<i>Zymoseptoria tritici</i>suppresses the host immune response and facilitates the success of avirulent strains in mixed infections

Bernasconi, Alessio; Lorrain, Cécile; Flury, Peter; Alassimone, Julien; McDonald, Bruce A.; Sánchez‐Vallet, Andrea

doi:10.1101/2023.05.13.540507

Cited by 3 publications

(3 citation statements)

References 69 publications

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“…Although we did not test this specifically, we observed several instances of plants infected by Rhizoctonia solani in Rudolfingen in 2020 that might have compromised CLS resistance. Furthermore, experiments with mixed infections in Z. tritici showed that virulent strains were able to suppress the immune system of plants carrying the Stb6 R-gene, enabling avirulent strains to infect the resistant plants (Bernasconi et al, 2023). We hypothesize that similar mechanisms could be operating in the CLS pathosystem.…”

Section: Discussionmentioning

confidence: 86%

GWAS reveals a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogen

Chen,

Keunecke,

Bemm

et al. 2023

Molecular Plant Pathology

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The major resistance gene BvCR4 recently bred into sugar beet hybrids provides a high level of resistance to Cercospora leaf spot caused by the fungal pathogen Cercospora beticola. The occurrence of pathogen strains that overcome BvCR4 was studied using field trials in Switzerland conducted under natural disease pressure. Virulence of a subset of these strains was evaluated in a field trial conducted under elevated artificial disease pressure. We created a new C. beticola reference genome and mapped whole genome sequences of 256 isolates collected in Switzerland and Germany. These were combined with virulence phenotypes to conduct three separate genome‐wide association studies (GWAS) to identify candidate avirulence genes. We identified a locus associated with avirulence containing a putative avirulence effector gene named AvrCR4. All virulent isolates either lacked AvrCR4 or had nonsynonymous mutations within the gene. AvrCR4 was present in all 74 isolates from non‐BvCR4 hybrids, whereas 33 of 89 isolates from BvCR4 hybrids carried a deletion. We also mapped genomic data from 190 publicly available US isolates to our new reference genome. The AvrCR4 deletion was found in only one of 95 unique isolates from non‐BvCR4 hybrids in the United States. AvrCR4 presents a unique example of an avirulence effector in which virulent alleles have only recently emerged. Most likely these were selected out of standing genetic variation after deployment of BvCR4. Identification of AvrCR4 will enable real‐time screening of C. beticola populations for the emergence and spread of virulent isolates.

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Section: Discussionmentioning

confidence: 86%

GWAS reveals a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogen

Chen,

Keunecke,

Bemm

et al. 2023

Molecular Plant Pathology

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“…This greatly expands the number of effectors known to be functional during symptomless colonisation, beyond the previously described LysMdomain effector family 7,17 . It is known that Z. tritici suppresses the wheat immune response during infection, and, further, Z. tritici infection can lead to systemic induced susceptibility (SIS), enabling nonadapted pathogens or avirulent isolates of Z. tritici to co-infect 33,34 . It is likely that SIS is induced as a result of effector manipulation of the host; for example, by altering long-range hormonal signalling.…”

Section: Discussionmentioning

confidence: 99%

“…This all occurs before expression of the immune suppressing effectors identified in this study, are at their peak. It is relevant to note that infection of a virulent strain of Z. tritici can enable subsequent infection of an independently avirulent strain, by inducing SIS 33,34 . Therefore, it is quite possible that timing of immune suppressing effectors plays an important role in SIS development, and inhibition of resistance gene function.…”

Section: Discussionmentioning

confidence: 99%

An array ofZymoseptoria triticieffectors suppress plant immune responses

Thynne,

Ali,

Seong

et al. 2024

Preprint

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Zymoseptoria tritici is the most economically significant fungal pathogen of wheat in Europe. However, despite the importance of this pathogen, the molecular interactions between pathogen and host during infection are not well understood. Herein, we describe the use of two libraries of cloned Z. tritici effectors that were screened to identify effector candidates with putative pathogen associated molecular pattern (PAMP) triggered immunity (PTI)-suppressing activity. The effectors from each library were transiently expressed in Nicotiana benthamiana, and expressing leaves were treated with bacterial or fungal PAMPs to assess the effectors' ability to suppress reactive oxygen species (ROS) production. From these screens, numerous effectors were identified with PTI-suppressing activity. In addition, some effectors were able to suppress cell death responses induced by other Z. tritici secreted proteins. We used structural prediction tools to predict the putative structures of all of the Z. tritici effectors, and used these predictions to examine whether there was enrichment of specific structural signatures among the PTI-suppressing effectors. From among the libraries, multiple members of the killer protein-like 4 (KP4) and killer protein-like 6 (KP6) effector families were identified as PTI-suppressors. This observation is intriguing, as these protein families were previously associated with antimicrobial activity rather than virulence or host manipulation. This data provides mechanistic insight into immune suppression by Z. tritici during infection, and suggests that similar to biotrophic pathogens, this fungus relies on a battery of secreted effectors to suppress host immunity during early phases of colonisation.

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Genome-wide association studies reveal a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogenCercospora beticola

Chen

Keunecke

Bemm

et al. 2023

Preprint

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The major resistance gene BvCR4 recently bred into sugar beets provides a high level of resistance to Cercospora leaf spot caused by the fungal pathogen Cercospora beticola. The occurrence of pathogen strains virulent to BvCR4 was studied using field trials in Switzerland and Germany. Virulence of a subset of these strains was tested in a field trial conducted under elevated artificial disease pressure. We created a new C. beticola reference genome and mapped whole genome sequences of 256 field-collected isolates and combined this with the virulence phenotypes to conduct three separate GWAS to identify candidate avirulence genes. GWAS analyses identified a locus associated with avirulence containing a single candidate avirulence effector gene named AvrCR4. All virulent isolates either lacked AvrCR4 or had non-synonymous mutations within the gene. AvrCR4 was present in all 74 unique isolates obtained from non-BvCR4 hybrids, whereas 33 of 89 unique isolates obtained from BvCR4 hybrids carried this deletion. We also mapped genomic data from 190 publicly available isolates from the U.S to our new reference genome. The AvrCR4 deletion was found in only one of 95 unique isolates from non-BvCR4 hybrids in the U.S. AvrCR4 presents a unique example of an avirulence effector in which virulent alleles have only recently emerged. Most likely these were selected out of the standing genetic variation after deployment of a new major resistance gene. Identification of AvrCR4 will enable real-time screening of C. beticola populations for the emergence and spread of virulent isolates as well as long-term studies of effector evolution.

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Zymoseptoria triticisuppresses the host immune response and facilitates the success of avirulent strains in mixed infections

Cited by 3 publications

References 69 publications

GWAS reveals a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogen

GWAS reveals a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogen

An array ofZymoseptoria triticieffectors suppress plant immune responses

Genome-wide association studies reveal a rapidly evolving candidate avirulence effector in the Cercospora leaf spot pathogenCercospora beticola

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