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Feurtey, A.

Publications and source records attributed to Feurtey, A..

17 recordsLinked to original sources

Contrasting transcriptional responses and genetic determinants underlie Zymoseptoria tritici adaptation mechanisms to simulated host defense environments

Successful colonization of the wheat apoplast requires that Zymoseptoria tritici tolerate host-derived stresses, but the mechanisms underlying this adaptation remain poorly understood. We combined phenotypic assays, transcriptomics, and genome-wide association analyses to characterize fungal responses to acidic pH, salicylic acid, gibberellic acid, and oxidative stress. Exposure to salicylic acid inhibited in vitro growth across a global collection of 411 Z. tritici strains, whereas acidic pH promoted growth, illustrating contrasting effects on pathogen performance of environments simulating host-defense responses. At the transcriptional level, acidic pH and oxidative stress induced the strongest and most similar responses, while salicylic acid elicited a more distinct transcriptional program and gibberellic acid caused only limited transcriptional changes. Although the sets of differentially expressed genes were largely condition specific, overlapping enrichment of transport- and redox-related functions across conditions indicated shared transcriptional responses. K-mer based genome-wide association mapping identified five candidate loci associated with growth under acidic pH, gibberellic acid and salicylic acid, including four loci specific to a single growth condition. These loci colocalized with genes implicated in cell wall remodeling, nitrogen metabolite regulation, proteostasis, and ubiquitin-related processes. This study highlights the multifaceted strategies employed by Z. tritici to navigate environments simulating host-defense responses, involving shared and environment-specific adaptations. We provide new insights into the genetic and molecular basis of fungal resilience, with implications for understanding pathogen-host interactions.

genomics↗

A large European diversity panel reveals complex azole fungicide resistance gains of a major wheat pathogen

Fungicide resistance in crop pathogens poses severe challenges to sustainable agriculture. Demethylation inhibitors (DMIs) are critical for controlling crop diseases but face rapid resistance gains in the field. Even though the main molecular basis of resistance is well established, field surveys have repeatedly revealed alternative resistance mechanisms. The European continent in particular has seen rapid and heterogeneous gains in azole resistance in the past decades. Here, we establish a large genome panel to dissect the genetic architecture of emerging resistance in the major wheat pathogen Zymoseptoria tritici. The European diversity panel spans 15 sampling years and 27 countries for a total of 1394 sequenced and phenotyped strains. Using two complementary assays to quantify resistance levels of each strain, we captured fine-grained shifts in DMI resistance over space and time. We conducted genome-wide association studies based on a comprehensive set of genotyping approaches for six DMIs. We mapped a total of 21,220 genetic variants and 158 genes linked to resistance. The substantial scope in genetic mechanisms underpinning DMI resistance significantly expands our mechanistic understanding how continent-wide resistance arises in fungal pathogens over time. Diversification of the Cyp51 coding sequence was particularly striking with new resistant haplotypes emerging with complex configurations and geographic patterns. This study provides expansive new insights into fungicide resistance gains of crop pathogens relevant for future resistance management strategies.

microbiology↗

Responses to temperature shocks in Zymoseptoria tritici reveal specific transcriptional reprogramming and novel candidate genes for thermal adaptation

Pathogens responses to sudden temperature fluctuations, spanning various temporal scales, are critical determinants of their survival, growth, reproduction, and homeostasis. Here, we combined phenotyping, transcriptomics, and genome-wide association approaches to investigate how the wheat pathogen Zymoseptoria tritici responds to and recovers from temperature shocks. Survival emerged as the most significantly affected trait immediately following temperature shocks across 122 geographically diverse strains. In contrast, post-recovery phenotypic traits, including growth rate and melanization, showed no significant deviations from control conditions. Transcriptomic analyses of a reference strain revealed temperature stress-specific gene expression patterns, with genes involved in protein folding, redox homeostasis, membrane stabilization, and cell-wall remodeling playing central roles in the response. A multi-reference k-mer genome-wide association study (GWAS) identified six loci significantly associated with cold shock responses. Among these, two loci emerged as strong candidates for near-freezing temperature adaptation, including a 60S ribosomal protein gene involved in protein synthesis and stress recovery, and an NADH oxidoreductase gene implicated in redox homeostasis and oxidative stress tolerance. These findings shed light on the distinct molecular strategies Z. tritici employs to adapt to temperature stress and provide novel insights into fungal resilience under dynamic environmental conditions. Author summaryTemperature fluctuations, an inherent aspect of natural environments, are increasingly exacerbated by climate change, intensifying challenges for organisms to maintain homeostasis amid more frequent and severe extreme weather events. This study reveals distinct phenotypic, transcriptomic, and genetic mechanisms underlying Z. triticis responses to short-term temperature shocks. Survival-related phenotypic traits were significantly reduced by heat and cold shocks, while other traits measured after a recovery period demonstrated the resilience of Z. tritici strains to temperature stress, reflecting efficient recovery mechanisms. Transcriptomic analyses uncovered temperature-specific gene expression patterns, emphasizing unique regulatory strategies, which mostly return to baseline levels after a recovery period. The discovery of novel loci associated with cold shock responses provides valuable insights into the genetic basis of resilience to short-term temperature stress, offering a foundation for future research on pathogen adaptation to fluctuating environments.

genomics↗

Interspecies hybridization as a route of accessory chromosome origin in fungal species infecting wild grasses

Many fungal plant pathogens have dynamic genomic architectures that can contribute to rapid evolution and adaptation to new niches. Zymoseptoria tritici, an important fungal pathogen of wheat, has a compartmentalized and rapidly evolving genome. In the genome of the reference isolate Z. tritici IPO323, 8 of the 21 chromosomes are accessory. In spite of the profound impact on genome organization, the origin of accessory chromosomes in Z. tritici is still poorly understood. Combining genomics, transcriptomics and epigenomics, we discovered a new chromosome in Z. tritici isolates infecting wild grasses from the genus Aegilops, and we use this discovery to study the origin of accessory chromosomes. The newly identified chromosome presents similar characteristics to known accessory chromosomes in Zymoseptoria species, including presence-absence variation, low gene expression in vitro and in planta, and enrichment with heterochromatin-associated histone methylation marks (H3K27me3). Interestingly, we found an orthologous chromosome in Zymoseptoria ardabiliae, a closely related fungal species also infecting wild grasses. This ortholog chromosome also presents accessory chromosomes characteristics, but lacks the enrichment of heterochromatin-associated methylation marks. Transcriptomic analyses revealed that the orthologous chromosome in Z. ardabiliae harbors active transposable elements (TEs) congruent with lower signatures of host-genome defense mechanisms against TE expansion and spread (quantified as repeat-induced-point (RIP) mutation signatures). Our findings suggest that the chromosome has been exchanged between Z. tritici and Z. ardabiliae by introgressive hybridization events underlining the relevance of hybridization in the evolution of new accessory chromosomes. We speculate that the regulation of TEs has not yet occurred on this new accessory chromosome in Z. ardabiliae, contributing to its rapid evolution.

evolutionary biology↗

Host specialization defines the emergence of new fungal plant pathogen populations

Host-driven selection can be considered a strong driver of pathogen evolution. To successfully infect, colonize and complete their life cycle, plant pathogens are under constant selective pressures imposed by hosts, leading to genetic adaptation and possibly lineage radiation or speciation. Population and comparative genomics approaches are powerful tools to identify signatures of selection associated with host specialization in pathogen genomes and further allow recapturing population histories. Implementing such approaches, we identified evolutionary signatures of divergent host specialisation in distinct lineages of the fungal pathogen Zymoseptoria tritici, a major disease causing-agent of wheat. Unique collections of Z. tritici were isolated from wild (Aegilops spp.) and domesticated (Triticum aestivum) host grasses in the Middle East and whole-genome sequencing was performed in a selected subset of isolates from each collection. We observed distinct population structure between the two host-diverging pathogens and identified particular genomic features in the Aegilops-infecting isolates that may have shaped their evolutionary history. Phylogenomic analyses revealed that A. cylindrica and A. tauchii -infecting populations of Z. tritici form separate clusters, possibly reflecting incipient speciation driven by divergent host specialization. Using infection experiments, we confirm that Z. tritici isolates collected from Aegilops spp. only infect their respective host species and not T. aestivum. Population genomics analyses and demographic inference furthermore allowed us to detect signatures of recent selection and show that divergence of the wheat-infecting lineage likely coincided with wheat domestication. At last, we confirm a virulence-related role for one candidate effector located in a selective sweep region of the A. cylindrica-infecting pathogen. Taken together, our findings highlight the interplay between agricultural and wild hosts on the evolution of fungal plant pathogens and illustrate host specialization as a possible route of rapid pathogen emergence.

evolutionary biology↗

Thermal adaptation in worldwide collections of a major fungal pathogen

Adaptation to new climates poses a significant challenge for plant pathogens during range expansion, highlighting the importance of understanding their response to climate to accurately forecast future disease outbreaks. The wheat pathogen Zymoseptoria tritici is ubiquitous across most wheat production regions distributed across diverse climate zones. We explored the genetic architecture of thermal adaptation using a global collection of 411 Z. tritici strains that were phenotyped across a wide range of temperatures and then included in a genome-wide association study. Our analyses provided evidence for local thermal adaptation in Z. tritici populations worldwide, with a significant positive correlation between bioclimatic variables and optimal growth temperatures. We also found a high variability in thermal performance among Z. tritici strains coming from the same field populations, reflecting the high evolutionary potential of this pathogen at the field scale. We identified 69 genes putatively involved in thermal adaptation, including one high-confidence candidate potentially involved in cold adaptation. These results highlight the complex polygenic nature of thermal adaptation in Z. tritici and suggest that this pathogen is likely to adapt well when confronted with climate change.

genomics↗

Copy number variation introduced by a massive mobile element underpins global thermal adaptation in a fungal wheat pathogen

Copy number variation (CNV) can drive rapid evolution in changing environments. In microbial pathogens, such adaptation is a key factor underpinning epidemics and colonization of new niches. However, the genomic determinants of such adaptation remain poorly understood. Here, we systematically investigate CNVs in one of the largest to date genome sequencing dataset spanning a worldwide collection of 1109 genomes from the major wheat pathogen Zymoseptoria tritici. We found overall strong purifying selection acting on most CNVs. Genomic defense mechanisms likely accelerated gene loss over episodes of continental colonization. Local adaptation along climatic gradients was facilitated by CNVs affecting secondary metabolite production and gene loss in general. One of the strongest candidates for climatic adaptation is a highly conserved gene of the NAD-dependent Sirtuin family. The Sirtuin CNV locus localizes to an [~]68-kb Starship mobile element unique to the species carrying genes highly expressed during plant infection. The element has likely lost the ability to transpose, demonstrating how the ongoing domestication of cargo-carrying selfish elements can contribute to selectable variation within populations. Our work highlights how standing variation in gene copy numbers at the global scale is a major factor driving climatic and metabolic adaptation in microbial species.

evolutionary biology↗

Emergence and spread of the barley net blotch pathogen coincided with crop domestication and cultivation history

Fungal pathogens cause devastating disease in crops. Understanding the evolutionary origin of pathogens is essential to the prediction of future disease emergence and the potential of pathogens to disperse. The fungus Pyrenophora teres f. teres causes net form net blotch (NFNB), an economically significant disease of barley. In this study, we have used 104 P. teres f. teres genomes from four continents to explore the population structure and demographic history of the fungal pathogen. We showed that P. teres f. teres is structured into populations that tend to be geographically restricted to different regions. Using Multiple Sequentially Markovian Coalescent and machine learning approaches we demonstrated that the demographic history of the pathogen correlates with the history of barley, highlighting the importance of human migration and trade in spreading the pathogen. Exploring signatures of natural selection, we identified several population-specific selective sweeps that colocalized with genomic regions enriched in putative virulence genes, and loci previously identified as determinants of virulence specificities by quantitative trait locus analyses. This reflects rapid adaptation to local hosts and environmental conditions of P. teres f. teres as it spread with barley. Our research highlights how human activities can contribute to the spread of pathogens that significantly impact the productivity of field crops.

evolutionary biology↗

Segmental Duplications Drive the Evolution of Accessory Regions in a Major Crop Pathogen

O_LIMany pathogens evolved compartmentalized genomes with conserved core and variable accessory regions which carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such accessory regions often spanning entire chromosomes. The presence of specific accessory regions influences the host range, and horizontal transfer of some accessory regions can modify the pathogenicity of the receiving strain. However, understanding how these accessory regions evolve in strains that infect the same host remains limited. C_LIO_LIHere, we define the pan-genome of 69 diverse Fusarium strains that cause Fusarium wilt of banana, a significant constraint to global banana production. In this diverse panel of Fusarium strains infecting banana, we analyzed the diversity and evolution of the accessory regions. C_LIO_LIAccessory regions in Fusarium strains infecting the same banana cultivar are highly diverse, and we could not identify any shared genomic regions and in planta induced effectors. We demonstrate that segmental duplications drive the evolution of accessory regions. Furthermore, we show that recent segmental duplications and aneuploidy occur specifically in accessory chromosomes and cause the expansion of accessory regions in F. oxysporum. C_LIO_LITaken together we conclude that extensive recent duplications drive the evolution of accessory regions in Fusarium, which contribute to the evolution of virulence. C_LI

genomics↗

Improved gene annotation of the fungal wheat pathogen Zymoseptoria tritici based on combined Iso-Seq and RNA-Seq evidence

Despite large omics datasets, the establishment of a reliable gene annotation is still challenging for eukaryotic genomes. Here, we used the reference genome of the major fungal wheat pathogen Zymoseptoria tritici (isolate IPO323) as a case study to develop methods to improve eukaryotic gene prediction. Four previous IPO323 annotations identified 10,933 to 13,260 gene models, but only one third of these coding sequences (CDS) have identical structures. To resolve these discrepancies and improve gene models, we generated full-length transcripts using long-read sequencing. This dataset was used together with other evidence (RNA-Seq transcripts and protein sequences) to generate novel ab initio gene models. The selection of the best structure among novel and existing gene models was performed according to transcript and protein evidence using InGenAnnot, a novel bioinformatics suite. Overall, 13,414 re-annotated gene models (RGMs) were predicted, including 671 new genes among which 53 encoded effector candidates. This process corrected many of the errors (15%) observed in previous gene models (coding sequence fusions, false introns, missing exons). While fungal genomes have poor annotations of untranslated regions (UTRs), our Iso-Seq long-read sequences outlined 5 and 3UTRs for 73% of the RGMs. Alternative transcripts were identified for 13% of RGMs, mostly due to intron retention (75%), likely corresponding to unprocessed pre-mRNAs. A total of 353 genes displayed alternative transcripts with combinations of previously predicted or novel exons. Long non-coding transcripts (lncRNAs) and double-stranded RNAs from two fungal viruses were also identified. Most lncRNAs corresponded to antisense transcripts of genes (52%). lncRNAs that were up or down regulated during infection were enriched in antisense transcripts (70%), suggesting their involvement in the control of gene expression. Our results showed that combining different ab initio gene predictions and evidence-driven curation using InGenAnnot improved the quality of gene annotations of a compact eukaryotic genome. Our analysis also provided new insights into the transcriptional landscape of Z. tritici, helping develop an increasingly complex picture of its biology.

genomics↗

Recent reactivation of a pathogenicity-associated transposable element triggers major chromosomal rearrangements in a fungal wheat pathogen

Transposable elements (TEs) are key drivers of genomic variation contributing to recent adaptation in most species. Yet, the evolutionary origins and insertion dynamics within species remain poorly understood. We recapitulate the spread of the pathogenicity-associated Styx element across five species that last diverged [~]11,000 years ago. We show that the element likely originated in the Zymoseptoria fungal pathogen genus and underwent multiple independent reactivation events. Using a global 900-genome panel of the wheat pathogen Z. tritici, we assess Styx copy number variation and identify renewed transposition activity in Oceania and South America. We show that the element can mobilize to create additional Styx copies in a four-generation pedigree. Importantly, we find that new copies of the element are not affected by genomic defenses revealing a recent loss of control against the element. Styx copies are preferentially located in recombination breakpoints and likely triggered multiple types of large chromosomal rearrangements. Taken together, we establish the origin, diversification, and reactivation of a highly active TE with major consequences for chromosomal integrity and the expression of disease.

genomics↗

A thousand-genome panel retraces the global spread and climatic adaptation of a major crop pathogen

Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen.

genomics↗

Dynamics of transposable elements in recently diverged fungal pathogens: lineage-specific transposable element content and efficiency of genome defences

Transposable elements (TEs) impact genome plasticity, architecture and evolution in fungal plant pathogens. The wide range of TE content observed in fungal genomes reflects diverse efficacy of host-genome defence mechanisms that can counter-balance TE expansion and spread. Closely related species can harbour drastically different TE repertoires, suggesting variation in the efficacy of genome defences. The evolution of fungal effectors, which are crucial determinants of pathogenicity, has been linked to the activity of TEs in pathogen genomes. Here we describe how TEs have shaped genome evolution of the fungal wheat pathogen Zymoseptoria tritici and four closely related species. We compared de novo TE annotations and Repeat-Induced Point mutation signatures in thirteen genomes from the Zymoseptoria species-complex. Then, we assessed the relative insertion ages of TEs using a comparative genomics approach. Finally, we explored the impact of TE insertions on genome architecture and plasticity. The thirteen genomes of Zymoseptoria species reflect different TE dynamics with a majority of recent insertions. TEs associate with distinct genome compartments in all Zymoseptoria species, including chromosomal rearrangements, genes showing presence/absence variation and effectors. European Z. tritici isolates have reduced signatures of Repeat-Induced Point mutations compared to Iranian isolates and closely related species. Our study supports the hypothesis that ongoing but moderate TE mobility in Zymoseptoria species shapes pathogen genome evolution.

genomics↗

Asian wild apples threatened by gene flow from domesticated apples and by their pestified pathogen

Massive gene flow between crops and their wild relatives may threaten the genetic integrity of wild species. Such threats are now well documented, but little is known about indirect consequences involving the spillover of crop pathogens to wild plants or introgression between crop and wild pathogens. To address these questions, we used population genetics approaches, demographic inference and pathogenicity tests on host-pathogen pairs composed of wild or domesticated apple trees of Central Asia and their fungal pathogen, Venturia inaequalis, itself showing differentiated agricultural-type and wild-type populations. We confirmed the occurrence of gene flow from cultivated to wild apple trees in Asian forests, threatening the Asian wild apple genetic integrity. SNP markers and demographic modeling revealed the occurrence of a secondary contact followed by hybridization between agricultural-type and wild-type fungal pathogen populations, and the dispersal of the agricultural-type pathogen in wild forests. We detected a SNP predicting the ability of the fungus to parasitize the different host populations, which induced an early stop codon in a gene coding for a small secreted protein in the agricultural-type fungal population, thus representing a putative avirulence gene which function loss would enable to parasitize cultivated apples. Pathogenicity tests in fact revealed the pestification of V. inaequalis, with higher virulence of the agricultural-type population on both wild and domesticated trees. Our findings highlight the threat posed by cultivating a crop near its center of origin, with the invasion of a pestified pathogen on wild plants and introgression in the wild-type pathogen.

evolutionary biology↗

Recent loss of the Dim2 cytosine DNA methyltransferase impacts mutation rate and evolution in a fungal plant pathogen

DNA methylation is found throughout all domains of life, yet the extent and function of DNA methylation differ between eukaryotes. Strains of the plant pathogenic fungus Zymoseptoria tritici appeared to lack cytosine DNA methylation (5mC) because gene amplification followed by Repeat-Induced Point mutation (RIP) resulted in the inactivation of the dim2 DNA methyltransferase gene. 5mC is, however, present in closely related sister species. We demonstrate that inactivation of dim2 occurred recently as some Z. tritici isolates carry a functional dim2 gene. Moreover, we show that dim2 inactivation occurred by a different path than previously hypothesized. We mapped the genome-wide distribution of 5mC in strains with and without functional dim2. Presence of functional dim2 correlates with high levels of 5mC in transposable elements (TEs), suggesting a role in genome defense. We identified low levels of 5mC in strains carrying inactive dim2 alleles, suggesting that 5mC is maintained over time, presumably by an active Dnmt5 DNA methyltransferase. Integration of a functional dim2 allele in strains with mutated dim2 restored normal 5mC levels, demonstrating de novo cytosine methylation activity of dim2. To assess the importance of 5mC for genome evolution, we performed an evolution experiment, comparing genomes of strains with high levels of 5mC to genomes of strains lacking dim2. We found that the presence of dim2 alters nucleotide composition by promoting C to T transitions (C[->]T) specifically at CpA (CA) sites during mitosis, likely contributing to TE inactivation. Our results show that 5mC density at TEs is a polymorphic trait in Z. tritici populations that can impact genome evolution. Author SummaryCytosine DNA methylation (5mC) is known to silence transposable elements in fungi and thereby appears to contribute to genome stability. The genomes of plant pathogenic fungi are highly diverse, differing substantially in transposon content and distribution. Here, we show extensive differences of 5mC levels within a single species of an important wheat pathogen. These differences were caused by inactivation of the DNA methyltransferase Dim2 in the majority of studied isolates. Presence of widespread 5mC increased point mutation rates in regions with active or mutated transposable elements during mitosis. The mutation pattern is dependent on the presence of Dim2 and resembles a mitotic version of Repeat-Induced Point mutation (RIP). Thus, loss of 5mC may represent an evolutionary trade-off offering adaptive potential at the cost of transposon control.

genetics↗

Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

BackgroundAntagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome architecture may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome and has emerged as a model organism to study the genomic evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and genomes of sister species infecting wild grasses to address the evolution of genome composition and structure. ResultsUsing long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts. ConclusionDespite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic signatures of genome architecture and compartmentalization across the genus Zymoseptoria. The compartmentalized genome may reflect purifying selection to retain a functional core genome and relaxed selection on the accessory genome allowing a higher extent of polymorphism.

genomics↗

Independent domestication events in the blue-cheese fungus Penicillium roqueforti

Domestication provides an excellent framework for studying adaptive divergence. Using population genomics and phenotypic assays, we reconstructed the domestication history of the blue cheese mold Penicillium roqueforti. We showed that this fungus was domesticated twice independently. The population used in Roquefort originated from an old domestication event associated with weak bottlenecks and exhibited traits beneficial for pre-industrial cheese production (slower growth in cheese and greater spore production on bread, the traditional multiplication medium). The other cheese population originated more recently from the selection of a single clonal lineage, was associated to all types of blue cheese worldwide but Roquefort, and displayed phenotypes more suited for industrial cheese production (high lipolytic activity, efficient cheese cavity colonization ability and salt tolerance). We detected genomic regions affected by recent positive selection and putative horizontal gene transfers. This study sheds light on the processes of rapid adaptation and raises questions about genetic resource conservation.

evolutionary biology↗