Comparative Transcriptome Analyses in Zymoseptoria tritici Reveal Significant Differences in Gene Expression Among Strains During Plant Infection

Zymoseptoria tritici is an ascomycete fungus that causes Septoria tritici blotch, a globally distributed foliar disease on wheat. Z. tritici populations are highly polymorphic and exhibit significant quantitative variation for virulence. Despite its importance, the genes responsible for quantitative virulence in this pathogen remain largely unknown. We investigated the expression profiles of four Z. tritici strains differing in virulence in an experiment conducted under uniform environmental conditions. Transcriptomes were compared at four different infection stages to characterize the regulation of gene families thought to be involved in virulence and to identify new virulence factors. The major components of the fungal infection transcriptome showed consistent expression profiles across strains. However, strain-specific regulation was observed for many genes, including some encoding putative virulence factors. We postulate that strain-specific regulation of virulence factors can determine the outcome of Z. tritici infections. We show that differences in gene expression may be major determinants of virulence variation among Z. tritici strains, adding to the already known contributions to virulence variation based on differences in gene sequence and gene presence/absence polymorphisms.

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Characterisation of an antimicrobial and phytotoxic ribonuclease secreted by the fungal wheat pathogen Zymoseptoria tritici

10.1101/130393 ◽

2017 ◽

Cited By ~ 1

Author(s):

Graeme J. Kettles ◽

Carlos Bayon ◽

Caroline A. Sparks ◽

Gail Canning ◽

Kostya Kanyuka ◽

...

Keyword(s):

Expression Pattern ◽

Effector Proteins ◽

Yeast Cells ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

List Type ◽

Expression Systems ◽

Zymoseptoria Tritici ◽

Loop Region

Abstract-The fungus Zymoseptoria tritici is the causal agent of Septoria Tritici Blotch (STB) disease of wheat leaves. Z. tritici secretes many functionally uncharacterised effector proteins during infection. Here we characterised a secreted ribonuclease (Zt6) with an unusual biphasic expression pattern.-Transient expression systems were used to characterise Zt6, and mutants thereof, in both host and non-host plants. Cell-free protein expression systems monitored impact of Zt6 protein on functional ribosomes, and in vitro assays of cells treated with recombinant Zt6 determined toxicity against bacteria, yeasts and filamentous fungi.-We demonstrated that Zt6 is a functional ribonuclease and that phytotoxicity is dependent on both the presence of a 22-amino acid N-terminal “loop” region and its catalytic activity. Zt6 selectively cleaves both plant and animal rRNA species, and is toxic to wheat, tobacco, bacterial and yeast cells but not to Z. tritici itself.-Zt6 is the first Z. tritici effector demonstrated to have a likely dual functionality. The expression pattern of Zt6 and potent toxicity towards microorganisms suggests that whilst it may contribute to the execution of wheat cell death, it is also likely to have an important secondary function in antimicrobial competition and niche protection.

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Prevalence of QoI resistance and mtDNA diversity in the Irish Zymoseptoria tritici population

Irish Journal of Agricultural and Food Research ◽

10.2478/ijafr-2019-0004 ◽

2019 ◽

Vol 58 (1) ◽

pp. 27-33

Author(s):

S. Kildea ◽

D.E. Bucar ◽

F. Hutton ◽

S. de la Rosa ◽

T.E. Welch ◽

...

Keyword(s):

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Entire Group ◽

Zymoseptoria Tritici ◽

Qoi Fungicides ◽

Quinone Outside Inhibitor ◽

Strain Collection ◽

Increased Sensitivity ◽

Mtdna Diversity

Abstract The emergence and spread of Quinone outside Inhibitor (QoI) fungicide resistance in the Irish Zymoseptoria tritici population in the early 2000s had immediate impacts on the efficacy of the entire group of fungicides for the control of septoria tritici blotch. As a result, a dramatic reduction in the quantities applied to winter wheat occurred in the following seasons. Even in the absence of these fungicides, the frequency of the resistance allele, G143A in the pathogens mtDNA has remained exceptionally high (>97%), and as such, it can be anticipated that continued poor efficacy of current QoI fungicides will be observed. Amongst the isolates with G143A, differences in sensitivity to the QoI pyraclostrobin were observed in vitro. The addition of the alternative oxidase (AOX) inhibitor salicylhydroxamic acid increased sensitivity in these isolates, suggesting some continued impairment of respiration by the QoI fungicides, albeit weak. Interestingly, amongst those tested, the strains from a site with a high frequency of inserts in the MFS1 transporter gene known to enhance QoI efflux did not exhibit this increase in sensitivity. A total of 19 mtDNA haplotypes were detected amongst the 2017 strain collection. Phylogenetic analysis confirmed the suggestion of a common ancestry of all the haplotypes, even though three of the haplotypes contained at least one sensitive strain.

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A Microbial Fermentation Mixture Reduces Fusarium Head Blight and Promotes Grain Weight but does not impact Septoria tritici blotch

European Journal of Plant Pathology ◽

10.1007/s10658-021-02396-4 ◽

2021 ◽

Author(s):

Tony Twamley ◽

Mark Gaffney ◽

Angela Feechan

Keyword(s):

Fusarium Head Blight ◽

Fungal Pathogens ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Microbial Fermentation ◽

In Planta ◽

Head Blight ◽

Zymoseptoria Tritici ◽

The Impact

AbstractFusarium graminearum and Zymoseptoria tritici cause economically important diseases of wheat. F. graminearum is one of the primary causal agents of Fusarium head blight (FHB) and Z. tritici is the causal agent of Septoria tritici blotch (STB). Alternative control methods are required in the face of fungicide resistance and EU legislation which seek to cut pesticide use by 2030. Both fungal pathogens have been described as either hemibiotrophs or necrotrophs. A microbial fermentation-based product (MFP) was previously demonstrated to control the biotrophic pathogen powdery mildew, on wheat. Here we investigated if MFP would be effective against the non-biotrophic fungal pathogens of wheat, F. graminearum and Z. tritici. We assessed the impact of MFP on fungal growth, disease control and also evaluated the individual constituent parts of MFP. Antifungal activity towards both pathogens was found in vitro but MFP only significantly decreased disease symptoms of FHB in planta. In addition, MFP was found to improve the grain number and weight, of uninfected and F. graminearum infected wheat heads.

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Differential dynamics of microbial community networks help identify microorganisms interacting with residue-borne pathogens: the case of Zymoseptoria tritici in wheat

10.1101/587667 ◽

2019 ◽

Author(s):

Lydie Kerdraon ◽

Matthieu Barret ◽

Valérie Laval ◽

Frédéric Suffert

Keyword(s):

Microbial Community ◽

Microbial Communities ◽

Fungal Pathogen ◽

Crop Residues ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Essential Information ◽

Linear Discriminant ◽

Network Analyses

AbstractBackgroundWheat 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 a 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.ResultsThe 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 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.ConclusionsThe 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.

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Advances in breeding techniques for durable Septoria tritici blotch (STB) resistance in cereals

10.19103/as.2021.0092.12 ◽

2021 ◽

pp. 303-356

Author(s):

Harsh Raman ◽

Keyword(s):

Quantitative Resistance ◽

Durable Resistance ◽

Genetic Resistance ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Winter Cereal ◽

Cereal Breeding ◽

Qualitative Resistance ◽

Breeding Techniques

Septoria tritici blotch (STB), caused by the hemibiotrophic fungus Zymoseptoria tritici, is one of the most important foliar diseases of winter cereal crops. Recent advances are helping to understand the genetic basis and architecture of resistance to STB. To date, at least 22 genes for qualitative resistance and over 200 quantitative trait loci (QTL) for quantitative resistance have been identified in cereals. This knowledge is enabling cereal breeding programs to develop varieties with more durable resistance to STB. This chapter reviews recent research on genetic resistance loci and breeding strategies based on both conventional and biotechnology-based breeding approaches (molecular marker/genomic-assisted breeding, genetic transformation, and gene-editing) to achieve achieving durable resistance to STB infection and minimise grain yield losses.

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Evidence of Selection for Fungicide Resistance in Zymoseptoria tritici Populations on Wheat in Western Oregon

Plant Disease ◽

10.1094/pdis-02-15-0214-re ◽

2016 ◽

Vol 100 (2) ◽

pp. 483-489 ◽

Cited By ~ 22

Author(s):

Laura E. Hayes ◽

Kathryn E. Sackett ◽

Nicole P. Anderson ◽

Michael D. Flowers ◽

Christopher C. Mundt

Keyword(s):

Fungicide Resistance ◽

Fungal Pathogen ◽

Plant Pathogens ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Resistance Evolution ◽

Regional Control ◽

Selection For ◽

Moderately Resistant

Plant pathogens pose a major challenge to maintaining food security in many parts of the world. Where major plant pathogens are fungal, fungicide resistance can often thwart regional control efforts. Zymoseptoria tritici, causal agent of Septoria tritici blotch, is a major fungal pathogen of wheat that has evolved resistance to chemical control products in four fungicide classes in Europe. Compared with Europe, however, fungicide use has been less and studies of fungicide resistance have been infrequent in North American Z. tritici populations. Here, we confirm first reports of Z. tritici fungicide resistance evolution in western Oregon through analysis of the effects of spray applications of propiconazole and an azoxystrobin + propiconazole mixture during a single growing season. Frequencies of strobilurin-resistant isolates, quantified as proportions of G143A mutants, were significantly higher in azoxystrobin-sprayed plots compared with plots with no azoxystrobin treatment at two different locations and were significantly higher in plots of a moderately resistant cultivar than in plots of a susceptible cultivar. Thus, it appears that western Oregon Z. tritici populations have the potential to evolve levels of strobilurin resistance similar to those observed in Europe. Although the concentration of propiconazole required to reduce pathogen growth by 50% values were numerically greater for isolates collected from plots receiving propiconazole than in control plots, this effect was not significant (P > 0.05).

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Expression profiles of cell-wall related genes vary broadly between two common maize inbreds during stem development

BMC Genomics ◽

10.1186/s12864-019-6117-z ◽

2019 ◽

Vol 20 (1) ◽

Cited By ~ 1

Author(s):

Bryan W. Penning ◽

Tânia M. Shiga ◽

John F. Klimek ◽

Philip J. SanMiguel ◽

Jacob Shreve ◽

...

Keyword(s):

Gene Expression ◽

Cell Wall ◽

Genetic Variation ◽

Secondary Wall ◽

Expression Profiles ◽

Gene Families ◽

Grass Species ◽

Specific Gene ◽

Maize Inbreds ◽

Stem Development

Abstract Background The cellular machinery for cell wall synthesis and metabolism is encoded by members of large multi-gene families. Maize is both a genetic model for grass species and a potential source of lignocellulosic biomass from crop residues. Genetic improvement of maize for its utility as a bioenergy feedstock depends on identification of the specific gene family members expressed during secondary wall development in stems. Results High-throughput sequencing of transcripts expressed in developing rind tissues of stem internodes provided a comprehensive inventory of cell wall-related genes in maize (Zea mays, cultivar B73). Of 1239 of these genes, 854 were expressed among the internodes at ≥95 reads per 20 M, and 693 of them at ≥500 reads per 20 M. Grasses have cell wall compositions distinct from non-commelinid species; only one-quarter of maize cell wall-related genes expressed in stems were putatively orthologous with those of the eudicot Arabidopsis. Using a slope-metric algorithm, five distinct patterns for sub-sets of co-expressed genes were defined across a time course of stem development. For the subset of genes associated with secondary wall formation, fifteen sequence motifs were found in promoter regions. The same members of gene families were often expressed in two maize inbreds, B73 and Mo17, but levels of gene expression between them varied, with 30% of all genes exhibiting at least a 5-fold difference at any stage. Although presence-absence and copy-number variation might account for much of these differences, fold-changes of expression of a CADa and a FLA11 gene were attributed to polymorphisms in promoter response elements. Conclusions Large genetic variation in maize as a species precludes the extrapolation of cell wall-related gene expression networks even from one common inbred line to another. Elucidation of genotype-specific expression patterns and their regulatory controls will be needed for association panels of inbreds and landraces to fully exploit genetic variation in maize and other bioenergy grass species.

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Presence of ice-nucleating Pseudomonas on wheat leaves promotes Septoria tritici blotch disease (Zymoseptoria tritici) via a mutually beneficial interaction

Scientific Reports ◽

10.1038/s41598-020-74615-7 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Helen N. Fones

Keyword(s):

Frost Damage ◽

Ice Nucleation ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Bacterial Populations ◽

Wheat Leaf ◽

Ina Bacteria ◽

Wheat Leaves ◽

Important Disease

Abstract Zymoseptoria tritici causes Septoria tritici blotch (STB) of wheat, an economically important disease causing yield losses of up to 10% despite the use of fungicides and resistant cultivars. Z. tritici infection is symptomless for around 10 days, during which time the fungus grows randomly across the leaf surface prior to entry through stomata. Wounded leaves show faster, more extensive STB, suggesting that wounds facilitate fungal entry. Wheat leaves also host epiphytic bacteria; these include ice-nucleating (INA+) bacteria, which induce frost damage at warmer temperatures than it otherwise occurs. Here, STB is shown to be more rapid and severe when wheat is exposed to both INA+ bacteria and sub-zero temperatures. This suggests that ice-nucleation-induced wounding of the wheat leaf provides additional openings for fungal entry. INA+ bacterial populations are shown to benefit from the presence of Z. tritici, indicating that this microbial interaction is mutualistic. Finally, control of INA+ bacteria is shown to reduce STB.

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Isolate specific responses of the non-host grass Brachypodium distachyon to the fungal pathogen Zymoseptoria tritici, compared to wheat.

Phytopathology ◽

10.1094/phyto-02-20-0041-r ◽

2020 ◽

Author(s):

Ailsing Reilly ◽

Sujit Jung Karki ◽

Anthony Twamley ◽

Anna M.M Tiley ◽

Steven Kildea ◽

...

Keyword(s):

Fungal Pathogen ◽

Plant Immunity ◽

Brachypodium Distachyon ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Pr Genes ◽

Zymoseptoria Tritici ◽

Expression Of Genes ◽

Pathogenesis Related ◽

Defence Gene Expression

Septoria tritici blotch (STB) is an important foliar disease of wheat that is caused by the fungal pathogen Zymoseptoria tritici. The grass Brachypodium distachyon has been used previously as a model system for cereal-pathogen interactions. In this study, we examined the non-host resistance (NHR) response of B. distachyon to two different Z. tritici isolates in comparison to wheat. These isolates vary in aggressiveness on wheat cv. Remus displaying significant differences in disease and pycnidia coverage. Using microscopy, we found that similar isolate specific responses were observed for H2O2 accumulation and cell death in both wheat and B. distachyon. Despite this, induction of isolate specific patterns of defence gene expression by Z. tritici did differ between B. distachyon and wheat. Our results suggest that phenylalanine ammonia lyase (PAL) expression may be important for NHR in B. distachyon while pathogenesis-related (PR) genes and expression of genes regulating reactive oxygen species (ROS) may be important to limit disease in wheat. Future studies of the B. distachyon-Z. tritici interaction may allow identification of conserved plant immunity targets which are responsible for the isolate specific responses observed in both plant species.

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Transcriptomic Analysis of Starch Biosynthesis in the Developing Grain of Hexaploid Wheat

International Journal of Plant Genomics ◽

10.1155/2009/407426 ◽

2009 ◽

Vol 2009 ◽

pp. 1-23 ◽

Cited By ~ 17

Author(s):

Boryana S. Stamova ◽

Debbie Laudencia-Chingcuanco ◽

Diane M. Beckles

Keyword(s):

Gene Expression ◽

Dna Microarrays ◽

Expression Profiles ◽

Expression Patterns ◽

Soluble Sugars ◽

Starch Synthesis ◽

Gene Families ◽

Starch Accumulation ◽

Protein Accumulation ◽

High Accumulation

The expression of genes involved in starch synthesis in wheat was analyzed together with the accumulation profiles of soluble sugars, starch, protein, and starch granule distribution in developing caryopses obtained from the same biological materials used for profiling of gene expression using DNA microarrays. Multiple expression patterns were detected for the different starch biosynthetic gene isoforms, suggesting their relative importance through caryopsis development. Members of the ADP-glucose pyrophosphorylase, starch synthase, starch branching enzyme, and sucrose synthase gene families showed different expression profiles; expression of some members of these gene families coincided with a period of high accumulation of starch while others did not. A biphasic pattern was observed in the rates of starch and protein accumulation which paralleled changes in global gene expression. Metabolic and regulatory genes that show a pattern of expression similar to starch accumulation and granule size distribution were identified, suggesting their coinvolvement in these biological processes.

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