Sulfate supply influences compartment specific glutathione metabolism and confers enhanced resistance to Tobacco mosaic virus during a hypersensitive response

Abstract

Sufficient sulfate supply has been linked to the development of sulfur induced resistance or sulfur enhanced defense (SIR/SED) in plants. In this study we investigated the effects of sulfate (S) supply on the response of genetically resistant tobacco (Nicotiana tabacum cv. Samsun NN) to Tobacco mosaic virus (TMV). Plants grown with sufficient sulfate (+S plants) developed significantly less necrotic lesions during a hypersensitive response (HR) when compared to plants grown without sulfate (−S plants). In +S plants reduced TMV accumulation was evident on the level of viral RNA. Enhanced virus resistance correlated with elevated levels of cysteine and glutathione and early induction of a Tau class glutathione S-transferase and a salicylic acid-binding catalase gene. These data indicate that the elevated antioxidant capacity of +S plants was able to reduce the effects of HR, leading to enhanced virus resistance. Expression of pathogenesis-related genes was also markedly up-regulated in +S plants after TMV-inoculation. On the subcellular level, comparison of TMV-inoculated +S and −S plants revealed that +S plants contained 55–132 % higher glutathione levels in mitochondria, chloroplasts, nuclei, peroxisomes and the cytosol than −S plants. Interestingly, mitochondria were the only organelles where TMV-inoculation resulted in a decrease of glutathione levels when compared to mock-inoculated plants. This was particularly obvious in −S plants, where the development of necrotic lesions was more pronounced. In summary, the overall higher antioxidative capacity and elevated activation of defense genes in +S plants indicate that sufficient sulfate supply enhances a preexisting plant defense reaction resulting in reduced symptom development and virus accumulation.

Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants

“…Recently, immunogold labeling was used to examine compartment-specific changes of glutathione in tobacco responding to an incompatible ( i.e. , HR-inducing) infection with tobacco mosaic virus (TMV) [223]. Interestingly, the mitochondrion exhibited a decline in glutathione level in response to TMV while its level tended to increase (or show little change) in the five other compartments examined.…”

Plant Resistance Inducers against Pathogens in Solanaceae Species—From Molecular Mechanisms to Field Application

“…So called sulfur-IR has been shown to be effective against TMV in tobacco [51]. This could be linked to increased glutathione levels and release of gluthatione from mitochondria upon TMV inoculation.…”

Oxidative stress and antioxidative responses in plant–virus interactions

“…In addition, OTC pretreatment considerably decreased both the number of necrotic lesions and the virus content in TMV-infected leaf discs [62]. Also, tobacco grown with a sufficient sulphate supply displayed significantly less HR-type necrotic lesions and reduced TMV accumulation coupled with at least 50% higher GSH levels in most intracellular organelles (mitochondria, chloroplasts, nuclei, peroxisomes and cytosol) as compared to controls [81]. These results point to the differential roles of GSH during virus resistance not only as an antioxidant but also as a defence signalling compound.…”