Xylella fastidiosa causes transcriptional shifts that precede tylose formation and starch depletion in xylem

Authors: INGEL, BRIAN - University Of California; REYES, CLARISSA - University Of California, Davis; MASSONNET, MELANIE - University Of California, Davis; BOUDREAU, BAILEY - University Wisconsin-Stevens Point-northern Aquaculture Demonstration Facility; SUN, YULING - University Wisconsin-Stevens Point-northern Aquaculture Demonstration Facility; SUN, QIANG - University Wisconsin-Stevens Point-northern Aquaculture Demonstration Facility; McElrone, Andrew; CANTU, DARIO - University Of California, Davis; ROPER, M. CAROLINE - University Of California

Submitted to: Molecular Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/17/2020
Publication Date: 11/20/2020
Citation: Ingel, B., Reyes, C.R., Massonnet, M., Boudreau, B., Sun, Y., Sun, Q., McElrone, A.J., Cantu, D., Roper, M. 2020. Xylella fastidiosa causes transcriptional shifts that precede tylose formation and starch depletion in xylem. Molecular Plant Pathology. 22(2):175-188. https://doi.org/10.1111/mpp.13016.
DOI: https://doi.org/10.1111/mpp.13016

Interpretive Summary:

Technical Abstract: Pierce’s disease (PD) in grapevine (Vitis vinifera) is caused by the bacterial pathogen, Xylella fastidiosa. X. fastidiosa is limited to the xylem tissue and following infection induces extensive plant-derived xylem blockages, primarily in the form of tyloses. Tylose-mediated vessel occlusions are a hallmark of PD, particularly in susceptible V. vinifera. Here, we temporally monitored tylose development over the course of the disease to link symptom severity to level of tylose occlusion and presence/absence of the bacterial pathogen at fine-scale resolution. The majority of vessels containing tyloses were devoid of bacterial cells, indicating that direct, localized perception of X. fastidiosa was not a primary cause of tylose formation. In addition, using X-ray computed microtomography aided by a machine learning technique, we determined that X. fastidiosa infection induces significant starch depletion in xylem ray parenchyma cells. These data, taken together, indicate that a signaling mechanism that emanates from the bacterium associated vessels that enables a systemic response to X. fastidiosa infection. To better understand the transcriptional changes underlying these phenotypes, we integrated global transcriptomics into the temporal phenotypes we tracked over the disease spectrum. We determined that genes related to tylose formation (ethylene signaling and cell wall biogenesis) and drought stress were up-regulated in both the early and late phases of disease, and those related to photosynthesis- and carbon-fixation were down-regulated during early and late disease. These responses correlated with the significant starch depletion observed in the ray cells indicating grapevines undergo significant carbon limitation as a result of prolonged X. fastidiosa infection.