Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/1/2008
Publication Date: 7/1/2008
Citation: Mcelrone, A.J., Jackson, S., Habdas, P. 2008. Hydraulic disruption and passive migration by a bacterial pathogen in oak tree xylem. Journal of Experimental Botany 59(10):2649-2657. Interpretive Summary: Xylella fastidiosa (Xf) is a plant pathogen that causes leaf scorch symptoms in numerous host plants in urban, agricultural, and natural ecosystems throughout the world. This pathogen inhabits the xylem (water conducting) tissue of host plants, but the exact mechanism of how it causes disease symptoms and moves within the xylem tissue of hosts is still unknown. To better understand these processes, we studied the function and structure of xylem in both healthy and Xf-infected trees of several oak species. The efficiency of water conduction in infected leaf petioles (leafstalks) of two oak species decreased significantly compared to healthy trees across the growing season in two consecutive years. Towards the end of each growing season, no water was able to move through infected petioles. Prior to disease leaf scorch symptoms, the amount of air within the xylem was greater in the infected petioles compared to healthy controls, likely resulted from damage caused by Xf while colonizing the new xylem of the petioles. We used four methods to determine if a pathway exists in woody stems that would allow Xf migration over long distances in host xylem without needed to degrade cell walls. All four methods consistently demonstrated that large pores (i.e. greater than the diameter of individual Xf) occur frequently throughout the stem xylem in several oak species. These large pores likely aid the bacteria in moving efficiently throughout the extensive xylem tissue of hosts and contribute to the high disease susceptibility exhibited among oak species.
Technical Abstract: Xylella fastidiosa (Xf) is a xylem-limited bacterial pathogen that causes leaf scorch symptoms in numerous host 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, therefore, to better understand both processes we studied functional and structural characteristics of xylem in different organs of both healthy and Xf-infected trees of several Quercus species. Hydraulic conductivity (Ks) in Xf-infected petioles of Q. palustris and Q. rubra decreased significantly compared to 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 to healthy controls and preceded significant reductions in Ks. Embolism likely resulted from pit membrane degradation during colonization of new petiole xylem and triggers the process that eventually leads 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 tissues that allows for passive Xf migration: 1) calculations based on vulnerability to cavitation data, 2) scanning electron micrographs, 3) microsphere injections, and 4) 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 likely facilitate systemic colonization of the secondary xylem network and contribute to the high susceptibility to bacterial leaf scorch exhibited among these species.