Susceptibility to Xylella fastidiosa and functional xylem anatomy in Olea europaea: revisiting a tale of plant–pathogen interaction

Abstract

Background Xylella fastidiosa is a xylem-limited bacterium causing the Olive Quick Decline Syndrome, which is currently devastating the agricultural landscape of Southern Italy. The bacterium is injected into the xylem vessels of leaf petioles after the penetration of the insect vector’s stylet. From here, it is supposed to colonize the xylem vasculature moving against water flow inside conductive vessels. Widespread vessel clogging following the bacterial infection and causing the failure of water transport seemed not to fully supported by the recent empirical xylem anatomical observations in infected olive trees. Aim We tested the hypothesis that the higher susceptibility to the X. fastidiosa's infection in Cellina di Nardò compared to Leccino is associated to the higher vulnerability to air embolism of its larger vessels. Such hypothesis is motivated by the recognized ability of X. fastidiosa in degrading pit membranes and also because air embolism would possibly provide microenvironmental conditions more favourable to its more efficient aerobic metabolism. Methods We revised the relevant literature on bacterium growth and xylem physiology, and carried out empirical field, mid-summer measurements of xylem anatomy and native embolism in olive cultivars with high (Cellina di Nardò) and low susceptibility (Leccino) to the infection by X. fastidiosa. Key results Both cultivars had similar shoot mass traits and vessel length (~80 cm), but the highly susceptible one had larger vessels and a lower number of vessels supplying a given leaf mass. Native air embolism reduced mean xylem hydraulic conductance by ~58 % (Cellina di Nardò) and ~38 % (Leccino). Conclusions The higher air-embolism vulnerability of the larger vessels in Cellina di Nardò possibly facilitate the X. fastidiosa’s infection compared to Leccino. Some important characteristics of the vector – pathogen – plant interactions still require deep investigations acknowledging both the pathogen metabolic pathways and the biophysical principles of xylem hydraulics.

The impact of xylem geometry on olive cultivar resistance to Xylella fastidiosa: An image‐based study

“…Similarly, studies suggest xylem vessel diameters probably play a role in the resistance of olive cultivar Leccino (Petit et al, 2021;Sabella et al, 2019). In particular, smaller diameter vessels are reported in Leccino in comparison with plants of susceptible cultivar Cellina di Nardò (Petit et al, 2021;Sabella et al, 2019). Moreover, Sabella et al (2019) made some general hypotheses as to how narrow vessels could be acting as a resistance mechanism in Leccino.…”

Xylella fastidiosa subsp. paucaST53 exploits pit membranes of susceptible olive cultivars to spread systemically in the xylem

“…Previous reports have indicated that the bacteria can cause an increase in pit permeability (increased size and diameter) through the action of a battery of CWDEs that degrade the polysaccharide components of the middle lamella, thus enlarging the pore diameter and allowing systemic colonization (Fanton & Brodersen, 2021; Ingel et al, 2019). A side effect of this degradation is an increased risk of embolism, which leads to the disruption of water transport; such an effect is exacerbated in the susceptible olive cultivar Cellina di Nardò, which has a higher air‐embolism vulnerability than the resistant Leccino because of the larger lumen of its xylem vessels (Petit et al, 2021). While we did not prove the direct involvement of CWDEs in olive infections, our observations clearly indicate that XfDD enlarges PMs of susceptible cultivars to spread systemically.…”

Understanding the root xylem plasticity for designing resilient crops

“…In the case of X. fastidiosa, Gram-negative bacteria that specialize in the colonization of xylem vessels, the primary infection happens through insect vectors feeding on the plant. The plant responds by secreting gels and creating tyloses, limiting the spread of the bacteria (Petit et al, 2021).…”

“…In the case of X. fastidiosa , Gram‐negative bacteria that specialize in the colonization of xylem vessels, the primary infection happens through insect vectors feeding on the plant. The plant responds by secreting gels and creating tyloses, limiting the spread of the bacteria (Petit et al, 2021 ). In a recent study on olive trees, the authors compared the xylem anatomy in two cultivars with different susceptibility to Xylella f. Interestingly, they found that the highly susceptible cultivar had larger xylem vessels and higher air‐embolism vulnerability that possibly facilitate the infection (Petit et al, 2021 ).…”

“…The plant responds by secreting gels and creating tyloses, limiting the spread of the bacteria (Petit et al, 2021 ). In a recent study on olive trees, the authors compared the xylem anatomy in two cultivars with different susceptibility to Xylella f. Interestingly, they found that the highly susceptible cultivar had larger xylem vessels and higher air‐embolism vulnerability that possibly facilitate the infection (Petit et al, 2021 ).…”