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. We temporally monitored tylose development over the course of the disease to link symptom severity to the level of tylose occlusion and the 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, we used X‐ray computed microtomography and machine‐learning to determine that X. fastidiosa induces significant starch depletion in xylem ray parenchyma cells. This suggests that a signalling mechanism emanating from the vessels colonized by bacteria enables a systemic response to X. fastidiosa infection. To understand the transcriptional changes underlying these phenotypes, we integrated global transcriptomics into the phenotypes we tracked over the disease spectrum. Differential gene expression analysis revealed that considerable transcriptomic reprogramming occurred during early PD before symptom appearance. Specifically, we determined that many genes associated with tylose formation (ethylene signalling and cell wall biogenesis) and drought stress were up‐regulated during both Phase I and Phase II of PD. On the contrary, several genes related to photosynthesis and carbon fixation were down‐regulated during both phases. These responses correlate with significant starch depletion observed in ray cells and tylose synthesis in vessels.
Highlights
Xylella fastidiosa is a gram-negative proteobacterium that colonizes and is limited to the xylem of its plant hosts
The internal symptoms associated with Pierce's disease (PD) include occlusions within the xylem that are composed of plant-derived pectin gels, crystals, and tyloses, with the latter being the predominant form of vessel occlusion observed in PD-infected grapevines (Sun et al, 2013)
Because effective tylose production is a determinant in susceptibility or resistance to PD in grapevines, we sought to better understand the dynamics of tylose development across the PD disease spectrum in susceptible V. vinifera
Summary
Xylella fastidiosa is a gram-negative proteobacterium that colonizes and is limited to the xylem of its plant hosts. The functional category “Cell wall organization and biogenesis” was found enriched among the up-regulated genes at both Phase I and Phase II (Figure 7b and Data set S2) Induction of this biological process suggests the production and/or expansion of the plant cell wall in response to X. fastidiosa infection, possibly to replace the cell wall material damaged by the bacterial cell wall-degrading enzymes (Ingel et al, 2019; Roper et al, 2007) or to form tyloses (De Micco et al, 2016). Group V, corresponding to genes that were down-regulated during Phase I of the disease progression only, was enriched in functional categories related to photosynthetic metabolism, such as “Photosynthesis”, “Chlorophyll biosynthesis”, and “Thylakoid organization and biogenesis” (Figure 7c and Data set S2) This suggests that as a result of X. fastidiosa infection, the plant is slowing down photosynthesis during PD symptom onset. Aquaporins regulate cellular water homeostasis, and differential expression of genes encoding these proteins occurs during drought stress (Afzal et al, 2016)
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