Wood degradation by Fomitiporia mediterranea M. Fischer: Physiologic, metabolomic and proteomic approaches

Abstract

Fomitiporia mediterranea (Fmed) is one of the main fungal species found in grapevine wood rot, also called “amadou,” one of the most typical symptoms of grapevine trunk disease Esca. This fungus is functionally classified as a white-rot, able to degrade all wood structure polymers, i.e., hemicelluloses, cellulose, and the most recalcitrant component, lignin. Specific enzymes are secreted by the fungus to degrade those components, namely carbohydrate active enzymes for hemicelluloses and cellulose, which can be highly specific for given polysaccharide, and peroxidases, which enable white-rot to degrade lignin, with specificities relating to lignin composition as well. Furthermore, besides polymers, a highly diverse set of metabolites often associated with antifungal activities is found in wood, this set differing among the various wood species. Wood decayers possess the ability to detoxify these specific extractives and this ability could reflect the adaptation of these fungi to their specific environment. The aim of this study is to better understand the molecular mechanisms used by Fmed to degrade wood structure, and in particular its potential adaptation to grapevine wood. To do so, Fmed was cultivated on sawdust from different origins: grapevine, beech, and spruce. Carbon mineralization rate, mass loss, wood structure polymers contents, targeted metabolites (extractives) and secreted proteins were measured. We used the well-known white-rot model Trametes versicolor for comparison. Whereas no significant degradation was observed with spruce, a higher mass loss was measured on Fmed grapevine culture compared to beech culture. Moreover, on both substrates, a simultaneous degradation pattern was demonstrated, and proteomic analysis identified a relative overproduction of oxidoreductases involved in lignin and extractive degradation on grapevine cultures, and only few differences in carbohydrate active enzymes. These results could explain at least partially the adaptation of Fmed to grapevine wood structural composition compared to other wood species, and suggest that other biotic and abiotic factors should be considered to fully understand the potential adaptation of Fmed to its ecological niche. Proteomics data are available via ProteomeXchange with identifier PXD036889.

First Description of Non-Enzymatic Radical-Generating Mechanisms Adopted by Fomitiporia mediterranea: An Unexplored Pathway of the White Rot Agent of the Esca Complex of Diseases

“…Even if described as a simultaneous white rot relying on in vitro wood mineralization assays, at the nanoscale, the wood cell wall decay pattern observed for Fmed does not resemble a typical enzymatic white rot decay pattern [20,51,58].…”

“…CAZymes, laccases, class II-PODs (manganese peroxidases [MnPs] and generic peroxidases [GPs]), and other AAs have been reported in genomic, proteomic, and enzymological studies of Fmed, while genes encoding for versatile peroxidases (VPs) and lignin peroxidases (LiP) have been demonstrated to be absent in the Fmed genome [20,33,[49][50][51]; ii.…”

An Engineered Laccase from Fomitiporia mediterranea Accelerates Lignocellulose Degradation

“…The versatility of laccases makes them valuable tools in both natural ecosystems and industrial applications. Fomitiporia mediterranea is a polypore fungal species that grows on olive trees [ 4 ] and has been associated with esca in grapevines and their roots [ 5 , 6 ]. Functionally, F. mediterranea is a white rot-causing basidiomycete that secretes both cellulolytic enzymes that catalyze depolymerization of cellulose and hemicellulose and ligninolytic enzymes, including laccases and peroxidases, which catalyze depolymerization of lignin.…”

Development of a molecular diagnostic to discriminate between Fomitiporia species and advancements in detection of the main grapevine decline‐related pathogens in propagating material and mature vines

“…The ascomycetes associated with Petri disease have been hypothesized to detoxify antimicrobial substances produced by the plant xylem parenchyma cells upon pathogen invasion (Mugnai et al, 1999). However, according to resent studies, F. mediterranea is also capable of degrading wood polymers such as celluloses, hemicelluloses, phenolics and lignin, which suggests that it could act as a primary pathogen (Schilling et al, 2022).…”

“…However, according to resent studies, F . mediterranea is also capable of degrading wood polymers such as celluloses, hemicelluloses, phenolics and lignin, which suggests that it could act as a primary pathogen (Schilling et al., 2022).…”