Exploring the Hydraulic Failure Hypothesis of Esca Leaf Symptom Formation

Abstract

Vascular pathogens cause disease in a large spectrum of perennial plants, with leaf scorch being one of the most conspicuous symptoms. Esca in grapevine (Vitis vinifera) is a vascular disease with huge negative effects on grape yield and the wine industry. One prominent hypothesis suggests that vascular disease leaf scorch is caused by fungal pathogen-derived elicitors and toxins. Another hypothesis suggests that leaf scorch is caused by hydraulic failure due to air embolism, the pathogen itself, and/or plant-derived tyloses and gels. In this study, we transplanted mature, naturally infected esca symptomatic vines from the field into pots, allowing us to explore xylem integrity in leaves (i.e. leaf midveins and petioles) using synchrotron-based in vivo x-ray microcomputed tomography and light microscopy. Our results demonstrated that symptomatic leaves are not associated with air embolism. In contrast, symptomatic leaves presented significantly more nonfunctional vessels resulting from the presence of nongaseous embolisms (i.e. tyloses and gels) than control leaves, but there was no significant correlation with disease severity. Using quantitative PCR, we determined that two vascular pathogen species associated with esca necrosis in the trunk were not found in leaves where occlusions were observed. Together, these results demonstrate that symptom development is associated with the disruption of vessel integrity and suggest that symptoms are elicited at a distance from the trunk where fungal infections occur. These findings open new perspectives on esca symptom expression where the hydraulic failure and elicitor/toxin hypotheses are not necessarily mutually exclusive.

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

“…GLSD, characterized by tiger stripe-like symptoms on the leaves, is the most common expression of the disease [ 3 , 44 ]. ESCA-associated fungi are undetected in the distal organs of the vines (i.e., annual stems and leaves), demonstrating that vascular occlusions and symptoms occur at a distance from the pathogen niche localized in the wood [ 2 ]. Exhaustive research has shown that losses in grape yield and quality caused by ESCA are correlated with leaf symptom severity [ 34 , 40 ].…”

“…The plant cell represents a complex of molecules combined with numerous additional components. Plant growth and development depends on the interaction between these components and environmental stimuli, such as pathogen attacks [ 1 , 2 , 3 , 4 ]. Plant response to pathogens is complex and composed of at least two layers: A basal, broad-band immunity called pathogen-associated molecular pattern-triggered immunity and a strain-specific level of immunity known as effector-triggered immunity.…”

“…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.…”

Seasonal and long-term consequences of esca on grapevine stem xylem integrity

“…Plants were then classified by their long-term symptomatology record: plants asymptomatic from 2012 to 2018 (pA, previously asymptomatic), and plants that have expressed symptoms at least once between 2012 and 2018 (pS, previously symptomatic). The uprooting method and greenhouse growth conditions are detailed in Bortolami et al (2019).…”

“…While the pathogens responsible for esca-induced trunk necrosis have been identified (Morales-Cruz et al, 2018;Brown et al, 2020), the underlying mechanisms of leaf and fruit symptoms, and plant death are still poorly understood. Bortolami et al (2019) demonstrated that the two vascular pathogens related to esca (Phaeomoniella chlamydospora and Phaeoacremonium minimum) were never detected in leaves or in one-year old stems, but always in the trunk (independently from leaf symptom presence). They further showed that esca symptomatic leaves presented significant losses in hydraulic conductivity due to the occlusion of the xylem conduits by tyloses.…”