Signaling Cross-Talk between Salicylic and Gentisic Acid in the ‘Candidatus Phytoplasma Solani’ Interaction with Sangiovese Vines

Abstract

“Bois noir” disease associated with ‘Candidatus Phytoplasma solani’ seriously compromises the production and survival of grapevines (Vitis vinifera L.) in Europe. Understanding the plant response to phytoplasmas should help to improve disease control strategies. Using a combined metabolomic and transcriptomic analysis, this work, therefore, investigated the phytoplasma–grapevine interaction in red cultivar Sangiovese in a vineyard over four seasonal growth stages (from late spring to late summer), comparing leaves from healthy and infected grapevines (symptomatic and symptomless). We found an accumulation of both conjugate and free salicylic acids (SAs) in the leaves of ‘Ca. P. solani’-positive plants from early stages of infection, when plants are still asymptomatic. A strong accumulation of gentisic acid (GA) associated with symptoms progression was found for the first time. A detailed analysis of phenylpropanoids revealed a significant accumulation of hydroxycinnamic acids, flavonols, flavan 3-ols, and anthocyanin cyanidin 3-O-glucoside, which are extensively studied due to their involvement in the plant response to various pathogens. Metabolomic data corroborated by gene expression analysis indicated that phenylpropanoid biosynthetic and salicylic acid-responsive genes were upregulated in ‘Ca. P. solani-positive plants compared to -negative ones during the observed period.

The Significance of Xylem Structure and Its Chemical Components in Certain Olive Tree Genotypes with Tolerance to Xylella fastidiosa Infection

“…Among the hydroxybenzoic acids, salicylic acid is well known to play an important role in plant stress response; in the PRPs, a significant increase in salicylic acid was reported compared with the symptomatic plants (Figure 8). Salicylic acid is crucial to induce the expression of pathogenesis-related genes [38] and the synthesis of compounds which are involved both in local and systemic acquired resistance in plants [39]. Moreover, a wide range of studies reported salicylic acid as a pivotal signaling molecule that plays a crucial role in plant tolerance and resistance both to biotic and abiotic stresses by activating mechanisms that act at different levels [40,41], some of which are the induction of activities and the expression of antioxidant enzymes such as superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD), thus enhancing a plant's ability to eliminate reactive oxygen species (also ROS produced as by-products by plant-pathogenic microbes) and reducing cellular oxidative damage [42][43][44].…”

“…Segments of one-year-old branches were ground in pre-cooled mortar to a fine powder using liquid nitrogen and processed according to Nutricati et al [38]. Approximately 0.5 g of pulverized tissue was homogenized in 3 mL of 100% methanol (1:6).…”

Advances in Roles of Salicylic Acid in Plant Tolerance Responses to Biotic and Abiotic Stresses

“…However, the exact mechanisms in this process are not yet fully understood [78]. In a word, recent studies made remarkable advances in SA's roles in plant tolerance responses to both biotic and abiotic stresses [47,48,71,72,82,84,[86][87][88][118][119][120][121][122][123], and in both physiological [124][125][126] and molecular perspectives [127][128][129][130]. For example, Yao et al proposed a high air humidity-triggered significant suppression of SA accumulation and signaling associated with compromised immunity of Arabidopsis plants [130], which indicates the value of research concerning SA's roles in multiple stresses confronted by plants.…”

“…From Table 1, it can be seen that these selected articles mainly deal with such biotic stress factors as bacteria, fungi, and insects. pathogens grapevines GA's role as a component of the grapevine SA-dependent response [123] pests grapevines Reduced injury by JA and SA application; reduction of number of eggs laid by D. suzukii females in JA-and SA-treated plants [125] Abbreviations: SA (salicylic acid), PR genes (pathogen-related genes), SAR (systemic acquired resistance), PCD (programmed cell death), SM (secondary metabolites), PK (protein kinase), MAPK (mitogen-activated protein kinase), CDPK (calcium-dependent protein kinase), SABC1 (salicylic acid biogenesis controller 1), JA (jasmonic acid), PR1 (pathogenesis-related genes 1), NPR1 (nonexpressor of pathogenesis-related genes 1), cAMP (cyclic adenosine monophosphate), NO (nitric oxide), cGMP (cyclic guanosine monophosphate), ASM (acibenzolar-Smethyl), HR (hypersensitive response), GA (gibberellins).…”

“…Overall, SA helps plants adapt to salt stress environments and mitigate the damage caused by salt stress [136][137][138][139]. Other mechanisms by which SA enhances plant salt tolerance are mainly as follows: activation of stress response pathways [96,[118][119][120][121][122], induction of heat shock protein synthesis [40], and regulation of the expression of stress response genes [103,123].…”