditions can affect cellular morphology and lead to the formation of new morphotypes, with each morphotype having a potential impact on both pathogen survival and disease epidemiology.

microbiology↗

Measuring tolerance to a major fungal pathogen in elite wheat cultivars

O_LITolerance and resistance represent two strategies that hosts evolved to protect themselves from pathogens. Tolerance alleviates the reduction in host fitness due to infection without reducing a pathogens growth, while resistance reduces pathogen growth. We investigated tolerance of wheat to the major fungal pathogen Zymoseptoria tritici in 335 elite wheat cultivars. C_LIO_LIWe used a novel digital phenotyping approach that included 11,152 infected leaves and counted 2,069,048 pathogen fruiting bodies. C_LIO_LIWe discovered a new component of tolerance that is based on the relationship between the green area remaining on a leaf and the number of pathogen fruiting bodies. We found a negative correlation between tolerance and resistance among intolerant cultivars, presenting the first compelling evidence for a tradeoff between tolerance and resistance to plant pathogens. Surprisingly, the tradeoff arises due to limits in the host resources available to the pathogen and not due to metabolic constraints, contrary to what ecological theory suggests. C_LIO_LIThe mechanism underlying this tradeoff may be relevant for many plant diseases in which the amount of host resources available to the pathogen can limit the pathogen population. Our analysis indicates that European wheat breeders may have selected for tolerance instead of resistance to an important pathogen. C_LI

ecology↗

Transposable element insertions shape gene regulation and melanin production in a fungal pathogen

Background\n\nVariation in gene expression contributes to phenotypic diversity within species and adaptation. However, very few cases of adaptive regulatory changes have been reported and the mechanisms underlying variation in gene expression remain largely unexplored. Fungal pathogen genomes are highly plastic and harbour numerous insertions of transposable elements, which can potentially contribute to gene expression regulation. In this work we elucidated how transposable elements contribute to variation of melanin accumulation, a quantitative adaptive trait of fungal pathogens that is involved in survival under stress conditions.\n\nResults\n\nWe demonstrated that differential transcriptional regulation of the gene encoding the transcription factor Zmr1, which controls expression of the genes in the melanin biosynthetic gene cluster, is responsible for variation in melanin accumulation in the fungal plant pathogen Zymoseptoria tritici. We show that differences in melanin levels between two strains of Z. tritici are due to two levels of transcriptional regulation: 1) variation in the promoter sequence of Zmr1, and 2) an insertion of transposable elements upstream of the Zmr1 promoter. Remarkably, independent insertions of transposable elements upstream of Zmr1 occurred in 9% of Z. tritici strains from around the world and negatively regulated Zmr1 expression, contributing to melanin accumulation variation.\n\nConclusions\n\nOur studies demonstrate that different layers of transcriptional control fine-tune the synthesis of melanin. These regulatory mechanisms potentially evolved to balance the fitness costs associated with melanin production against its positive contribution to survival in stressful environments.

molecular biology↗

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

O_LICultivar-strain specificity in the wheat-Zymoseptoria tritici pathosystem determines the infection outcome and is controlled by resistance genes on the host side, of which many have been identified. However, on the pathogen side, the molecular determinants of specificity are largely unknown.\nC_LIO_LIWe used genetic mapping, targeted gene disruption and allele swapping to characterize the recognition of the new avirulence factor Avr3D1. We then combined population genetic and comparative genomic analyses to estimate the evolutionary trajectory of Avr3D1.\nC_LIO_LIAvr3D1 is specifically recognized by cultivars harboring the resistance gene Stb7 and triggers a strong defence response without preventing pathogen infection and reproduction. Avr3D1 resides in a cluster of putative effector genes located in a region populated by independent transposable element insertions. The gene is present in all 132 investigated strains and is highly polymorphic, with a total of 30 different protein variants. We demonstrated that certain amino acid mutations in Avr3D1 led to evasion of recognition.\nC_LIO_LIThese results demonstrate that quantitative resistance and gene-for-gene interactions are not mutually exclusive per se. Location of avirulence genes in highly plastic genomic regions likely facilitates accelerated evolution that enables escape from recognition by resistance proteins.\nC_LI

plant biology↗

Genome-wide detection of genes under positive selection in worldwide populations of the barley scald pathogen

The coevolution between hosts and pathogens generates strong selection pressures to maintain resistance and infectivity, respectively. Genomes of plant pathogens often encode major effect loci for the ability to successfully infect a specific host. Hence, heterogeneity in the host genotypes and abiotic factors leads to locally adapted pathogen populations. However, the genetic basis of local adaptation is poorly understood. We analyzed global field populations of Rhynchosporium commune, the pathogen causing barley scald disease, to identify candidate genes for local adaptation. Whole genome sequencing data generated for 125 isolates showed that the pathogen is subdivided into three genetic clusters associated with distinct geographic and climatic regions. Using haplotype-based selection scans applied independently to each genetic cluster, we found strong evidence for selective sweeps throughout the genome. Comparisons of loci under selection among clusters revealed little overlap, suggesting that ecological differences associated with each cluster led to variable selection regimes. The strongest signals of selection were found predominantly in the two clusters composed of isolates from Central Europe and Ethiopia. The strongest selective sweep regions encoded proteins with functions related to both biotic and abiotic stresses. We found that selective sweep regions were enriched in genes encoding functions in cellular localization, protein transport activity, and DNA damage responses. In contrast to the prevailing view that a small number of gene-for-gene interactions govern plant pathogen evolution, our analyses suggest that the evolutionary trajectory is largely determined by spatially heterogeneous biotic and abiotic selection pressures.

genomics↗

Meiosis leads to pervasive segregation distortion and copy-number variation in accessory chromosomes of the wheat pathogen Zymoseptoria tritici

Meiosis is one of the most conserved molecular processes in eukaryotes. The fidelity of pairing and segregation of homologous chromosomes has a major impact on the proper transmission of genetic information. Aberrant chromosomal transmission can have major phenotypic consequences, yet the mechanisms are poorly understood. Fungi are excellent models to investigate processes of chromosomal transmission, because many species have highly polymorphic genomes that include accessory chromosomes. Inheritance of accessory chromosomes is often unstable and chromosomal losses have little impact on fitness. We analyzed chromosomal inheritance in 477 progeny coming from two crosses of the fungal wheat pathogen Zymoseptoria tritici. For this, we developed a high-throughput screening method based on restriction site associated DNA sequencing (RAD-seq) that generated dense coverage of genetic markers along each chromosome. We identified rare instances of chromosomal duplications (disomy) in core chromosomes. Accessory chromosomes showed high overall frequencies of disomy. Chromosomal rearrangements were found exclusively on accessory chromosomes and were more frequent than disomy. Accessory chromosomes present in only one of the parents in an analyzed cross were inherited at significantly higher rates than the expected 1:1 segregation ratio. Both the chromosome and the parental background had significant impacts on the rates of disomy, losses, rearrangements and segregation distortion. We found that chromosomes with higher sequence similarity and lower repeat content were inherited more faithfully. The large number of rearranged progeny chromosomes identified in this species will enable detailed analyses of the mechanisms underlying chromosomal rearrangement.

evolutionary biology↗

Ranking quantitative resistance to Septoria tritici blotch in elite wheat cultivars using automated image analysis

Quantitative resistance is likely to be more durable than major gene resistance for controlling Septoria tritici blotch (STB) on wheat. Earlier studies hypothesized that resistance affecting the degree of host damage, as measured by the percentage of leaf area covered by STB lesions, is distinct from resistance that affects pathogen reproduction, as measured by the density of pycnidia produced within lesions. We tested this hypothesis using a collection of 335 elite European winter wheat cultivars that was naturally infected by a diverse population of Zymoseptoria tritici in a replicated field experiment. We used automated image analysis (AIA) of 21420 scanned wheat leaves to obtain quantitative measures of conditional STB intensity that were precise, objective, and reproducible. These measures allowed us to explicitly separate resistance affecting host damage from resistance affecting pathogen reproduction, enabling us to confirm that these resistance traits are largely independent. The cultivar rankings based on host damage were different from the rankings based on pathogen reproduction, indicating that the two forms of resistance should be considered separately in breeding programs aiming to increase STB resistance. We hypothesize that these different forms of resistance are under separate genetic control, enabling them to be recombined to form new cultivars that are highly resistant to STB. We found a significant correlation between rankings based on automated image analysis and rankings based on traditional visual scoring, suggesting that image analysis can complement conventional measurements of STB resistance, based largely on host damage, while enabling a much more precise measure of pathogen reproduction. We showed that measures of pathogen reproduction early in the growing season were the best predictors of host damage late in the growing season, illustrating the importance of breeding for resistance that reduces pathogen reproduction in order to minimize yield losses caused by STB. These data can already be used by breeding programs to choose wheat cultivars that are broadly resistant to naturally diverse Z. tritici populations according to the different classes of resistance.

plant biology↗