A wheat cysteine-rich receptor-like kinase confers broad-spectrum resistance against Septoria tritici blotch

AbstractThe poverty of disease resistance gene reservoirs limits the breeding of crops for durable resistance against evolutionary dynamic pathogens. Zymoseptoria tritici which causes Septoria tritici blotch (STB), represents one of the most genetically diverse and devastating wheat pathogens worldwide. No fully virulent Z. tritici isolates against synthetic wheats carrying the major resistant gene Stb16q have been identified. Here, we use comparative genomics, mutagenesis and complementation to identify Stb16q, which confers broad-spectrum resistance against Z. tritici. The Stb16q gene encodes a plasma membrane cysteine-rich receptor-like kinase that was recently introduced into cultivated wheat and which considerably slows penetration and intercellular growth of the pathogen.

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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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Mapping for adult-plant resistance against Septoria tritici blotch in a common wheat line Murga

Phytopathology ◽

10.1094/phyto-05-20-0172-r ◽

2020 ◽

Author(s):

Xinyao He ◽

Gustavo Azzimonti ◽

Mariel del Rosario Sánchez-Vidaña ◽

Silvia Pereyra ◽

Carolina Sansaloni ◽

...

Keyword(s):

Broad Spectrum ◽

Resistance Mechanism ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Adult Plant ◽

Wheat Line ◽

Synthetic Wheat ◽

Broad Spectrum Resistance ◽

Fast Development ◽

The One

Septoria tritici blotch (STB) is a major foliar disease globally, which is notorious in the fast development of fungicide resistance, making host resistance an indispensable component in mitigating STB. CIMMYT wheat line Murga is well known for its high, durable, and broad-spectrum resistance against STB infection, and the purpose of this study was to investigate its resistance mechanism to facilitate its utilization in breeding. A recombinant inbred line population was derived from a cross between Murga and a STB susceptible line Huirivis#1, comprising 297 progenies. The population was evaluated for adult-plant STB resistance in Toluca, Mexico (from 2017 to 2019), and in La Estanzuela, Uruguay (from 2016 to 2018). Genotyping was performed with the DArTSeq platform. QTL mapping indicated a major and stable QTL on chromosome 3DL, explaining a phenotypic variation for STB of 41.2-62.5% in Mexico and 27.5-40.3% in Uruguay. This QTL was regarded as Stb16 based on comparison of its physical position, the possible origin from synthetic wheat, and its broad-spectrum resistance. Additional QTL with minor effects were identified on chromosomes 2B, 2D, 3A, 3B, and 5B. The one on 5BS was significant in four out of the six environments and must be new. Murga was the resistant donor for all QTL, except for those on 2B and 3A. Being an elite breeding line, the Stb16 carrier Murga could be used as a promising STB resistance donor. The rational employment of Stb16 could contribute to STB management yet avoid the rapid emergence of Stb16-virulent isolates.

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Remarkable recent changes in genetic diversity of the avirulence gene AvrStb6 in global populations of the wheat pathogen Zymoseptoria tritici

10.1101/2020.09.18.303370 ◽

2020 ◽

Author(s):

Christopher Stephens ◽

Fatih Ölmez ◽

Hannah Blyth ◽

Megan McDonald ◽

Anuradha Bansal ◽

...

Keyword(s):

Genetic Diversity ◽

Gene Interaction ◽

Protein Isoforms ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Avirulence Gene ◽

Zymoseptoria Tritici ◽

Reference Isolate ◽

Receptor Like Kinase ◽

Global Population

SUMMARYSeptoria tritici blotch (STB), caused by the fungus Zymoseptoria tritici, is one of the most economically important diseases of wheat. Recently, both factors of a gene-for-gene interaction between Z. tritici and wheat, the wheat receptor-like kinase Stb6 and the Z. tritici secreted effector protein AvrStb6, have been identified. Previous analyses revealed a high diversity of AvrStb6 alleles present in historic Z. tritici isolate collections, with up to ~ 18% of analysed isolates possessing the avirulence isoform of AvrStb6 identical to that originally identified in the reference isolate IPO323. With Stb6 present in many commercial wheat cultivars globally, we aimed to assess potential changes in AvrStb6 genetic diversity and the incidence of alleles allowing evasion of Stb6-mediated resistance in more recent Z. tritici populations. Here we show, using targeted re-sequencing of AvrStb6, that this gene is universally present in field isolates sampled from major wheat-growing regions of the world between 2013–2017. However, in contrast to the data from studies of historic isolates, our study revealed a complete absence of the originally described avirulence isoform of AvrStb6 amongst modern Z. tritici isolates. Moreover, a remarkably small number of alleles, each encoding AvrStb6 protein isoforms conditioning virulence on Stb6-containing wheat, were found to predominate among modern Z. tritici isolates. A single virulence isoform of AvrStb6 was found to be particularly abundant throughout the global population. These findings indicate that, despite the ability of Z. tritici to sexually reproduce on resistant hosts, AvrStb6 avirulence alleles tend to be eliminated in subsequent populations.

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Resistance and virulence variability in wheat–Zymoseptoria tritici interactions

Crop and Pasture Science ◽

10.1071/cp20126 ◽

2020 ◽

Vol 71 (7) ◽

pp. 645

Author(s):

Mojgan Mahboubi ◽

Reza Talebi ◽

Mostafa Aghaee Sarbarzeh ◽

Amir Mohammad Naji ◽

Rahim Mehrabi

Keyword(s):

Resistance Gene ◽

Effective Resistance ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Zymoseptoria Tritici ◽

Resistance Response ◽

Breeding Programs ◽

Wheat Genotypes ◽

Broad Spectrum Resistance ◽

Important Disease

Septoria tritici blotch (STB), caused by Zymoseptoria tritici, is an important disease of wheat worldwide. This study was performed to investigate the efficacy of Stb genes against 10 isolates of Z. tritici and to elucidate the resistance response pattern of 185 wheat genotypes to STB. The 10 isolates showed different virulence patterns on the Stb differentials. Effectiveness determination showed that most Stb genes (particularly Stb1–Stb9) were ineffective against the 10 isolates, whereas Kavkaz-K4500 (possessing Stb10, Stb12), Arina and Riband (possessing Stb15), and M3 (possessing Stb16 and Stb17) were resistant to all isolates tested. Of the 185 wheat genotypes, 72% were susceptible to all isolates, indicating that these genotypes lacked any effective resistance genes at the seedling stage against the isolates used. The remaining 51 genotypes showed specific resistance to one or more isolates, suggesting that they contain at least one effective resistance gene. Six genotypes were resistant to all isolates, indicating that they may possess broad-spectrum resistance gene(s) or a combination of diverse uncharacterised Stb genes that could be effectively used in breeding programs.

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New broad-spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat

Theoretical and Applied Genetics ◽

10.1007/s00122-011-1692-7 ◽

2011 ◽

Vol 124 (1) ◽

pp. 125-142 ◽

Cited By ~ 62

Author(s):

S. Mahmod Tabib Ghaffary ◽

Justin D. Faris ◽

Timothy L. Friesen ◽

Richard G. F. Visser ◽

Theo A. J. van der Lee ◽

...

Keyword(s):

Broad Spectrum ◽

Hexaploid Wheat ◽

Septoria Tritici Blotch ◽

Septoria Tritici ◽

Synthetic Hexaploid Wheat ◽

Broad Spectrum Resistance ◽

Synthetic Hexaploid

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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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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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