Glutathione contributes to resistance responses to TMV through a differential modulation of salicylic acid and reactive oxygen species

• Published in: Molecular plant pathology Vol. 22; no. 12; pp. 1668 - 1687
• Main Authors: Zhu, Feng, Zhang, Qi‐Ping, Che, Yan‐Ping, Zhu, Peng‐Xiang, Zhang, Qin‐Qin, Ji, Zhao‐Lin
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01-12-2021; John Wiley and Sons Inc
• Subjects: Accumulation; Antioxidants; Bacterial infections; Biosynthesis; Buthionine sulfoximine; By products; Carboxylic acids; Cloning; Damage accumulation; Disease Resistance; Enzymes; Flowers & plants; Gene expression; Gene Expression Regulation, Plant; Genes; Genetics; Glutathione; Homeostasis; Infections; Metabolites; Modulation; Nicotiana - metabolism; Nicotiana - virology; Nicotiana benthamiana; Original; Oxidation resistance; Oxidative stress; Pathogens; Plant diseases; Plant Diseases - virology; Plant Proteins - metabolism; Plant resistance; Plant virus diseases; Reactive oxygen species; Reactive Oxygen Species - metabolism; Salicylic acid; Salicylic Acid - metabolism; Scavenging; Signal transduction; Signaling; systemic resistance; Tobacco; Tobacco Mosaic Virus; Tobamovirus; Viral infections; Viruses; Nicotiana benthamiana; salicylic acid; systemic resistance; tobacco mosaic virus; glutathione; reactive oxygen species
• ISSN: 1464-6722; 1364-3703
• DOI: 10.1111/mpp.13138

Systemic acquired resistance (SAR) is induced by pathogens and confers protection against a broad range of pathogens. Several SAR signals have been characterized, but the nature of the other unknown signalling by small metabolites in SAR remains unclear. Glutathione (GSH) has long been implicated in the defence reaction against biotic stress. However, the mechanism that GSH increases plant tolerance against virus infection is not entirely known. Here, a combination of a chemical, virus‐induced gene‐silencing‐based genetics approach, and transgenic technology was undertaken to investigate the role of GSH in plant viral resistance in Nicotiana benthamiana. Tobacco mosaic virus (TMV) infection results in increasing the expression of GSH biosynthesis genes NbECS and NbGS, and GSH content. Silencing of NbECS or NbGS accelerated oxidative damage, increased accumulation of reactive oxygen species (ROS), compromised plant resistance to TMV, and suppressed the salicylic acid (SA)‐mediated signalling pathway. Application of GSH or l‐2‐oxothiazolidine‐4‐carboxylic acid (a GSH activator) alleviated oxidative damage, decreased accumulation of ROS, elevated plant local and systemic resistance, enhanced the SA‐mediated signalling pathway, and increased the expression of ROS scavenging‐related genes. However, treatment with buthionine sulfoximine (a GSH inhibitor) accelerated oxidative damage, elevated ROS accumulation, compromised plant systemic resistance, suppressed the SA‐mediated signalling pathway, and reduced the expression of ROS‐regulating genes. Overexpression of NbECS reduced oxidative damage, decreased accumulation of ROS, increased resistance to TMV, activated the SA‐mediated signalling pathway, and increased the expression of the ROS scavenging‐related genes. We present molecular evidence suggesting GSH is essential for both local and systemic resistance of N. benthamiana to TMV through a differential modulation of SA and ROS.
Glutathione is required for both local and systemic resistance of Nicotiana benthamiana to tobacco mosaic virus infection through a differential modulation of salicylic acid signalling and reactive oxygen species.