Multiple scenarios for sexual crosses in the fungal pathogen Zymoseptoria tritici on wheat residues: Potential consequences for virulence gene transmission

Orellana-Torrejon, Carolina; Vidal, Tiphaine; Gazeau, Gwilherm; Boixel, Anne‐Lise; Gélisse, Sandrine; Lageyre, Jérôme; Saint‐Jean, Sébastien; Suffert, Frédéric

doi:10.1016/j.fgb.2022.103744

Cited by 8 publications

(11 citation statements)

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“…Although these isolates have not been sequenced, the range of different resistance responses they triggered in some wheat genotypes suggests a high level of genetic diversity. This is supported by the well-established genetic diversity of Z. tritici even in limited geographic regions ( Berraies et al., 2013 ; Mekonnen et al., 2020 ; Orellana-Torrejon et al., 2022b ) and indicates that the results identified here should be broadly applicable to UK Z. tritici populations.…”

Section: Discussionsupporting

confidence: 82%

A large bioassay identifies Stb resistance genes that provide broad resistance against Septoria tritici blotch disease in the UK

et al. 2023

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IntroductionSeptoria tritici blotch (STB) is one of the most damaging fungal diseases of wheat in Europe, largely due to the paucity of effective resistance genes against it in breeding materials. Currently dominant protection methods against this disease, e.g. fungicides and the disease resistance genes already deployed, are losing their effectiveness. Therefore, it is vital that other available disease resistance sources are identified, understood and deployed in a manner that maximises their effectiveness and durability.MethodsIn this study, we assessed wheat genotypes containing nineteen known major STB resistance genes (Stb1 through to Stb19) or combinations thereof against a broad panel of 93 UK Zymoseptoria tritici isolates. Seedlings were inoculated using a cotton swab and monitored for four weeks. Four infection-related phenotypic traits were visually assessed. These were the days post infection to the development of first symptoms and pycnidia, percentage coverage of the infected leaf area with chlorosis/necrosis and percentage coverage of the infected leaf area with pycnidia.ResultsThe different Stb genes were found to vary greatly in the levels of protection they provided, with pycnidia coverage at four weeks differing significantly from susceptible controls for every tested genotype. Stb10, Stb11, Stb12, Stb16q, Stb17, and Stb19 were identified as contributing broad spectrum disease resistance, and synthetic hexaploid wheat lines were identified as particularly promising sources of broadly effective STB resistances.DiscussionNo single Z. tritici isolate was found to be virulent against all tested resistance genes. Wheat genotypes carrying multiple Stb genes were found to provide higher levels of resistance than expected given their historical levels of use. Furthermore, it was noted that disease resistance controlled by different Stb genes was associated with different levels of chlorosis, with high levels of early chlorosis in some genotypes correlated with high resistance to fungal pycnidia development, potentially suggesting the presence of multiple resistance mechanisms.The knowledge obtained here will aid UK breeders in prioritising Stb genes for future breeding programmes, in which optimal combinations of resistance genes could be pyramided. In addition, this study identified the most interesting Stb genes for cloning and detailed functional analysis.

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Section: Discussionsupporting

confidence: 82%

A large bioassay identifies Stb resistance genes that provide broad resistance against Septoria tritici blotch disease in the UK

et al. 2023

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“…tritici have been shown to proliferate epiphytically on resistant plants and induce early defense responses [ 53 ]. The proliferation of AvrStb6-expressing strains on the leaf surface together with the frequently occurring genetically diverse STB infections, might facilitate on the one hand sexual reproduction, as previously shown [ 41 , 46 ] and on the other hand penetration through the stomata and pycnidia formation, as shown in this work. Additionally, we showed that 1E4 pycnidia in detached leaves are formed but in contrast to what we found in intact plants, the presence of 3D7 hindered asexual reproduction of 1E4.…”

Section: Discussionsupporting

confidence: 74%

“…The epiphytic growth of Z . tritici has been shown to be critical for its life cycle [ 46 , 51 , 52 ]. In fact, avirulent isolates of Z .…”

Section: Discussionmentioning

confidence: 99%

“…Overall, these results highlight that even when avirulent strains are detected and their infection is prevented, they can still survive on the leaf surface and their co-existence with virulent strains or leaf damage can facilitate the persistence of avirulent strains in Z . tritici populations [ 46 , 53 ]. Although the avirulent strain formed many fewer pycnidia than the virulent strain, this ability of avirulent strains to reproduce in mixed infections will facilitate the survival of avirulent strains and enable the persistence of avirulent alleles in fields planted to resistant hosts.…”

Section: Discussionmentioning

confidence: 99%

“…tritici carry a diverse array of AvrStb6 isoforms, with virulent and avirulent strains typically coexisting in the same field [ 45 ]. Remarkably, it has been demonstrated that avirulent strains are capable of reproducing sexually with co-infecting virulent strains despite not being able to infect a resistant host [ 41 , 46 ]. It has yet to be determined if and how mixed infections affect asexual reproduction.…”

Section: Introductionmentioning

confidence: 99%

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Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections

Bernasconi,

Lorrain,

Flury

et al. 2023

PLoS Pathog

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Plants interact with a plethora of pathogenic microorganisms in nature. Pathogen-plant interaction experiments focus mainly on single-strain infections, typically ignoring the complexity of multi-strain infections even though mixed infections are common and critical for the infection outcome. The wheat pathogen Zymoseptoria tritici forms highly diverse fungal populations in which several pathogen strains often colonize the same leaf. Despite the importance of mixed infections, the mechanisms governing interactions between a mixture of pathogen strains within a plant host remain largely unexplored. Here we demonstrate that avirulent pathogen strains benefit from being in mixed infections with virulent strains. We show that virulent strains suppress the wheat immune response, allowing avirulent strains to colonize the apoplast and to reproduce. Our experiments indicate that virulent strains in mixed infections can suppress the plant immune system, probably facilitating the persistence of avirulent pathogen strains in fields planted with resistant host plants.

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The collembolan Heteromurus nitidus grazes the wheat fungal pathogen Zymoseptoria tritici on infected tissues: opportunities and limitations for bioregulation

Bourgeois,

Prado,

Suffert

et al. 2024

Pest Management Science

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BACKGROUNDSeptoria tritici blotch (STB), caused by the fungus Zymoseptoria tritici, is a foliar disease affecting wheat crops against which conventional control methods are not totally effective. During inter‐epidemic periods the fungus survives in wheat residues left on the ground. In this study, we tested the potential of the collembolan Heteromurus nitidus – a springtail species present in field soils and known to interact with different fungal species – as a potential bioregulation agent of Z. tritici on wheat residues through a choice and consumption experiment.RESULTSSpringtails preferred inoculated fresh residues but did not have a preference between inoculated and uninoculated old residues. Springtails grazed on Z. tritici fruiting bodies and reduced pycnidiospore numbers by ten‐fold compared to control inoculated fresh residues. Attraction toward fresh inoculated residues and pycnidiospore reduction support the hypothesis that Z. tritici is a food source for springtails. H. nitidus showed no preference between inoculated and uninoculated 18‐month‐old residues, probably because they no longer produced ascospores.CONCLUSIONAttraction towards fresh residues and spore reduction support our hypothesis that H. nitidus may contribute to the bioregulation of Z. tritici. Perspectives for field application would be determined by the ability of H. nitidus and Z. tritici to interact at key epidemiological stages. The impact of H. nitidus on the quantity of pathogen primary inoculum over time should be estimated using residues of intermediate age. This would help to identify the optimal period for enhancing the effectiveness of springtails as consumers of Z. tritici.This article is protected by copyright. All rights reserved.

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Multiple scenarios for sexual crosses in the fungal pathogen Zymoseptoria tritici on wheat residues: Potential consequences for virulence gene transmission

Cited by 8 publications

References 71 publications

A large bioassay identifies Stb resistance genes that provide broad resistance against Septoria tritici blotch disease in the UK

A large bioassay identifies Stb resistance genes that provide broad resistance against Septoria tritici blotch disease in the UK

Virulent strains of Zymoseptoria tritici suppress the host immune response and facilitate the success of avirulent strains in mixed infections

The collembolan Heteromurus nitidus grazes the wheat fungal pathogen Zymoseptoria tritici on infected tissues: opportunities and limitations for bioregulation

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