Nicotiana benthamiana gp91phox Homologs NbrbohA and NbrbohB Participate in H2O2 Accumulation and Resistance to Phytophthora infestans

Yoshioka, Hirofumi; Numata, Noriko; Nakajima, Kazumi; Katou, Shinpei; Kawakita, Kazuhito; Rowland, Owen; Jones, Jonathan D. G.; Doke, Noriyuki

doi:10.1105/tpc.008680

Cited by 559 publications

(458 citation statements)

References 64 publications

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“…tomato DC3000 (Avr Rpm1) . Furthermore, there is genetic evidence that plant NADPH oxidases involved in responses to pathogen attack are activated by mitogen-activated protein kinase kinases (Yoshioka et al, 2003;Yamamizo et al, 2006). It remains to be seen whether in TMV-infected plants the decrease in NADPH oxidase activity at 30 u C is a consequence of a lack of mitogen-activated protein kinase kinase activation.…”

Section: Discussionmentioning

confidence: 99%

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

Király

Hafez

Fodor

et al. 2008

Journal of General Virology

115

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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...

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Section: Discussionmentioning

confidence: 99%

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

Király

Hafez

Fodor

et al. 2008

Journal of General Virology

115

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“…The cDNAs of 2 RBOHs were described in Nicotiana benthamiana: NbRBOHA expressed constitutively at low levels and NbRBOHB induced by the elicitor INF1 from the oomycete P. infestans a pathogen of potato. When these genes were silenced by virus-induced gene silencing the suppressed plants show a reduction in ROS accumulation and INF1-induced cell death, along with a loss in resistance to P. infestans (Asai et al, 2008;Yoshioka et al, 2003).…”

Section: Ros and Resistance To Fungal Pathogens Of Leavesmentioning

confidence: 99%

Reactive oxygen species and plant resistance to fungal pathogens

et al. 2015

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Reactive oxygen species (ROS) have been studied for their role in plant development as well as in plant immunity. ROS were consistently observed to accumulate in the plant after the perception of pathogens and microbes and over the years, ROS were postulated to be an integral part of the defence response of the plant. In this article we will focus on recent findings about ROS involved in the interaction of plants with pathogenic fungi. We will describe the ways to detect ROS, their modes of action and their importance in relation to resistance to fungal pathogens. In addition we include some results from works focussing on the fungal interactor and from studies investigating roots during pathogen attack.

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“…RbohD or RbohF loss of function increases the susceptibility of host plants to infection by fungi or bacteria (3,6,8). We asked whether A. thaliana Rboh-family NADPH oxidases were involved in H. schachtii infection.…”

Section: Rbohd and Rbohf Promote Nematode Parasitismmentioning

confidence: 99%

“…Rbohs generate ROS in response to bacterial and fungal pathogens (3,6), and genetic disruption of specific Rbohs alters plant responses to pathogens (7)(8)(9). In A. thaliana, loss of RbohF enhances cell death and increases resistance to a weakly virulent strain of the oomycete Hyaloperonospora parasitica (3).…”

Section: Introductionmentioning

confidence: 99%

Parasitic Worms Stimulate Host NADPH Oxidases to Produce Reactive Oxygen Species That Limit Plant Cell Death and Promote Infection

et al. 2014

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Plants and animals produce reactive oxygen species (ROS) in response to infection. In plants, ROS not only activate defense responses and promote cell death to limit the spread of pathogens but also restrict the amount of cell death in response to pathogen recognition. Plants also use hormones, such as salicylic acid, to mediate immune responses to infection. However, there are long-lasting biotrophic plant-pathogen interactions, such as the interaction between parasitic nematodes and plant roots during which defense responses are suppressed and root cells are reorganized to specific nurse cell systems. In plants, ROS are primarily generated by plasma membrane-localized NADPH (reduced form of nicotinamide adenine dinucleotide phosphate) oxidases, and loss of NADPH oxidase activity compromises immune responses and cell death. We found that infection of Arabidopsis thaliana by the parasitic nematode Heterodera schachtii activated the NADPH oxidases RbohD and RbohF to produce ROS, which was necessary to restrict infected plant cell death and promote nurse cell formation. RbohD-and RbohF-deficient plants exhibited larger regions of cell death in response to nematode infection, and nurse cell formation was greatly reduced. Genetic disruption of SID2, which is required for salicylic acid accumulation and immune activation in nematode-infected plants, led to the increased size of nematodes in RbohD-and RbohF-deficient plants, but did not decrease plant cell death. Thus, by stimulating NADPH oxidase-generated ROS, parasitic nematodes fine-tune the pattern of plant cell death during the destructive root invasion and may antagonize salicylic acid-induced defense responses during biotrophic life stages.

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Nicotiana benthamiana gp91^phox Homologs NbrbohA and NbrbohB Participate in H₂O₂ Accumulation and Resistance to Phytophthora infestans

Cited by 559 publications

References 64 publications

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

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

Reactive oxygen species and plant resistance to fungal pathogens

Parasitic Worms Stimulate Host NADPH Oxidases to Produce Reactive Oxygen Species That Limit Plant Cell Death and Promote Infection

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