Ecophysiological impacts of Esca, a devastating grapevine trunk disease, on Vitis vinifera L.

Abstract

Esca is a Grapevine Trunk Disease (GTD) caused by a broad range of taxonomically unrelated fungal pathogens. These attack grapevine wood tissues inducing necroses even in the conductive vascular tissues, thus affecting the vine physiology and potentially leading to plant death. However, the influence of Esca on leaf and whole-plant water transport disruption remains poorly understood. In this paper, a detailed analysis of xylem-related physiological parameters in grapevines that expressed Esca-foliar symptoms was carried out. The experiments were conducted in a vineyard in the Bordeaux region (France) on cv. Cabernet-Sauvignon (Vitis vinifera L.) grapevines, which were monitored for Esca-foliar symptoms over a two-year period. Heat dissipation sap-flow sensors were installed during the summer on grapevines having expressed or not Esca-foliar symptoms. Leaf water potential, stomatal conductance and leaf transpiration were also measured. Physiological monitoring showed that sap flow density and whole-plant transpiration of Esca-infected grapevines decreased significantly a week before the first foliar symptoms appeared. When atmospheric water demand (Vapour Pressure Deficit, VPD) was the highest, both parameters tended to be about twice as low in symptomatic grapevines as in asymptomatic ones. Sap flow density data at the maximum transpiration-time, was systematically 29–30% lower in Esca-infected grapevines compared to control plants before or after the appearance of Esca-foliar symptoms. This trend was observed whatever the temperatures and VPD values measured. In Esca-diseased plants, larger amounts of necrotic wood, mainly white rot, were found in the trunk and cordon of symptomatic grapevines compared to healthy ones, suggesting necroses have an influence in reducing the whole-plant hydraulic capacity. This study reveals that the use of physiological monitoring methods, together with the visual monitoring of foliar symptoms, could prove useful in providing accurate measurements of Esca disease severity.

Major changes in grapevine wood microbiota are associated with the onset of esca, a devastating trunk disease

“…Esca is associated with extensive necrosis of grapevine trunk and cordon woody tissues, as well as its typical foliar symptoms (reviews: Bertsch et al ., 2013; Mondello et al ., 2018). This slow evolving disease can lead to plant death (apoplexy) depending on plant physiology, climatic factors and cultural practices (Lecomte et al ., 2012; Ouadi et al ., 2019). This disease is associated with the colonization of wood tissues by unrelated plant pathogenic fungi such as P. chlamydospora , P. minimum , N. parvum and D. seriata , mainly isolated from black necrotic sectors or punctuations, whereas F. mediterranea is mostly isolated from white‐rot necrotic tissues (Bertsch et al ., 2013; Mondello et al ., 2018).…”

A Lipidomic Analysis of Leaves of Esca-Affected Grapevine Suggests a Role for Galactolipids in the Defense Response and Appearance of Foliar Symptoms

“…It is known that besides pathogens, multiple factors, such as climatic/edaphic conditions and cultural practices, contribute to ESCA development [ 3 , 26 , 32 , 38 , 39 ]. Physiologically, the apparition of foliar visual symptoms has been attributed to two main events: (i) The production of tyloses and gels by the vine, which together with the fungi occlude the vessels (hydraulic failure hypothesis), and/or (ii) the production of plant-derived signals and pathogen molecules in the transpiration stream, which is translocated through the phloem and accumulated in the canopy (elicitor-toxin hypothesis), both leading to leaf desiccation [ 2 , 3 , 37 ].…”

“…Three major characteristics of ESCA are the undetermined period of latency within the vine (asymptomatic status) [ 3 , 38 ], the irregular annual recurrence of foliar symptoms in the vineyard [ 29 , 40 ], and the high variability of symptoms in both their discoloration and shape [ 26 , 36 ]. Considering these peculiarities of ESCA, affected vines were identified during a continuous survey period of 6 years, by assessing internal and external symptoms yearly after grape cluster harvesting.…”

“…Esca complex disease (ESCA) is another GTD that attacks the perennial organs of grapevines, leading to tiger-stripe symptoms on leaves, apoplexy of shoots [ 2 , 3 ], and extensive wood necrosis (white rot, brown streaking, and other types of dark necrotic spots) on the trunk and cordons [ 26 ] colonized by fungi, such as Phaeomoniella chlamydospora [ 5 , 27 , 28 , 29 ], Phaeoacremonium minimum [ 5 , 30 ], Fomitiporia mediterranea [ 31 , 32 ], Botryosphaeriaceae species, and other fungal taxa [ 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 ]. Protection against GTDs relies mainly on prophylactic measures, remedial surgery [ 26 , 39 ], and the application of biological agents [ 8 , 31 ] or mixtures of fertilizers [ 40 , 41 ] to reduce symptom incidence and severity; these control strategies often offer only partial protection.…”

“…While no grapevine cultivar is known to be completely resistant to ESCA, degrees of susceptibility ranging from highly susceptible to tolerant have been reported [ 44 ]; however, the plant defense mechanisms underlying these observations have not been completely elucidated. Studies that have focused on identifying the host response to ESCA have found that the wood/foliar symptomatology described above is linked to characteristic adaptive physiological [ 38 ] and metabolic changes [ 36 ]. A prominent change observed during metabolomic profiling experiments is the presence of large amounts of stilbene phytoalexins in symptomatic tissues of ESCA-affected vines [ 33 , 34 , 45 ].…”