Biochemical characterization of wood decay and metabolization of phenolic compounds by causal fungi of grapevine trunk diseases

Grapevine trunk diseases, such as Esca, Botryosphaeria dieback, and Eutypa dieback, are caused by various Ascomycota and Basidiomycota fungi that colonize wood and form internal lesions. Basidiomycota fungi, such as Fomitiporia species, are associated only with the trunk disease Esca, and are wood-decay fungi. Variation in the extent of lesion development among the fungal pathogens reflects a combination of fungal virulence and host susceptibility. To evaluate factors that may affect lesion development, we compared in vitro wood-decay abilities and tolerance of host secondary metabolites (cell-wall and soluble phenolic compounds) of four fungi that cause trunk diseases: Eutypa lata (Eutypa dieback), Fomitiporia polymorpha (Esca), and Diplodia seriata and Neofusicoccum parvum (Botryosphaeria dieback). Fungi were grown on autoclaved blocks of Vitis vinifera 'Merlot' wood for six months, to examine fungal colonization of wood cells and percentages of wood components remaining after decay. Fungi were also grown on medium amended with starch, pectin, lignin, cellulose, hemicellulose, tannic acid, gallic acid, magnesium sulfate, or grape wood powder, to determine cell wall-degrading enzyme activity and impacts on fungal growth. Lastly, to determine tolerance of phenolic compounds, fungi were grown in medium amended with piceid, rutin, epicatechin, or gallic acid. Our novel findings for F. polymorpha include its preferential degradation of hemicellulose and pectin (and detection of corresponding enzymatic activities), but no degradation of lignin, in spite of growth in lignin-amended media and detection of laccase, lignin peroxidase, and peroxidase activities. Together, these findings suggest F. polymorpha has characteristics of both brown-rot and white-rot fungi. The type of wood decay caused by D. seriata and N. parvum, based on their degradation of pectin, cellulose, hemicellulose, and lignin (and detection of corresponding enzymatic activities), is characteristic of a soft rot, similar to that of E. lata. Unique among these three Ascomycetes was induction of N. parvum growth by piceid, rutin, epicatechin, and gallic acid, and efficient metabolism and/or detoxification of these phenolic compounds by N. parvum. As all four fungi metabolize components of the wood as substrate, and also can metabolize/detoxify host-defense compounds, a clearer understanding of their roles as wood-decay fungi might further research on managing the chronic wood infections.

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PLoS ONE
Published
2025-04-16
DOI
https://doi.org/10.1371/journal.pone.0315412
Citations
1
Primary Topic
Plant Pathogens and Fungal Diseases
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article
Field-Weighted Citation Impact
1.15

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article

Biochemical characterization of wood decay and metabolization of phenolic compounds by causal fungi of grapevine trunk diseases

Christopher M. Wallis, Erin Galarneau, Kendra Baumgartner
1 citations
PLoS ONE
Plant Pathogens and Fungal Diseases
1.15
article

Biochemical characterization of wood decay and metabolization of phenolic compounds by causal fungi of grapevine trunk diseases

Christopher M. Wallis, Erin Galarneau, Kendra Baumgartner
article en
1 citations

Abstract

Grapevine trunk diseases, such as Esca, Botryosphaeria dieback, and Eutypa dieback, are caused by various Ascomycota and Basidiomycota fungi that colonize wood and form internal lesions. Basidiomycota fungi, such as Fomitiporia species, are associated only with the trunk disease Esca, and are wood-decay fungi. Variation in the extent of lesion development among the fungal pathogens reflects a combination of fungal virulence and host susceptibility. To evaluate factors that may affect lesion development, we compared in vitro wood-decay abilities and tolerance of host secondary metabolites (cell-wall and soluble phenolic compounds) of four fungi that cause trunk diseases: Eutypa lata (Eutypa dieback), Fomitiporia polymorpha (Esca), and Diplodia seriata and Neofusicoccum parvum (Botryosphaeria dieback). Fungi were grown on autoclaved blocks of Vitis vinifera 'Merlot' wood for six months, to examine fungal colonization of wood cells and percentages of wood components remaining after decay. Fungi were also grown on medium amended with starch, pectin, lignin, cellulose, hemicellulose, tannic acid, gallic acid, magnesium sulfate, or grape wood powder, to determine cell wall-degrading enzyme activity and impacts on fungal growth. Lastly, to determine tolerance of phenolic compounds, fungi were grown in medium amended with piceid, rutin, epicatechin, or gallic acid. Our novel findings for F. polymorpha include its preferential degradation of hemicellulose and pectin (and detection of corresponding enzymatic activities), but no degradation of lignin, in spite of growth in lignin-amended media and detection of laccase, lignin peroxidase, and peroxidase activities. Together, these findings suggest F. polymorpha has characteristics of both brown-rot and white-rot fungi. The type of wood decay caused by D. seriata and N. parvum, based on their degradation of pectin, cellulose, hemicellulose, and lignin (and detection of corresponding enzymatic activities), is characteristic of a soft rot, similar to that of E. lata. Unique among these three Ascomycetes was induction of N. parvum growth by piceid, rutin, epicatechin, and gallic acid, and efficient metabolism and/or detoxification of these phenolic compounds by N. parvum. As all four fungi metabolize components of the wood as substrate, and also can metabolize/detoxify host-defense compounds, a clearer understanding of their roles as wood-decay fungi might further research on managing the chronic wood infections.

PLoS ONEVol. 20(4)
United States Department of Agriculture (US)
National Institute of Food and Agriculture
Life in Land
Openalex Percentile: Top 26%
Plant Pathogens and Fungal Diseases
1.15
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