Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance

Kema, G.H.J.; Gohari, Amir Mirzadi; Aouini, Lamia; Gibriel, Hesham; Ware, S.B.; Bosch, Frank van den; Manning-Smith, Robbie; Alonso-Chavez, Vasthi; Helps, Joseph; M’Barek, Sarrah Ben; Mehrabi, Rahim; Díaz-Trujillo, Caucasella; Zamani, Elham; Schouten, Henk J.; Lee, Theo A. J. van der; Waalwijk, C.; Waard, M.A. de; Wit, P.J.G.M. de; Verstappen, E.C.P.; Thomma, B.P.H.J.; Meijer, H.J.G.; Seidl, Michael

doi:10.1038/s41588-018-0052-9

Cited by 112 publications

(146 citation statements)

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“…Coupled with frequent sexual recombination in Z. tritici (Banke et al , ; Welch et al , ), this has catered for the rapid evolution of fungal virulence, resistance to the major classes of fungicides (Lucas, ; Hayes et al , ; Dooley et al , ) and rapid breakdown of host resistance (Cowger et al , ; Stukenbrock & McDonald, ; McDonald & Stukenbrock, ; Haueisen et al , ). Ongoing research aimed at controlling STB disease involves a multipronged approach for understanding host–pathogen gene interactions, resistance breeding and the development of new fungicide mixtures (Adhikari et al ., 2004a,b; Brown et al , ; Heick et al , ; Kema et al , ; Saintenac et al , ).…”

Section: Septoria Tritici Blotchmentioning

confidence: 99%

“…The Z. tritici avirulence factor AvrStb6 is a small cysteine-rich effector protein that interacts with STB6 (a wall-associated receptor kinase-like protein and the first major STB resistance gene to be cloned), which confers gene-for-gene resistance in wheat to Z. tritici (Zhong et al, 2017;Kema et al, 2018;Saintenac et al, 2018). A direct interaction between STB6 and AvrStb6 has not been demonstrated (Saintenac et al, 2018) and the function of the AvrStb6 effector in the absence of stb6 remains unknown (Brunner & McDonald, 2018).…”

Section: The Role Of Fungal Effectorsmentioning

confidence: 99%

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A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

et al. 2019

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Septoria tritici blotch (STB) disease of wheat is caused by the fungal pathogen Zymoseptoria tritici. It is the most important foliar disease of wheat in western Europe and affects wheat cultivation worldwide. The combination of intensive fungicide usage, a polycyclic asexual life cycle and an active sexual cycle has led to the emergence of fungal strains resistant/tolerant to all the major classes of fungicides used in its control. The hallmark of this disease is a long, symptomless latent phase that precedes the onset of visible symptoms. Understanding the processes that occur during the symptomless phase of infection is paramount in developing alternative strategies for disease control; however, large gaps in our knowledge of the disease remain. The known unknowns of the latent stage of infection can be summarized in three questions. Does the fungus initiate or manipulate host defences to trigger programmed cell death in order to facilitate nutrient acquisition or is the host acting exclusively? Does the fungus feed during both the latent phase and the necrotrophic phase like a true hemibiotroph? Does the long latent phase serve a beneficial function for the fungus or is it simply an artefact of evolution? This review aims to distil observations made during studies that have directly or indirectly contributed to answering these questions and points towards their most likely answers.

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Section: Septoria Tritici Blotchmentioning

confidence: 99%

Section: The Role Of Fungal Effectorsmentioning

confidence: 99%

A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

et al. 2019

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“…Two highly conserved lysin motif (LysM) effectors, Mg1LysM and Mg3LysM, prevent fungal recognition and shield the fungal cell wall from degradation by host hydrolytic enzymes (Marshall et al ., 2011). The other known effectors of Z. tritici , Zt80707, AvrStb6 and Zt_8_609, are rapidly evolving small secreted proteins (Poppe et al ., 2015; Hartmann et al ., 2017; Zhong et al ., 2017; Kema et al ., 2018). The latter two were identified because they are specifically recognised by certain wheat cultivars, and they were found to be located in transposable element‐rich genomic regions (Brading et al ., 2002; Hartmann et al ., 2017; Zhong et al ., 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The latter two were identified because they are specifically recognised by certain wheat cultivars, and they were found to be located in transposable element‐rich genomic regions (Brading et al ., 2002; Hartmann et al ., 2017; Zhong et al ., 2017). AvrStb6 is recognised by the resistance protein Stb6 in a gene‐for‐gene interaction that leads to a strong resistance response, completely blocking the progression of the infection (Kema et al ., 2000, 2018; Brading et al ., 2002; Saintenac et al ., 2018). In addition to Stb6 , 19 other race‐specific Stb resistance genes with large effects have been mapped, but their corresponding avirulence factors remain unknown (Brown et al ., 2015).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2018

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Summary Cultivar‐strain specificity in the wheat–Zymoseptoria tritici pathosystem determines the infection outcome and is controlled by resistance genes on the host side, many of which have been identified. On the pathogen side, however, the molecular determinants of specificity remain largely unknown.We used genetic mapping, targeted gene disruption and allele swapping to characterise the recognition of the new avirulence factor Avr3D1. We then combined population genetic and comparative genomic analyses to characterise the evolutionary trajectory of Avr3D1.Avr3D1 is specifically recognised by wheat cultivars harbouring the Stb7 resistance gene, triggering a strong defence response without preventing pathogen infection and reproduction. Avr3D1 resides in a cluster of putative effector genes located in a genome region populated by independent transposable element insertions. The gene was present in all 132 investigated strains and is highly polymorphic, with 30 different protein variants identified. We demonstrated that specific amino acid substitutions in Avr3D1 led to evasion of recognition.These results demonstrate that quantitative resistance and gene‐for‐gene interactions are not mutually exclusive. Localising avirulence genes in highly plastic genomic regions probably facilitates accelerated evolution that enables escape from recognition by resistance proteins.

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“…GWAS was also used in another pathogen of wheat, Zymoseptoria tritici . Sequencing of 103 isolates and subsequent identification of 584,171 single nucleotide polymorphisms (SNPs) enabled the successfully identification of AvrStb6 , the gene conferring avirulence on wheat lines carrying a functional Stb6 resistance gene [47, 48].…”

Section: Introductionmentioning

confidence: 99%

Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States

Richards

Stukenbrock

Carpenter

et al. 2019

Preprint

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22Filamentous fungi rapidly evolve in response to environmental selection pressures, exemplified 23 by their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal 24 agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing 25 the gain, loss, or functional diversification of putative effector genes. Whole genome 26 resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat 27 production regions of the United States enabled the examination of effector diversity and 28 genomic regions under selection specific to geographically discrete populations. A total of 29 1,026,859 quality SNPs/InDels were identified within the natural population. Implementation of 30 GWAS identified novel loci, as well as SnToxA and SnTox3 as major factors in disease. Genes 31 displaying presence/absence variation and predicted effector genes, as well as genes localized on 32 an accessory chromosome, had significantly higher pN/pS ratios, indicating a greater level of 33 diversifying selection. Population structure analyses indicated two major P. nodorum populations 34 corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States 35 (Population 2). Prevalence of SnToxA varied greatly between the two populations which 36 correlated with presence of the host sensitivity gene Tsn1. Additionally, 12 and 5 candidate 37 effector genes were observed to be diversifying among isolates from Population 1 and 38 Population 2, respectively, but under purifying or neutral selection in the opposite population. 39 Selective sweep analysis revealed 10 and 19 regions of positive selection from Population 1 and 40 Population 2, respectively, with 92 genes underlying population-specific selective sweeps. Also, 41 genes exhibiting presence/absence variation were significantly closer to transposable elements. 42 Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection 3 43 pressures unique to spring and winter wheat production regions by various routes of genomic 44 diversification, potentially facilitated through transposable element activity. 45Author Summary: 46 Parastagonospora nodorum is an economically important pathogen of wheat, employing 47 5 88 host resistance gene and a biotrophic effector follows the gene-for-gene model [17]. However, 89 necrotrophic pathogens use effectors to exploit the same host defense cellular machinery. 90Occurring in an inverse gene-for-gene manner, effectors are recognized by dominant host 91 susceptibility genes resulting in necrotrophic effector triggered susceptibility [18]. The lack of 92 homology or conserved domains between effector proteins hinders efforts towards novel effector 93 discovery. This lack of similarity can be attributed to the rapid evolution in response to local 94 selection pressure exerted by host resistance or susceptibility. However, this can be remedied via 95 thorough genomic and genetic analyses. 96Fungi have become a great res...

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Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance

Cited by 112 publications

References 61 publications

A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

A review of the known unknowns in the early stages of septoria tritici blotch disease of wheat

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

Local adaptation drives the diversification of effectors in the fungal wheat pathogen Parastagonospora nodorum in the United States

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