Suppression of tobacco mosaic virus-induced hypersensitive-type necrotization in tobacco at high temperature is associated with downregulation of NADPH oxidase and superoxide and stimulation of dehydroascorbate reductase

Abstract

Tissue necroses and resistance during the hypersensitive response (HR) of tobacco to tobacco mosaic virus (TMV) are overcome at temperatures above 28 6C and the virus multiplies to high levels in the originally resistant N-gene expressing plants. We have demonstrated that chemical compounds that generate reactive oxygen species (ROS) or directly applied hydrogen peroxide (H 2 O 2 ) are able to induce HR-type necroses in TMV-inoculated Xanthi-nc tobacco even at high temperatures (e.g. 30 6C). The amount of superoxide (O 2 $ " ) decreased, while H 2 O 2 slightly increased in TMV-and mock-inoculated leaves at 30 6C, as compared with 20 6C. Activity of NADPH oxidase and mRNA levels of genes that encode NADPH oxidase and an alternative oxidase, respectively, were significantly lower, while activity of dehydroascorbate reductase was significantly higher at 30 6C, as compared with 20 6C. It was possible to reverse or suppress the chemically induced HR-type necrotization at 30 6C by the application of antioxidants, such as superoxide dismutase and catalase, demonstrating that the development of HR-type necroses indeed depends on a certain level of superoxide and other ROS. Importantly, high TMV levels at 30 6C were similar in infected plants, whether the HR-type necrotization developed or not. Suppression of virus multiplication in resistant, HR-producing tobacco at lower temperatures seems to be independent of the appearance of necroses but is associated with temperatures below 28 6C. INTRODUCTIONOne of the best characterized plant-pathogen interactions is the hypersensitive type of resistance (HR) elicited by tobacco mosaic virus (TMV) in tobacco (Nicotiana tabacum). It is known that in the case of the tobacco2 TMV interaction, the HR is governed by the interaction of proteins encoded by the tobacco N (necrosis) gene (Holmes, 1938) and the replicase gene of TMV (Padgett & Beachy, 1993;Padgett et al., 1997). A typical HR is characterized by localized necrotic lesions around the infection sites. It was shown as early as 1931 that tissue necroses associated with the HR of Xanthi-nc tobacco to TMV do not develop at temperatures above 28 u C and the virus multiplies to high levels in the originally resistant N-gene expressing plants (Samuel, 1931). Doke & Ohashi (1988) showed that in TMV-infected Ngene expressing local lesion tobacco hosts, a superoxide (O 2 $ 2 ) generating system is induced. However, this is not the case with systemic hosts lacking the N resistance gene, where virus multiplication and spread are accompanied by non-necrotic symptoms. Furthermore, in a transgenic local lesion host (NahG tobacco) that produces large necrotic lesions upon TMV infection, an increased level of O 2 $ 2 and hydrogen peroxide (H 2 O 2 ) production can be detected at the edge of necrotic spots, as compared with the control non-transgenic tobacco that displays normal-sized lesions (Király et al., 2002). Some investigators claimed that reactive oxygen species (ROS) like O 2 $ 2 and H 2 O 2 could be responsible not only for host cell...

Heat shock, with recovery, promotes protection of Nicotiana tabacum during subsequent exposure to Ralstonia solanacearum

“…This reveals a hierarchical response to stress where the HS response has priority over a pathogen response (Schweizer et al 1995). Resistance to HRtype necrosis was overcome in TMV-infected tobacco kept at high temperature (30°C), as seen by decreased ROS, SA, and PR proteins, leading to eventual virus replication and spread (Király et al 2008). This highlights the importance of recovery after HS, prior to pathogen exposure, allowing chaperone production without jeopardizing defense protein production.…”

“…ETI is often accompanied by accumulation of reactive oxygen species (ROS), triggering the hypersensitive response (HR). HR is a rapid form of programed cell death (PCD) associated with plant defense (Espinosa and Alfano 2004) and characterized, morphologically, by the formation of localized necrotic lesions around the site of pathogen entry (Király et al 2008). HR isolates the pathogen, preventing dissemination and further damage while limiting pathogen access to water and nutrients (Coll et al 2011).…”

Overexpression of a tobacco Dof transcription factor BBF1 stimulates the transcription of the tobacco mosaic virus resistance gene N and defense-related responses including ROS production

“…Additionally, we analyzed the profile of the expression of NtrbohD, a NADPH oxidase gene that may be involved in ROS production during TMV-induced HR (Király et al 2008). Although the gene expression of NtrbohD in BBF1-overexperssing and control leaves increased after agrobacterium infiltration, there were no significant differences in mRNA levels between the two leaves.…”

“…Production of ROS is associated with N-mediated HR upon TMV infection or p50 expression in tobacco (Allan et al 2001;Király et al 2008;Ogata et al 2012). We examined the effect of BBF1 overexpression on ROS production in both Samsun nn and Samsun NN tobacco.…”

Antioxidant and Oxidant Levels of Pepper (Capsicum annuum cv. ‘Charlee’) Infected with Pepper Mild Mottle Virus

“…Symptoms of virus infection in pepper plants usually develops within 1-3 weeks of infection (Anandakumar et al, 2008). When plants are attacked by pathogens they respond by activating a variety of defense mechanisms, including the rapid production and accumulation of ROS (reacting oxygen species) (Kiraly et al, 2008). On the other hand, the phenolic content of the plants increases as a response of the defense mechanism (Katoh et al, 2009).…”