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Sultanova N. Influence of grapevine leafroll-associated virus 3 on the endogenous an-tioxidant system of field-grown Vitis vinifera L. plants. Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2026, Vol. 61, № 1, p. 189-204.
(how to cite this article)

doi: 10.15389/agrobiology.2026.1.189eng

UDC: 634.8:632.3:578

 

INFLUENCE OF GRAPEVINE LEAFROLL-ASSOCIATED VIRUS 3 ON THE ENDOGENOUS ANTIOXIDANT SYSTEM OF FIELD-GROWN Vitis vinifera L. PLANTS

N. Sultanova ✉

Azerbaijan State Oil and Industry University, Faculty of Chemical Technology, Department of Technology of Organic Substances and High-Molecular Compounds, 34, Azadliq Avenue, AZ1010, Baku, Azerbaijan, e-mail sultanova.nargiz@asoiu.edu.az (✉ corresponding author)

ORCID:
Sultanova N. orcid.org/0000-0002-4445-6902

Final revision received January 13, 2025
Accepted September 26, 2025

Viral infections exert a pronounced negative impact on the growth, development, and productivity of crops, causing significant yield losses worldwide. One of the key mechanisms underlying the damaging effects of viruses is the induction of oxidative stress, accompanied by excessive accumulation of reactive oxygen species (ROS) in plant cells. To maintain cellular homeostasis, plants utilize a complex antioxidant system that includes both enzymatic components (catalase, ascorbate peroxidase, etc.) and non-enzymatic low-molecular-weight metabolites ascorbate, glutathione, and tocopherols, forming an interconnected ascorbate—glutathione—tocopherol defense system. Grapevine leafroll-associated virus 3 (GLRaV-3) belongs to the genus Ampelovirus (family Closteroviridae) and is one of the most widespread and economically significant pathogens of grapevine. The infection is accompanied by characteristic symptoms, including reddening or yellowing of leaves, leaf rolling, and reduced sugar accumulation in berries, which ultimately affects both the quality and quantity of yield. In the present study, it was established for the first time that GLRaV-3 infection leads to a coordinated restructuring of the ascorbate—glutathione—tocopherol system in grapevine plants, accompanied by significant changes in the content of ascorbate, glutathione, and tocopherols, as well as enhanced activity of key antioxidant enzymes (catalase and ascorbate peroxidase). It was demonstrated that the increase in the components of the ascorbate—glutathione—tocopherol triad closely correlates with viral load intensity and the degree of lipid peroxidation (malondialdehyde, MDA content), indicating their involvement in the regulation of cellular redox homeostasis under viral stress. The coordinated functioning of this triad is accompanied by enhanced antioxidant protection and appears to be associated with metabolic reprogramming of cells, including processes related to secondary metabolite biosynthesis. The aim of the study was a comprehensive evaluation of the antioxidant potential of the ascorbate–glutathione–tocopherol triad to assess its role in the formation of grapevine resistance to GLRaV-3. During 2022-2023, surveys were conducted to identify symptoms of grapevine leafroll disease in the main grape-growing regions of Azerbaijan (Shamakhi, Ismayilli, and Salyan). Samples were collected from white grape cultivar Bayan Shire and red cultivars Madrasa and Kara Shany. Healthy, virus-free leaves served as controls. Samples were analyzed for the presence of GLRaV-3 using three diagnostic methods, the AgriStrip rapid immunochromatographic assay, double-antibody sandwich ELISA (DAS-ELISA), and reverse transcription followed by polymerase chain reaction (RT-PCR). Tocopherol content in the samples was determined spectrophotometrically based on the Emmerie-Engel reaction. Reduced glutathione content was measured using the reaction with 5,5′-dithiobis-2-nitrobenzoic acid at λ = 412 nm. The intensity of lipid peroxidation processes was assessed by calculating malondialdehyde (MDA) content in healthy and infected leaf samples. MDA content was determined spectrophotometrically using the thiobarbituric acid reaction. The concentration of ascorbic acid (AA) was also evaluated. Ascorbate peroxidase (APX) activity was determined by recording the decrease in optical density due to ascorbic acid oxidation at λ = 290 nm. Catalase (CAT) activity was determined at λ = 240 nm based on the rate of H₂O₂ decomposition over 1 minute. According to the results, virus-like symptoms were detected in both red and white cultivars, and RT-PCR confirmed infection in 21 out of 52 samples (40.3 %). The highest disease prevalence was observed in the Salyan region (32 %), followed by Ismayilli (28 %) and Shamakhi (16 %), indicating regional features of viral circulation. Biochemical analysis of the Kara Shany cultivar demonstrated a direct relationship between viral load and the severity of oxidative stress. MDA content increased significantly (p < 0.05) in all infected variants (6.5-7.9 µmolłg-1 fresh weight) compared to the control (2.27 µmolłg⁻1 fresh weight), indicating membrane damage. Simultaneously, activation of the antioxidant system was observed: ascorbate peroxidase and catalase activities increased 1.5-2.2 and 1.6-2.0 times, respectively (p < 0.05). Reduced glutathione content increased 1.6-2.4 times while ascorbic acid and tocopherol contents also increased, reaching maximum values under moderate and high viral load. The obtained data indicate that GLRaV-3 induces pronounced oxidative stress accompanied by activation of both enzymatic and non-enzymatic components of antioxidant defense. The increase in MDA levels alongside the enhanced antioxidant response suggests partial compensation of cellular damage and reflects specific features of the host–pathogen interaction. Interactions among antioxidants reflect the complex nature of the plant response to viral infection and underscore the importance of a deeper understanding of redox signaling pathways. Investigation of the specific roles of glutathione and ascorbic acid in virus-infected plants improves our understanding of plant–virus interactions and provides insight into potential targets for developing strategies to enhance plant resistance to viral pathogens.

Keywords: grapevine, viruses, metabolites, antioxidant enzymes.

 

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