White Rot Fungi (Hymenochaetales) and Esca of Grapevine: Insights from Recent Microbiome Studies

Abstract

Esca is a major grapevine trunk disease that heavily affects vineyards in the Northern hemisphere. The etiology and epidemiology of this disease have been subject of dispute ever since the earliest disease reports. The reason behind such debate is the presence of multiple internal and external symptoms, as well as several putative and confirmed wood pathogens. While the role of pathogenic fungi, as causal agents of wood symptoms, has been thoroughly assessed, their role in the expression of leaf symptoms remains to be fully elucidated. In this review, we analyzed etiological and epidemiological data, with a special focus on the microbiological aspect of esca and the involvement of Hymenochaetales (Basidiomycota). Vineyard studies have associated leaf symptoms with the presence of white rot, most frequently caused by Fomitiporia mediterranea (Hymenochaetales), while tracheomycotic fungi are commonly found, with similar abundance, in symptomatic and asymptomatic vines. Pathogenicity trials have excluded a direct effect of Hymenochaetales species in triggering leaf symptoms, while the data concerning the role of tracheomycotic fungi remains controversial. Recent microbiome studies confirmed that F. mediterranea is more abundant in leaf-symptomatic vines, and treatments that effectively control leaf symptoms, such as sodium arsenite spray and trunk surgery, act directly on the abundance of F. mediterranea or on the presence of white rot. This suggest that the simultaneous presence of Hymenochaetales and tracheomycotic fungi is a pre-requisite for leaf symptoms; however, the relation among fungal pathogens, grapevine and other biotic and abiotic factors needs further investigation.

Grapevine wood microbiome analysis identifies key fungal pathogens and potential interactions with the bacterial community implicated in grapevine trunk disease appearance

“…The key role of Fomitiporia , along with the two trachemycotic fungi ( P. chlamydospore and Phaeoacremonium sp.) and other confounding factors like climatic conditions and vineyard age, in leaf symptoms manifestation was recently highlighted in two comprehensive reviews by Morreti et al [ 60 ] and Del Frari et al [ 19 ].…”

“…Foliar symptoms often appear years after infestation [ 6 ] and show transitory patterns of appearance [ 14 ]. Fungal pathogens have not been recovered yet from symptomatic leaves suggesting that leaf symptoms are associated with the production and translocation to leaves of (1) secondary metabolites produced by the wood pathogens [ 15 – 18 ] (2) phytotoxic by-products of wood decay or phytotoxic metabolites produced by the plant–fungi interaction [ 19 ].…”

Minimal versus Intensive: How the Pruning Intensity Affects Occurrence of Grapevine Leaf Stripe Disease, Wood Integrity, and the Mycobiome in Grapevine Trunks

“…Besides vessel restructuring by the plant, pathogenic fungi can also interfere with the vessel integrity, e.g., by tissue degradation or by formation of occlusion [ 27 , 69 , 70 ]. Since wounds are the main gate for esca-associated pathogens to enter the vascular system, the risk of infection should decrease with reduced pruning measures on the trunk [ 1 , 71 , 72 ].…”

“…are frequently found in young, esca-affected vines [ 17 , 18 , 19 , 20 , 21 , 22 ]. In older vines, this set of fungi are also common; however, this is in combination with basidiomycetes, mainly from the genus Fomitiporia spp., which is the causal agent of white rot [ 23 , 24 , 25 , 26 , 27 ]. Besides the already-named fungal genera and species, the list of fungi associated with the esca complex has become even longer over recent decades and is still increasing [ 28 , 29 , 30 , 31 , 32 , 33 ].…”

Activity of Trichoderma asperellum Strain ICC 012 and Trichoderma gamsii Strain ICC 080 Toward Diseases of Esca Complex and Associated Pathogens

“…The leaf symptoms have been reproduced only on very few occasions by the inoculation of different pathogens (Sparapano et al, 2001;Reis et al, 2016;Markakis et al, 2017). GLSD appears not to be linked to specific fungal agents but as a reaction of the plant to the activity of fungal wood colonization affecting the plant physiology and the quality of production (Calzarano et al, 2004b(Calzarano et al, , 2017aLorrain et al, 2012;Pouzoulet et al, 2014;Fontaine et al, 2016;Mary et al, 2017;Bortolami et al, 2021;Del Frari et al, 2021).…”