Abstract
Pierce’s disease is a major threat to grapevines caused by the bacterium Xylella fastidiosa. Although devoid of a type 3 secretion system commonly employed by bacterial pathogens to deliver effectors inside host cells, this pathogen is able to influence host parenchymal cells from the xylem lumen by secreting a battery of hydrolytic enzymes. Defining the cellular and biochemical changes induced during disease can foster the development of novel therapeutic strategies aimed at reducing the pathogen fitness and increasing plant health. To this end, we investigated the transcriptional, proteomic, and metabolomic responses of diseased Vitis vinifera compared to healthy plants. We found that several antioxidant strategies were induced, including the accumulation of gamma-aminobutyric acid (GABA) and polyamine metabolism, as well as iron and copper chelation, but these were insufficient to protect the plant from chronic oxidative stress and disease symptom development. Notable upregulation of phytoalexins, pathogenesis-related proteins, and various aromatic acid metabolites was part of the host responses observed. Moreover, upregulation of various cell wall modification enzymes followed the proliferation of the pathogen within xylem vessels, consistent with the intensive thickening of vessels’ secondary walls observed by magnetic resonance imaging. By interpreting the molecular profile changes taking place in symptomatic tissues, we report a set of molecular markers that can be further explored to aid in disease detection, breeding for resistance, and developing therapeutics.
Highlights
Plants have evolved complex responses to adapt to both biotic and abiotic environmental stresses, with an increase in the production of reactive oxygen species (ROS) as a key mechanism common to several types of stress conditions (Mittler, 2017)
A T2SS that has been shown to secrete a number of hydrolytic enzymes that correlate to the observed disease symptoms
Our data further depict a wealth of molecular details of its complex interaction with grapevines leading to Pierce’s disease (PD) that suggest: (1) activation of a complex defense response that includes both pathogen- and damage-associated molecular pattern (PAMP/DAMP)-triggered immunity (PTI), but impairment of downstream salicylic acid-mediated immune response; (2) chronic oxidative stress despite activation of antioxidant metabolism; and (3) intensive cell wall remodeling and lignification, which can lead to reduced sap flow and increased water and nutrient deficiency
Summary
Plants have evolved complex responses to adapt to both biotic and abiotic environmental stresses, with an increase in the production of reactive oxygen species (ROS) as a key mechanism common to several types of stress conditions (Mittler, 2017). Detection and spread of different strains in the European continent in recent years have raised great concern, given its potential to colonize plant hosts already attacked in the American continent such as grapevines and oranges among others It poses the threat of causing new diseases like olive quick decline syndrome, which is annihilating olive groves in southern Italy and progressively spreading in the Mediterranean area (Martelli et al, 2016). Our data highlighted major metabolites accumulated in PD and revealed novel members of the pathogen-sensing and stress response network This enabled us to select which genes within paralog groups play a more pronounced role in the defense response to PD and can be further explored as early disease markers or therapeutic targets in case of disease susceptibility genes. Since current mitigation strategies to control PD rely on intensive insecticide applications to prevent vectors from disseminating X. fastidiosa across grapevines, understanding disease susceptibility and the host molecular responses to infection can lead to improved resistance breeding and novel control approaches
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