Hydraulic disruption and passive migration by a bacterial pathogen in oak tree xylem

Xylella fastidiosa (Xf) is a xylem-limited bacterial pathogen that causes leaf scorch symptoms in numerous plant species in urban, agricultural, and natural ecosystems worldwide. The exact mechanism of hydraulic disruption and systemic colonization of xylem by Xf remains elusive across all host plants. To understand both processes better, the functional and structural characteristics of xylem in different organs of both healthy and Xf-infected trees of several Quercus species were studied. Hydraulic conductivity (K(s)) in Xf-infected petioles of Q. palustris and Q. rubra decreased significantly compared with healthy trees as the season progressed and plummeted to zero with the onset of scorch symptoms. Prior to the onset of symptoms, embolism was as much as 3.7 times higher in Xf-infected petioles compared with healthy controls and preceded significant reductions in K(s). Embolism likely resulted from pit membrane degradation during colonization of new petiole xylem and triggered the process that eventually led to vessel occlusion. Pit membrane porosity was studied using the following four methods to determine if a pathway exists in the xylem network of woody stems that allows for passive Xf migration: (i) calculations based on vulnerability to cavitation data, (ii) scanning electron micrographs, (iii) microsphere injections, and (iv) air seeding thresholds on individual vessels. All four methods consistently demonstrated that large pit membrane pores (i.e. greater than the diameter of individual Xf) occur frequently throughout the secondary stem xylem in several Quercus species. These large pores probably facilitate systemic colonization of the secondary xylem network and contribute to the high susceptibility to bacterial leaf scorch exhibited among these species.