Molecular Profiling of Pierce’s Disease Outlines the Response Circuitry of Vitis vinifera to Xylella fastidiosa Infection

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.

In-Field and Early Detection of Xylella fastidiosa Infections in Olive Using a Portable Instrument

“…The discovery of potential markers linked with early olive response to Xfd infection may be performed using RNA-seq approaches and Illumina technology (Hiseq 2000). Some transcriptomic studies at different symptomatic stages have been conducted in Vitis and Citrus crops infected by Xylella fastidiosa (Rodrigues et al, 2013; Zaini et al, 2018). Some genes are commonly expressed in Vitis and Citrus responses to Xylella fastidiosa (Table 1).…”

“…Our meta-analysis identified some good candidate genes: a leucine-rich repeat protein kinase family protein, MYB66 , chitinase A, a trypsin inhibitor family protein, expansin A4 and some auxin-responsive and gibberellin-regulated genes (Table 1). Xf-regulated genes commonly present in the two transcriptomic works conducted in Vitis and olive might be also of interest (Giampetruzzi et al, 2016; Zaini et al, 2018; Table 2). Some key cell wall modification genes that are potentially involved in pathogen signaling responses were observed: a pectin-lyase, a laccase and a poligalacturonase.…”

Pierce's Disease of Grapevines: A Review of Control Strategies and an Outline of an Epidemiological Model

“…This review concerns control strategies already tested but many more studies could serve as a source of inspiration for the development of efficient strategies against Xff . For example, a recent study by Zaini et al ( 2018 ) has specified various response mechanisms of vines to Xff infection that could be exploited, including accumulation of gamma-aminobutyric acid and upregulation of phytoalexins. As presented in this first section, various prophylactic and therapeutic strategies have already been proposed in order to minimize the effects of Xff in vineyards.…”

“…More specifically, XYLEFA exopolysaccharides seem to be responsible for the appearance of water stress symptoms along with plant-derived physiological responses, such as extensive tylose and gum production (Hopkins, 1989 ; Choi et al, 2013 ). Examples of plant defense response mechanisms include cell-wall remodeling and upregulation of plant hormone pathways and defense-related recognition receptors (Rodrigues et al, 2013 ; Giampetruzzi et al, 2016 ; Zaini et al, 2018 ), while the various virulence factors of XYLEFA have been extensively reviewed elsewhere (Rapicavoli et al, 2017 ).…”

Trans-Graft Protection Against Pierce’s Disease Mediated by Transgenic Grapevine Rootstocks

“…It doesn’t explain for example why biofilm-deficient Xf mutants display hypervirulence (Guilhabert and Kirkpatrick, 2005; Chatterjee et al, 2008b; Gouran et al, 2016). The xylem occlusion hypothesis also doesn’t explain the battery of enzymes and other compounds secreted by the pathogen that modify the xylem microenvironment and trigger chronic host stress responses (Roper et al, 2007; Pérez-Donoso et al, 2010; Pierce et al, 2014; Gouran et al, 2016; Merfa et al, 2016; Nascimento et al, 2016; Assis et al, 2017; Labroussaa et al, 2017; Zaini et al, 2018). These studies are broadening our understanding of virulence strategies employed by Xf and of how it thrives in the nutrient-poor xylem environment.…”