Secondary and primary metabolites reveal putative resistance-associated biomarkers against Erysiphe necator in resistant grapevine genotypes

Abstract

Numerous fungicide applications are required to control Erysiphe necator, the causative agent of powdery mildew. This increased demand for cultivars with strong and long-lasting field resistance to diseases and pests. In comparison to the susceptible cultivar ‘Teroldego’, the current study provides information on some promising disease-resistant varieties (mono-locus) carrying one E. necator-resistant locus: BC4 and ‘Kishmish vatkana’, as well as resistant genotypes carrying several E. necator resistant loci (pyramided): ‘Bianca’, F26P92, F13P71, and NY42. A clear picture of the metabolites’ alterations in response to the pathogen is shown by profiling the main and secondary metabolism: primary compounds and lipids; volatile organic compounds and phenolic compounds at 0, 12, and 48 hours after pathogen inoculation. We identified several compounds whose metabolic modulation indicated that resistant plants initiate defense upon pathogen inoculation, which, while similar to the susceptible genotype in some cases, did not imply that the plants were not resistant, but rather that their resistance was modulated at different percentages of metabolite accumulation and with different effect sizes. As a result, we discovered ten up-accumulated metabolites that distinguished resistant from susceptible varieties in response to powdery mildew inoculation, three of which have already been proposed as resistance biomarkers due to their role in activating the plant defense response.

Pre‐infection efficacy of resistance inducers against grapevine powdery mildew

“…Primed plants are assumed to display an immune response similar to varieties exhibiting genetic resistance (Qiu et al, 2015;Schnee et al, 2008). Host resistance restricts E. necator invasion through the inhibition of conidial germination, appressorium development, haustorium formation and development of secondary hyphae, thus preventing infection (Gadoury et al, 2012), or through programmed cell death at the site of infection and phytoalexin accumulation in the surrounding cells (Schnee et al, 2008), thus stopping infection in the early stages (Ciubotaru et al, 2023;Qiu et al, 2015). Genetic resistance also inhibits the proliferation of hyphae on the plant surface and reduces fungal sporulation (Ciubotaru et al, 2023;Fedorina et al, 2022;Sosa-Zuniga et al, 2022).…”

“…Dishes were randomly placed in a settling tower and then artificially inoculated by wiping conidia from naturally infected leaves with fresh, visible and abundant sporulation (Sosa-Zuniga et al, 2022); these leaves were collected from different vineyards and untreated plots located in northern Italy between 2020 and 2022, to inoculate a fungal population. This dry inoculation provides effective infections, as conidia may be inhibited when using a wet inoculation (Ciubotaru et al, 2023). The number of conidia deposited per cm 2 leaf area was assessed by placing two Burker chambers without the coverslip alongside the Petri dishes on the settling tower and counting the number of E. necator conidia; the density of inoculated spores was 75 to 90 conidia/cm 2 , depending on the inoculation experiment.…”

Semi-Targeted Profiling of the Lipidome Changes Induced by Erysiphe Necator in Disease-Resistant and Vitis vinifera L. Varieties

“…The inoculation with E. necator was achieved according to the modified methods of [ 53 , 54 ], described in [ 23 ]. Briefly, naturally infected powdery mildew leaves from the same untreated vineyard of the grape variety “Pinot Noir” were collected.…”

“…We previously provided metabolomics evidence on the early interaction between grapevine varieties with one locus and grapevine varieties with several loci and E. necator [ 23 ]. We discovered that the class of molecules most affected by the pathogen was lipids, highlighting the importance of lipids in grapevine defense against the powdery mildew causative agent.…”

Microbial degradation of plant toxins

“…In grapevine, resistance to the powdery mildew pathogen Erysiphe nectator was associated with both plant primary and secondary metabolites (Ciubotaru et al, 2023). Metabolic profiles of susceptible and resistant plants pointed towards the involvement of many different compounds in plant resistance, including primary compounds, volatile organic compounds, and phenolic compounds.…”