Search

The fungal pathogen Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB), a major wheat disease in Western Europe. Microorganisms inhabiting wheat leaves might act as beneficial, biocontrol, or facilitating agents that could limit or stimulate the development of Z. tritici. Improving our understanding of microbial communities in the wheat phyllosphere would lead to new insights into STB management. This article provides fungal and bacterial metabarcoding datasets obtained by sampling wheat leaves with and without symptoms caused by Z. tritici. Tissues were sampled from three commercial wheat varieties on three sampling dates during a cropping season. Weeds around wheat fields were sampled as well. In total, more than 450 leaf samples were collected. The pathogen Z. tritici was quantified using quantitative PCR. We provide the raw metabarcoding datasets, the amplicon sequence variant tables obtained after bioinformatic processing, the metadata associated with each sample (sampling date, wheat variety and tissue health condition), a preliminary descriptive analysis of the data, and the code used for bioinformatic and descriptive statistical analysis. [Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Abstract Dispersal is a key ecological process, but it remains difficult to measure. By recording numbers of dispersed individuals at different distances from the source, one acquires a dispersal gradient. Dispersal gradients contain information on dispersal, but they are influenced by the spatial extent of the source. How can we separate the two contributions to extract knowledge about dispersal? One could use a small, point‐like source for which a dispersal gradient represents a dispersal kernel, which quantifies the probability of an individual dispersal event from a source to a destination. However, the validity of this approximation cannot be established before conducting measurements. This represents a key challenge hindering progress in characterization of dispersal. To overcome it, we formulated a theory that incorporates the spatial extent of sources to estimate dispersal kernels from dispersal gradients. Using this theory, we re‐analyzed published dispersal gradients for three major plant pathogens. We demonstrated that the three pathogens disperse over substantially shorter distances compared to conventional estimates. This method will allow the researchers to re‐analyze a vast number of existing dispersal gradients to improve our knowledge about dispersal. The improved knowledge has potential to advance our understanding of species' range expansions and shifts, and inform management of weeds and diseases in crops.

Zymoseptoria tritici is an important fungal pathogen of wheat which has spread globally. Here, the authors perform genomic analyses on a collection of ~1100 Z. tritici samples from 42 countries to describe its global spread and elucidate mechanisms of adaptation to different environmental conditions.

Septoria leaf blotch is a foliar wheat disease controlled by a combination of plant genetic resistances and fungicides use. R-gene-based qualitative resistance durability is limited due to gene-for-gene interactions with fungal avirulence (Avr) genes. Quantitative resistance is considered more durable but the mechanisms involved are not well documented. We hypothesize that genes involved in quantitative and qualitative plant-pathogen interactions are similar. A bi-parental population of Zymoseptoria tritici was inoculated on wheat cultivar ‘Renan’ and a linkage analysis performed to map QTL. Three pathogenicity QTL, Qzt-I05-1, Qzt-I05-6 and Qzt-I07-13, were mapped on chromosomes 1, 6 and 13 in Z. tritici, and a candidate pathogenicity gene on chromosome 6 was selected based on its effector-like characteristics. The candidate gene was cloned by Agrobacterium tumefaciens-mediated transformation, and a pathology test assessed the effect of the mutant strains on ‘Renan’. This gene was demonstrated to be involved in quantitative pathogenicity. By cloning a newly annotated quantitative-effect gene in Z. tritici that is effector-like, we demonstrated that genes underlying pathogenicity QTL can be similar to Avr genes. This opens up the previously probed possibility that ‘gene-for-gene’ underlies not only qualitative but also quantitative plant-pathogen interactions in this pathosystem.

Capacity for dispersal is a fundamental fitness component of plant pathogens. Characterization of plant pathogen dispersal is important for understanding how pathogen populations change in time and space. We devised a systematic approach to measure and analyze rain splash-driven dispersal of plant pathogens in field conditions, using the major fungal wheat pathogen Zymoseptoria tritici as a case study. We inoculated field plots of wheat (Triticum aestivum) with two distinct Z. tritici strains. Next, we measured disease intensity as counts of fruiting bodies (pycnidia) using automated image analysis. These measurements characterized primary disease gradients, which we used to estimate effective dispersal of the pathogen population. Genotyping of reisolated pathogen strains with strain-specific PCR confirmed the conclusions drawn from phenotypic data. Consistently with controlled environment studies, we found that the characteristic scale of dispersal is tens of centimeters. We analyzed the data using a spatially explicit mathematical model that incorporates the spatial extent of the source, rather than assuming a point source, which allows for a more accurate estimation of dispersal kernels. We employed bootstrapping methods for statistical testing and adopted a two-dimensional hypotheses test based on kernel density estimation, enabling more robust inference compared with standard methods. We report the first estimates of dispersal kernels of the pathogen in field conditions. However, repeating the experiment in other environments would lead to more robust conclusions. We put forward advanced methodology that paves the way for further measurements of plant pathogen dispersal in field conditions, which can inform spatially targeted plant disease management. [Figure: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.

Abstract Plant pathogen populations inhabit patchy environments with contrasting, variable thermal conditions. We investigated the diversity of thermal responses in populations sampled over contrasting spatiotemporal scales, to improve our understanding of their dynamics of adaptation to local conditions. Samples of natural populations of the wheat pathogen Zymoseptoria tritici were collected from sites within the Euro‐Mediterranean region subject to a broad range of climatic conditions. We tested for local adaptation, by accounting for the diversity of responses at the individual and population levels on the basis of key thermal performance curve parameters and “thermotype” (groups of individuals with similar thermal responses) composition. The characterization of phenotypic responses and genotypic structure revealed the following: (i) a high degree of individual plasticity and variation in sensitivity to temperature conditions across spatiotemporal scales and populations; and (ii) geographic variation in thermal response among populations, with major alterations due to seasonal patterns over the wheat‐growing season. The seasonal shifts in functional composition suggest that populations are locally structured by selection, contributing to adaptation patterns. Further studies combining selection experiments and modeling are required to determine how functional group selection drives population dynamics and adaptive potential in response to thermal heterogeneity.

The negative contribution of crop residues as a source of inoculum for plant diseases is well established. However, microbial ecologists have long reported positive effects of residues on the stability of agrosystems and conservation tillage practices have become increasingly widespread. Most studies have suggested that large microbial communities should be taken into account in plant disease management, but we know little about their ecological interaction with pathogens in the crop residue compartment. This review focuses on microbiomes associated with residues within the context of other microbial habitats in cereal-producing agroecosystems such as phyllosphere or rhizosphere. We connected residue microbiome with the survival of residue-borne fungal plant pathogens, thus combining knowledge in microbial ecology and epidemiology, two disciplines still not sufficiently connected. We provide an overview of the impact of residues on cereal disease epidemics and how dynamic interactions between microbial communities of nonburied residues during their degradation, along with soil and multitude of abiotic factors, can contribute to innovative disease management strategies, including next-generation microbiome-based biocontrol strategies. Starting from the classical but still relevant view of crop residues as a source of pathogen inoculum, we first consider possibilities for limiting the amount of residues on the soil surface to reduce the pathogen pressure. We then describe residues as a transient half-plant/half-soil compartment constituting a key fully fledged microbial ecosystem: in other words, an ecotone which deserves special attention. We focus on microbial communities, the changes in these communities over time and the factors influencing them. Finally, we discuss how the interactions between the microbial communities and the pathogens present on residues could be used: identification of keystone taxa and beneficial assemblages, then preservation of these taxa by adapted agronomic practices or development of synthetic communities, rather than the introduction of a single exogenous biocontrol species designed as a treatment product.

Abstract Background Wheat residues are a crucial determinant of the epidemiology of Septoria tritici blotch, as they support the sexual reproduction of the causal agent Zymoseptoria tritici. We aimed to characterize the effect of infection with this fungal pathogen on the microbial communities present on wheat residues and to identify microorganisms interacting with it. We used metabarcoding to characterize the microbiome associated with wheat residues placed outdoors, with and without preliminary Z. tritici inoculation, comparing the first set of residues in contact with the soil and a second set without contact with the soil, on four sampling dates in two consecutive years. Results The diversity of the tested conditions, leading to the establishment of different microbial communities according to the origins of the constitutive taxa (plant only, or plant and soil), highlighted the effect of Z. tritici on the wheat residue microbiome. Several microorganisms were affected by Z. tritici infection, even after the disappearance of the pathogen. Linear discriminant analyses and ecological network analyses were combined to describe the communities affected by the infection. The number of fungi and bacteria promoted or inhibited by inoculation with Z. tritici decreased over time and was smaller for residues in contact with the soil. The interactions between the pathogen and other microorganisms appeared to be mostly indirect, despite the strong position of the pathogen as a keystone taxon in networks. Direct interactions with other members of the communities mostly involved fungi, including other wheat pathogens. Our results provide essential information about the alterations to the microbial community in wheat residues induced by the mere presence of a fungal pathogen, and vice versa. Species already described as beneficial or biocontrol agents were found to be affected by pathogen inoculation. Conclusions The strategy developed here can be viewed as a proof-of-concept focusing on crop residues as a particularly rich ecological compartment, with a high diversity of fungal and bacterial taxa originating from both the plant and soil compartments, and for Z. tritici-wheat as a model pathosystem. By revealing putative antagonistic interactions, this study paves the way for improving the biological control of residue-borne diseases.

This study combined culture-dependent (strain isolation plus molecular identification) and culture-independent (metabarcoding) approaches to characterize the diversity of microbiota on wheat and oilseed rape residues. The goal was to develop a methodology to culture microorganisms with the aim of being able to establish synthetic crop residue microbial communities for further study, i.e., testing potential interactions within these communities and characterizing groups of beneficial taxa that could be used as biological control agents against plant pathogens. We generated community-based culture collections. We adapted the isolation strategy to the potential differences in the spatial and temporal distribution of diversity between bacteria and fungi. We performed (i) a high-throughput isolation from few samples with no a priori for bacteria and (ii) a low-throughput isolation from several samples with a priori—i.e., morphotype selection—for fungi. Although isolation using a single medium did not allow us to characterize the microbiome as precisely as metabarcoding, the bacterial diversity (158 ASVs, 36 genera) was relatively higher than the fungal diversity (131 ASVs, 17 genera) known to be limited by competition for growth on non-selective solid media. Isolation and metabarcoding provided consistent and complementary information: they revealed several common but also specific ASVs, leading to close microbial community profiles of the most abundant fungal and bacterial taxa in residues. Finally, by empirically comparing the different profiles, we assessed the cultivability of the most abundant fungal and bacterial taxa obtained in metabarcoding.

Fungal genus Septoria causes diseases in a wide range of plants. Here, we report the first genome sequences of two strains of Septoria linicola, the causal agent of the pasmo disease of flax (Linum usitatissimum). The genome of the first strain, SE15195, was fully assembled in 16 chromosomes, while 35 unitigs were obtained for a second strain, SE14017. Structural annotations predicted 13,096 and 13,085 protein-encoding genes and transposable elements content of 19.0 and 18.1% of the genome for SE15195 and SE14017, respectively. The four smaller chromosomes 13 to 16 show genomics features of potential accessory chromosomes. The assembly of these two genomes is a new resource for studying S. linicola and improving management of pasmo. [Graphic: see text] Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Abstract 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 3.1 and 14.0 million pathogen genotypes per hectare and produce at least 2.1–9.9 trillion pycnidiospores per hectare. Given the experimentally derived mutation rate of 3 × 10−10 substitutions per site per cell division, we estimate that between 27 and 126 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.

The increased emergence of cereal stem rust in southern and western Europe, caused by the pathogen Puccinia graminis, and the prevalence of alternate (sexual) host, Berberis species, have regained attention as the sexual host may serve as source of novel pathogen variability that may pose a threat to cereal supply. The main objective of the present study was to investigate the functional role of Berberis species in the current epidemiological situation of cereal stem rust in Europe. Surveys in 11 European countries were carried out from 2018 to 2020, where aecial infections from five barberry species were collected. Phylogenetic analysis of 121 single aecial clusters of diverse origin using the elongation factor 1-α gene indicated the presence of different special forms (aka formae speciales) of P. graminis adapted to different cereal and grass species. Inoculation studies using aecial clusters from Spain, United Kingdom, and Switzerland resulted in 533 stem rust isolates sampled from wheat, barley, rye, and oat, which confirmed the presence of multiple special forms of P. graminis. Microsatellite marker analysis of a subset of 192 sexually-derived isolates recovered on wheat, barley and rye from the three populations confirmed the generation of novel genetic diversity revealed by the detection of 135 multilocus genotypes. Discriminant analysis of principal components resulted in four genetic clusters, which grouped at both local and country level. Here, we demonstrated that a variety of Berberis species may serve as functional alternate hosts for cereal stem rust fungi and highlights the increased risks that the sexual cycle may pose to cereal production in Europe, which calls for new initiatives within rust surveillance, epidemiological research and resistance breeding.

Abstract  Carrot cavity spot (CCS) is one of the most important soilborne diseases affecting the carrot crop. The few epidemiological studies that have investigated the temporal and spatial dynamics of the disease have been based solely on diagrammatic scales or semi-quantitative indices. To reveal epidemiological processes involved in the development of CCS epidemics, we investigated pathometric relationships. To this end, standardised measurements were defined (disease incidence i, lesion density d, conditional lesion density cd, lesion size ls, and total diseased area tda). The evolution of a cohort of CCS lesions according to their size suggested that lesions can expand over time. Two pathometric relationships were tested: a first one, between i and tda, is given by the equation i = 100(1−exp(−a(t)tda)), where t is thermal time, and a second one, between tda, d, and ls, is given by the equation tda = c(t)πd(ls/2)2. These relationships were validated for CCS epidemics in the case of field experiments, a survey in commercial fields, and a controlled-conditions experiment. The temporal linear decrease of the time-dependent parameter a(t) in the first relationship suggested that CCS epidemics followed classical epidemiological phases driven by successive processes: (1) the mobilisation of soil inoculum leading to primary infection, (2) the spread of disease to neighbouring taproots (alloinfection), and (3) the intensification of disease on the taproot (autoinfection). This is consistent with complementary experimental results which demonstrated that auto- and alloinfections occur in CCS epidemics. [ABSTRACT FROM AUTHOR]