Toxicity of Potential Fungal Defense Proteins towards the Fungivorous Nematodes Aphelenchus avenae and Bursaphelenchus okinawaensis

Tayyrov, Annageldi; Schmieder, Stefanie S.; Bleuler-Martinez, Silvia; Plaza, David Fernando; Künzler, Markus

doi:10.1128/aem.02051-18

Cited by 27 publications

(26 citation statements)

References 58 publications

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“…When feeding on germlings or hyphal filaments, P. aurantium penetrated the fungal cell wall, invaded the hyphae, and fed exclusively on the cytoplasmic content, indicating that the fungal cell wall primarily represents a barrier of rather low nutritional value. Hyphal perforation and cytoplasmic feeding have also been described for fungivorous nematodes which pierce the fungal cell wall and induce specific fungal defense mechanisms made up of lectins and anti‐nutritional proteins (Bleuler‐Martinez et al, ; Tayyrov et al, ). Adapting the feeding mode between phagocytosis to ‘ruphocytic’ invasion is, to our knowledge, an unprecedented predatory strategy on fungi.…”

Section: Discussionmentioning

confidence: 82%

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Radosa

Ferling

Sprague

et al. 2019

Environmental Microbiology

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Summary Size and diverse morphologies pose a primary challenge for phagocytes such as innate immune cells and predatory amoebae when encountering fungal prey. Although filamentous fungi can escape phagocytic killing by pure physical constraints, unicellular spores and yeasts can mask molecular surface patterns or arrest phagocytic processing. Here, we show that the fungivorous amoeba Protostelium aurantium was able to adjust its killing and feeding mechanisms to these different cell shapes. Yeast‐like fungi from the major fungal groups of basidiomycetes and ascomycetes were readily internalized by phagocytosis, except for the human pathogen Candida albicans whose mannoprotein coat was essential to escape recognition by the amoeba. Dormant spores of the filamentous fungus Aspergillus fumigatus also remained unrecognized, but swelling and the onset of germination induced internalization and intracellular killing by the amoeba. Mature hyphae of A. fumigatus were mostly attacked from the hyphal tip and killed by an actin‐mediated invasion of fungal filaments. Our results demonstrate that predatory pressure imposed by amoebae in natural environments selects for distinct survival strategies in yeast and filamentous fungi but commonly targets the fungal cell wall as a crucial molecular pattern associated to prey and pathogens.

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Section: Discussionmentioning

confidence: 82%

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Radosa

Ferling

Sprague

et al. 2019

Environmental Microbiology

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“…In the fungal prey–nematode predator relationship, just like other types of prey–predator relationships, the fungal prey can develop resistance mechanisms against nematode predation. One type of fungal prey defense is the production and secretion of toxic secondary metabolites and toxic proteins [ 18 ]. For example, the model mushroom Coprinopsis cinerea produces a toxic substance on its mycelial surface that can kill nematodes upon contact [ 19 ].…”

Section: Antagonistic Interactionsmentioning

confidence: 99%

“…One type of fungal prey defense is the production and secretion of toxic secondary metabolites and toxic proteins [18]. For example, the model mushroom Coprinopsis cinerea produces a toxic substance on its mycelial surface that can kill nematodes upon contact [19].…”

Section: Nematodes Feeding On and Antagonizing Fungimentioning

confidence: 99%

Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

Zhang

et al. 2020

JoF

119

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Fungi and nematodes are among the most abundant organisms in soil habitats. They provide essential ecosystem services and play crucial roles for maintaining the stability of food-webs and for facilitating nutrient cycling. As two of the very abundant groups of organisms, fungi and nematodes interact with each other in multiple ways. Here in this review, we provide a broad framework of interactions between fungi and nematodes with an emphasis on those that impact crops and agriculture ecosystems. We describe the diversity and evolution of fungi that closely interact with nematodes, including food fungi for nematodes as well as fungi that feed on nematodes. Among the nematophagous fungi, those that produce specialized nematode-trapping devices are especially interesting, and a great deal is known about their diversity, evolution, and molecular mechanisms of interactions with nematodes. Some of the fungi and nematodes are significant pathogens and pests to crops. We summarize the ecological and molecular mechanisms identified so far that impact, either directly or indirectly, the interactions among phytopathogenic fungi, phytopathogenic nematodes, and crop plants. The potential applications of our understanding to controlling phytophagous nematodes and soilborne fungal pathogens in agricultural fields are discussed.

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“…CCL2 exerts its toxicity by binding to glycoproteins carrying an α1,3-fucosylated N-glycan core at the surface of the C. elegans intestinal epithelium (Schubert et al, 2012;Stutz et al, 2015). Cytoplasmic expression of CCL2 in the fungus, Ashbya gossypii, conferred resistance toward fungivorous nematodes (Tayyrov et al, 2018). Purified CCL2 inhibited larval development of the animal parasitic nematode Haemonchus contortus (Heim et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Expression of a Fungal Lectin in Arabidopsis Enhances Plant Growth and Resistance Toward Microbial Pathogens and a Plant-Parasitic Nematode

et al. 2021

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Coprinopsis cinerea lectin 2 (CCL2) is a fucoside-binding lectin from the basidiomycete C. cinerea that is toxic to the bacterivorous nematode Caenorhabditis elegans as well as animal-parasitic and fungivorous nematodes. We expressed CCL2 in Arabidopsis to assess its protective potential toward plant-parasitic nematodes. Our results demonstrate that expression of CCL2 enhances host resistance against the cyst nematode Heterodera schachtii. Surprisingly, CCL2-expressing plants were also more resistant to fungal pathogens including Botrytis cinerea, and the phytopathogenic bacterium Pseudomonas syringae. In addition, CCL2 expression positively affected plant growth indicating that CCL2 has the potential to improve two important agricultural parameters namely biomass production and general disease resistance. The mechanism of the CCL2-mediated enhancement of plant disease resistance depended on fucoside-binding by CCL2 as transgenic plants expressing a mutant version of CCL2 (Y92A), compromised in fucoside-binding, exhibited wild type (WT) disease susceptibility. The protective effect of CCL2 did not seem to be direct as the lectin showed no growth-inhibition toward B. cinerea in in vitro assays. We detected, however, a significantly enhanced transcriptional induction of plant defense genes in CCL2- but not CCL2-Y92A-expressing lines in response to infection with B. cinerea compared to WT plants. This study demonstrates a potential of fungal defense lectins in plant protection beyond their use as toxins.

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Toxicity of Potential Fungal Defense Proteins towards the Fungivorous Nematodes Aphelenchus avenae and Bursaphelenchus okinawaensis

Cited by 27 publications

References 58 publications

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

The different morphologies of yeast and filamentous fungi trigger distinct killing and feeding mechanisms in a fungivorous amoeba

Fungi–Nematode Interactions: Diversity, Ecology, and Biocontrol Prospects in Agriculture

Expression of a Fungal Lectin in Arabidopsis Enhances Plant Growth and Resistance Toward Microbial Pathogens and a Plant-Parasitic Nematode

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