Molecular Chaperone Hsp90 Associates with Resistance Protein N and Its Signaling Proteins SGT1 and Rar1 to Modulate an Innate Immune Response in Plants

Liu, Yule; Burch‐Smith, Tessa M.; Schiff, Michael; Feng, Suhua; Dinesh‐Kumar, Savithramma P.

doi:10.1074/jbc.m310029200

Cited by 311 publications

(279 citation statements)

References 39 publications

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“…Not only is this indicated by high virus levels and the absence of HRtype necrotization, but also by the suppression of SA levels and defence-related genes encoding PR1, an epoxide hydrolase (EH-1) and a receptor-like protein kinase (WRK) (Malamy et al, 1992;Guo et al, 1998;Ito et al, 2002). The temperature sensitivity of N gene-mediated resistance to TMV could be caused by the effect of high temperatures on interactions between the N protein and other plant and virus-encoded proteins or on N gene transcription (Marathe et al, 2002;Liu et al, 2004;Takabatake et al, 2006). Our study, however, suggests that the N protein might be able to recognize TMV at high temperatures but the impaired expression of downstream signalling elements that are temperature sensitive (e.g.…”

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

113

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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

113

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“…The function of these proteins in disease resistance responses have been extensively investigated previously using mutant analyses Chandra-Shekara et al, 2004;Hubert el al., 2003;Lu et al, 2003;Shirasu et al, 1999;Takahashi et al, 2003) and by virus induced gene silencing (VIGS) analyses in several plant species (Bhattarai et al, 2007;de la Fuente van Bentem et al, 2005;Leister et al, 2005;Liu et al, 2004;Scofield et al, 2005). The data from these studies revealed differing specificities for these proteins in diverse NB-LRR-mediated resistance responses.…”

Section: Discussionmentioning

confidence: 99%

“…For example, RAR1 and SGT1 are required for MLA6-and MLA12-, but not MLA1-, mediated resistance (Azevedo et al, 2002). Tobacco N, a Tobacco mosaic virus resistance protein, and wheat Lr21, a Puccinia triticina resistance protein, require each of the proteins for the initiation of immune responses against pathogens (Liu et al, 2004;Lu et al, 2003;Peart et al, 2002;Scofield et al, 2005). The function of each of these chaperone proteins has not yet been fully explored in rice immune responses governed by NB-LRRs.…”

Section: Discussionmentioning

confidence: 99%

Differential Requirement of Oryza sativa RAR1 in Immune Receptor-Mediated Resistance of Rice to Magnaporthe oryzae

Song

Kim

Han

et al. 2013

Molecules and Cells

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The required for Mla12 resistance (RAR1) protein is essential for the plant immune response. In rice, a model monocot species, the function of Oryza sativa RAR1 (OsRAR1) has been little explored. In our current study, we characterized the response of a rice osrar1 T-DNA insertion mutant to infection by Magnaporthe oryzae, the causal agent of rice blast disease. osrar1 mutants displayed reduced resistance compared with wild type rice when inoculated with the normally virulent M. oryzae isolate PO6-6, indicating that OsRAR1 is required for an immune response to this pathogen. We also investigated the function of Os-RAR1 in the resistance mechanism mediated by the immune receptor genes Pib and Pi5 that encode nucleotide binding-leucine rich repeat (NB-LRR) proteins. We inoculated progeny from Pib/osrar1 and Pi5/osrar1 heterozygous plants with the avirulent M. oryzae isolates, race 007 and PO6-6, respectively. We found that only Pib-mediated resistance was compromised by the osrar1 mutation and that the introduction of the OsRAR1 cDNA into Pib/osrar1 rescued Pib-mediated resistance. These results indicate that OsRAR1 is required for Pib-mediated resistance but not Pi5-mediated resistance to M. oryzae.

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“…The SGT1 protein carries a TPR domain for binding heat shock protein 90 (HSP90) (Stemmann et al 2002). In 2003, several papers highlighted the role HSP90 in plant innate immune response (Hubert et al 2003;Liu et al 2004;Takahashi et al 2003). HSP90 was identified as an interacting partner of RAR1 and SGT1 in Arabidopsis, it is essential for RPS2-but not RPM1-dependent resistance .…”

Section: Components Participating In R-avr Protein Interactionmentioning

confidence: 99%

“…Both SGT1 and the RAR1-SGT1 complex interact with a ubiquitin ligase complex, which indicate that they may be involved in disease resistance related protein degradation pathways (Azevedo et al, 2002;Liu et al, 2002a;Peart et al, 2002). Several recent studies have also found that RAR1 and SGT1 are associated with the molecular chaperon HSP90 (Hubert et al, 2003;Liu et al, 2004;Liu et al, 2003;Takahashi et al, 2003).…”

Section: Introductionmentioning

confidence: 98%

Recognition and signal transduction in the expression of Phytophthora resistance in soybean [Glycine max (L) Merr]

Gao

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Molecular Chaperone Hsp90 Associates with Resistance Protein N and Its Signaling Proteins SGT1 and Rar1 to Modulate an Innate Immune Response in Plants

Cited by 311 publications

References 39 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

Differential Requirement of Oryza sativa RAR1 in Immune Receptor-Mediated Resistance of Rice to Magnaporthe oryzae

Recognition and signal transduction in the expression of Phytophthora resistance in soybean [Glycine max (L) Merr]

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