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Transposon Tagging of Tobacco Mosaic Virus Resistance Gene N: Its Possible Role in the TMV-N-Mediated Signal Transduction Pathway S

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Transposon Tagging of Tobacco Mosaic Virus Resistance Gene N: Its Possible Role in the TMV-N-Mediated Signal Transduction Pathway S Proc. Natl. Acad. Sci. USA Vol. 92, pp. 4175-4180, May 1995 Colloquium Paper This paper was presented at a colloquium entitled "Self-Defense by Plants: Induction and Signalling Pathways," organized by Clarence A. Ryan, Christopher J. Lamb, Andre T. Jagendorf, and Pappachan E. Kolattukudy, held September 15-17, 1994, by the National Academy ofSciences, in Irvine, CA. Transposon tagging of tobacco mosaic virus resistance gene N: Its possible role in the TMV-N-mediated signal transduction pathway S. P. DINESH-KUMARt, STEVE WHITHAMt, DOIL CHOIt§, REINHARD HEHL¶II, CATHERINE CORRt, AND BARBARA BAKERt¶ Departments of tPlant Biology and SPlant Pathology, University of California, Berkeley, CA 94720; and IPlant Gene Expression Center, University of California, Berkeley, and U.S. Department of Agriculture-Agricultural Research Service, Albany, CA 94710 ABSTRACT Plants can recognize and resist invading elicitor interaction has been hypothesized to initiate signal- pathogens by signaling the induction of rapid defense re- transduction pathways leading to expression of disease- sponses. Often these responses are mediated by single domi- resistance responses (4, 7). nant resistance genes (R genes). The products ofR genes have Several avirulence genes from different pathogens corre- been postulated to recognize the pathogen and trigger rapid sponding to specific R genes have been cloned (8). In some host defense responses. Here we describe isolation of the cases, the role of the avirulence gene product as an elicitor has classical resistance gene N oftobacco that mediates resistance been established (9-12). However, the lack of knowledge to the well-characterized pathogen tobacco mosaic virus about the nature of R genes or their protein products has (TMV). The N gene was isolated by transposon tagging using limited the study of their role in pathogen recognition, signal the maize Activator (Ac) transposon. We confirmed isolation of transduction, and activation of HR. To date, two disease- the N gene by complementation of the TMV-sensitive phenotype resistance genes have been cloned: the HMI gene of maize and with a genomic DNA fragment. Sequence analysis of the N gene the Pto gene of tomato. The HM1 gene, which confers resis- shows that it encodes a protein with an amino-terminal domain tance to the fungal pathogen Cochliobolus carbonum Nelson similar to that of the cytoplasmic domains ofthe Drosophila Toll race 1, was cloned by transposon tagging (13). HM1 encodes protein and the interleukin 1 receptor in mammals, a putative an NADPH- and NADH-dependent Helminthosporium carbo- nucleotide-binding site and 14 imperfect leucine-rich repeats. num (HC) toxin reductase responsible for detoxification of the The presence ofthese functional domains in the predictedNgene cyclic tetrapeptide HC toxin produced by C. carbonum race 1 product is consistent with the hypothesis that the N resistance (14). The Pto gene, which confers resistance to Pseudomonas gene functions in a signal transduction pathway. Similarities of syringae pv. tomato carrying the avrPto gene, was isolated by N to Toll and the interleukin 1 receptor suggest a similar positional cloning (15). The amino acid sequence of Pto does signaling mechanism leading to rapid gene induction and TMV not suggest that it acts as a receptor, but it shows significant resistance. similarity to serine/threonine kinases. The Pto kinase may interact directly or indirectly with the avrPto-encoded elicitor The hypersensitive response (HR), characterized by rapid, molecule, then phosphorylate a subsequent modulator of the localized cell death and tissue necrosis at the site of pathogen resistance responses, thereby participating in a signal-trans- ingress, is an active, primary, defense response that occurs in duction cascade. Molecular characterization of cloned R genes a wide variety of plants. The HR is associated with the rapid and isolation of new R genes which confer resistance to viral, induction of a number of biochemical, physiological, and fungal, or bacterial pathogens is necessary to understand their molecular processes that prevent pathogen growth and spread. role in mediating resistance. Some of the responses of cells undergoing HR include the Genetic approaches to obtain loss-of-function mutants with oxidative burst leading to production of reactive oxygen in- altered resistance responses offer powerful means to isolate R termediates (ROIs), alteration of membrane potentials, in- genes and gain insight into their functions. The interaction creases in lipoxygenase activity, production of antimicrobial between the resistance gene N of tobacco and tobacco mosaic compounds, such as phytoalexins, lignin deposition, and the virus (TMV) has long served as a classical model for the study expression of defense-related genes (1-3). The molecular and of plant-resistance responses to pathogens and provides an biochemical processes that trigger HR in plants are largely excellent system for this approach. The dominant N gene was unknown. However, the induction of HR generally occurs introgressed into tobacco cultivars by crossing the TMV- following an interaction between the product of a resistance resistant (TMVR) speciesNicotianaglutinosa to TMV-sensitive (R) gene and a corresponding pathogen avirulence (Avr) gene (TMVS) Nicotiana tabacum, followed by repeated backcrosses product (4). This "corresponding genes" hypothesis was first to a recurrent TMVS tobacco Plants the described by Flor (5) in studies of the interaction of flax with parent (16). bearing the rust fungus,Melampsora lini. Since then, this simple genetic has been described for numerous Abbreviations: TMV, tobacco mosaic virus; HR, hypersensitive re- relationship plant-pathogen sponse; IL-1R, interleukin 1 receptor; NBS, nucleotide-binding site; interactions. Plant R genes that mediate HR are often single, LRR, leucine-rich repeat; RFLP, restriction fragment length polymor- dominant loci whose products may function as specific recep- phism; ROI, reactive oxygen intermediate; Ntr, truncated form of tors which interact, either directly or indirectly, with elicitors N protein. produced byAvrgenes carried bypathogens (6). This receptor- §Present address: Bioproducts Research Group, Genetic Engineering Research Institute, KIST, P.O. Box 115 Yoosung, Taejon 305-600, South Korea. The publication costs of this article were defrayed in part by page charge lPresent address: Institut fur Genetik, Technische Universitat Braun- payment. This article must therefore be hereby marked "advertisement" in schweig, Spielmannstrasse 7, D-38106 Braunschweig, Federal Repub- accordance with 18 U.S.C. §1734 solely to indicate this fact. lic of Germany. 4175 Downloaded by guest on September 27, 2021 4176 Colloquium Paper: Dinesh-Kumar et al Proc. Natl. Acad Sci. USA 92 (1995) N gene (NN tobacco) mount an HR to all strains of TMV will be discussed with respect to features central to Toll and except the ToMV-ob strain, thereby preventing the systemic IL-1R signaling pathways. spread of the virus beyond the initial infection site. In contrast, TMVS tobacco cultivars (nn tobacco) allow TMV to spread systemically and develop mosaic symptoms characterized by RESULTS AND DISCUSSION intermittent areas of dark green tissue mixed with light green Isolation of an Unstable TMV-Susceptible Mutant. We leaf tissue. utilized the Activator (Ac) transposon of maize (21) for TMV, the type member of the tobamovirus group, is me- insertional mutagenesis and isolation of the N gene. In to- chanically transmitted and one of the most extensively char- bacco, critical functional aspects ofAc transposition in maize acterized pathogens of plants. The genome of TMV consists of are retained (22). These include conservation ofAc structural a single positive-sense RNA of 6395 nucleotides and encodes integrity following transposition, generation of an 8-bp dupli- at least four proteins (17). Two proteins, 126 kDa and 183 kDa, cation at the site of insertion, generation of footprints upon are synthesized from genomic RNA and are involved in viral excision, and continued transposition over several generations replication. The 30-kDa, cell-to-cell movement protein and (23). The Ac transposon was introduced into the TMVR 17.5-kDa viral coat protein are translated from subgenomic tobacco cultivar Samsun NN, which is homozygous for the N RNAs. The precise viral component that elicits N-mediated gene. HR has not been strictly defined. However, one study suggests The isolation of Ac-induced mutations of N required gen- that the 126-kDa replicase protein is required for HR induc- eration and screening of large populations of F1 seedlings tion in NN tobacco (18). heterozygous for N (Nn) to identify potential loss-of-function The precise events required for the TMV-N-induced HR mutations. These mutants would be identified as plants unable and the subsequent defense pathway have not been estab- to mount a TMV-dependent HR. Therefore, we developed and lished. It has been hypothesized that N gene product may utilized a positive mutant-selection scheme that exploited the function as a receptor capable of recognizing a component of reversible temperature sensitivity of the N-mediated HR to TMV, thereby initiating subsequent defense responses. To TMV. At temperatures below 28°C, plants carrying the N gene begin elucidation of the molecular and biochemical basis of can mount an HR in response to TMV infection. However, it N-mediated TMV resistance, we have isolated the Ngene from has been shown that some component
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