The investigation of the ecological role of Peniophora lycii in grapevine disease development

Abstract

Peniophora lycii (Höhnel and Litschauer 1907) is a white-rot, wood-decaying basidiomycete in the family Peniophoraceae (order Russales). It is commonly found on dead branches and stems of woody plants. As a saprotroph, P. lycii plays an important role in forest ecosystems by decomposing lignocellulosic substrates, especially cellulose, and contributing to nutrient cycling (Shabaev et al. 2022). White-rot fungi can degrade lignin through direct or indirect enzymatic mechanisms. In grapevine, the leaf mycobiome is dominated by ascomycetes, while basidiomycetes are less abundant (Pinto et al. 2014). In grapevine wood, however, higher basidiomycete abundance has been linked to the development of trunk diseases (GTDs; Paolinelli et al. 2020).

The present study explored the ecological behavior of a Peniophora lycii isolate associated with grapevine, focusing on its interactions with other vine-associated fungi and its colonization potential under conditions relevant to vineyard ecosystems. In inoculation trials, P. lycii did not infect intact detached leaves, but colonized and necrotized the edges of leaf discs, and induced black necrosis and white rot symptoms in grapevine cuttings. In dual culture assays, interactions between P. lycii and the epiphytic fungus Aureobasidium pullulans were influenced by the growth medium, indicating that environmental conditions shape fungal interactions on grapevine surfaces. P. lycii overgrew epiphytic Botrytis cinerea and Alternaria sp., as well as the endophytic fungus Botryosphaeria dothidea. P. lycii showed tropism towards Phaeomoniella chlamydospora without clear overgrowth or antagonism. Microscopy confirmed mycoparasitic interactions of P. lycii with B. cinerea, Alternaria sp. and B. dothidea, while interactions with A. pullulans were characterized by mutual inhibition. No direct hyphal interactions were detected with P. chlamydospora. In planta assays on leaf discs confirmed that these fungal interactions were maintained under plant conditions, although co-inoculation with epiphytic fungi did not affect necrosis development. Co-infection experiments on grapevine cuttings showed that interactions between P. lycii and either B. dothidea or P. chlamydospora did not influence wood symptom development. Beyond reporting the first isolation of P. lycii from grapevine, this work highlights the role of fungal interactions within grapevine-associated microbial communities. The results suggest that P. lycii may function as an opportunistic secondary colonizer in grapevine trunk disease complexes, underlining the importance of biotic components of the vineyard environment as part of terroir expression.

References

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Shabaev AV, Moiseenko KV, Glazunova OA, Savinova OS, Fedorova TV (2022) Comparative Analysis of Peniophora lycii and Trametes hirsuta exoproteomes demonstrates “Shades of Gray” in the concept of white-rotting fungi. Int J Mol Sci 7: 10322. https://doi.org/10.3390/ijms231810322.

Pinto C, Pinho D, Sousa S, Pinheiro M, Egas C, Gomes A (2014) Unravelling the diversity of grapevine microbiome. PloS ONE, 9: e85622. https://doi.org/10.1371/journal.pone.0085622

Paolinelli M, Escoriaza G, Cesari C, Garcia-Lampasona S, Hernandez-Martinez R (2020) Metatranscriptomic approach for microbiome characterization and host gene expression evaluation for “Hoja de malvón” disease in Vitis vinifera cv. Malbec. Res Square https://doi.org/10.21203/rs.3.rs-23526/v1.