La Dolce Vita: A Molecular Feast in Plant–Pathogen Interactions
1997; Cell Press; Volume: 91; Issue: 1 Linguagem: Inglês
10.1016/s0092-8674(01)80005-2
ISSN1097-4172
Autores Tópico(s)Plant pathogens and resistance mechanisms
ResumoPlants are sessile organisms and lack a circulating, somatically adaptive immune system to protect themselves against pathogens. They instead have evolved other mechanisms for defense against a spectrum of pathogens. Plants are, in fact, resistant to most microorganisms by means of constitutive chemical or physical barriers such as cuticular coats of wax armor that a potential pathogen must penetrate or bypass. Disease is therefore the exception rather than the rule when microbes and plants meet. Yet yield loss due to plant disease remains an important component of modern agriculture, as many pathogens are evolutionarily specialized to overcome preformed defense barriers. Plant defense is based on recognition of specific pathogen molecules and subsequent induction of a broad defense response. Recognition evolves germinally, so that an individual plant can only defend itself with the spectrum genes it inherited from its parents. Genetic diversity among individuals is therefore essential for survival of the host species against rapidly evolving pathogens. Specific pathogen recognition is governed genetically by interactions between the product of a disease resistance (R) gene in the host and molecules encoded in a given pathogen isolate by so-called avirulence (avr) genes. If either the host plant or pathogen isolate lack the corresponding R or avr allele, then the pathogen can continue to colonize the host, reproduce, and ultimately cause disease. Alternatively, matching R and avr alleles enable pathogen recognition and a subsequent series of intracellular signal events in the host (see below). The simplest mechanistic interpretation of the genetics would posit R products as receptors for avr-encoded ligands. Recognition typically leads to rapid localized cell death of host cells penetrated by the pathogen, termed the hypersensitive response (HR). In many plant species, the local HR initiates a systemic response by which distal tissues in the host become resistant to secondary infection. In contrast to specific memory in mammalian immune systems, plant systemic acquired resistance (SAR) is pathogen nonspecific. Thus, for example, the response of a lower leaf to attempted infection by a bacterial pathogen can lead to protection against subsequent infection by, for example, a fungal pathogen. A detailed understanding of pathogen recognition signaling of the defense response will contribute to engineering of disease resistance in crops. Disease resistance mediated by genotype-specific pathogen recognition has recently emerged as a major topic for investigating signal transduction in plants, catalyzed by the cloning of at least 10 functional R genes from Arabidopsis, tomato, tobacco, flax, and rice (reviewed by9Dangl J.L Pièce de Résistance novel classes of plant disease resistance genes.Cell. 1995; 80: 363-366Abstract Full Text PDF PubMed Scopus (91) Google Scholar, 4Bent A Function meets structure in the study of plant disease resistance genes.Plant Cell. 1996; 8: 1757-1771PubMed Google Scholar, 15Hammond-Kosack K.E Jones J.D.G Plant disease resistance genes.Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996; 48 (b): 575-607Crossref Scopus (879) Google Scholar, 3Baker B Zambryski P Staskawicz B Dinesh-Kumar S.P Signaling in plant–microbe interactions.Science. 1997; 276: 726-733Crossref PubMed Scopus (778) Google Scholar). These confer resistance to bacterial, viral, fungal, and nematode pathogens with very different extracellular and intracellular lifestyles. Thus, it was astounding that all of these R genes encode a limited set of products with related structural features. The cloning of R genes continues apace and has recently been augmented by isolation of other key signal transduction components. Additionally, the last year has produced evidence that bacterial plant pathogens probably "inject" virulence and avirulence proteins directly into eukaryotic host cells. This is consistent with the requirement for evolutionarily conserved Type III secretion systems in these pathogens and with the finding that bacterial pathogens of mammals also use this system to deliver virulence factors to host cells. Current key questions in this research field include: what are the structures of plant R proteins? How is specificity determined, how do new specificities evolve, and how is genetic diversity organized and maintained in the host species? Do all R proteins directly interact with pathogen avr proteins? What are the molecular steps required for R-dependent recognition to be translated into disease resistance as measured by killing or inhibiting pathogen growth? What are the positive functions of avr proteins for pathogens? Recent advances to answer these questions were addressed by nearly 80 participants in a recent sun-bathed EMBO Workshop in Maratea, Italy organized by Jonathan Jones and Giulia DeLorenzo. The most striking feature in all known R proteins, with one exception described below, is a variable number of Leucine-Rich Repeats (LRRs). These occur in diverse proteins and function as sites of protein–protein interaction, peptide–ligand binding, and protein–carbohydrate interaction (reviewed23Kobe B Deisenhofer J Proteins with leucine rich repeats.Curr. Opin. Struct. Biol. 1995; 5: 409-416Crossref PubMed Scopus (318) Google Scholar, 20Jones D.A Jones J.D.G The roles of leucine rich repeats in plant defences.Adv. Bot. Res. Adv. Plant Pathol. 1996; 24: 90-167Google Scholar). While the precise role of LRR domains in R gene function is unknown, Jonathan Jones (Sainsbury Lab, Norwich, United Kingdom) showed that the products of four cloned tomato Cf resistance genes are predicted to consist almost entirely of LRR units, with a putative membrane anchor and a small cytoplasmic domain at their C terminus. Nearly all amino acid differences between Cf proteins are in the amino-terminal 30% of the LRR domains, suggesting that they determine specificity. These amino-terminal LRRs are highly variable. In a core of nine amino acids, both synonymous and nonsynonymous base pair substitutions occur at frequencies similar to that observed in MHC peptide binding sites, and in ratios (compared to the rest of the protein) indicative of positive selection. A second class of resistance proteins is defined by C-terminal LRR domains and three conserved motifs defining a nucleotide (ATP or GTP) binding site. This class of R proteins, christened "ucleotide-inding site plus eucine-ich epeat" or NB-LRR, is the largest to which specific resistance function can be ascribed. Both degenerate PCR experiments (22Kanazin V Marek L.F Shoemaker R.C Resistance gene analogs are conserved and clustered in soybean.Proc. Natl. Acad. Sci. USA. 1996; 93: 11746-11750Crossref PubMed Scopus (441) Google Scholar, 25Leister D Ballvora A Salamini F Gebherdt C A PCR based approach for isolating pathogen resistance genes from potato with potential for wide application in plants.Nat. Genet. 1996; 14: 421-429Crossref PubMed Scopus (457) Google Scholar, 45Yu Y.G Buss G.R Saghai-Maroof M.A Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site.Proc. Natl. Acad. Sci. USA. 1996; 93: 11751-11756Crossref PubMed Scopus (335) Google Scholar) and the Arabidopsis genome sequencing initiative (http://genome-www.stanford.edu/Arabidopsis/EST/R-EST_main.html) have uncovered a great number of these sequences, many of which map to regions harboring clusters of functionally defined resistance specificities (see Figure 1). The original members of NB-LRR class can be subdivided: RPS2 and RPM1 encode putative Leucine Zipper domains at their N termini, while N, L6, and RPP5 encode a domain with homology to the intercellular signaling domains of the Drosophila TOLL and mammalian Interleukin 1 receptors, termed the TIR. Computer predictions offer no solid clue as to their subcellular localization. Jeff Ellis (CSIRO, Canberra, Australia) described his group's dissection of the Flax L locus, one of the classic examples used to define the specific nature of plant-pathogen recognition several decades ago. Fourteen alleles have been described at L, one of which does not confer resistance to any known isolate of Flax rust. Following on the identification of L6 as a TIR-NB protein with two directly repeated 150 amino acid domains, Ellis described the structure of five additional L alleles. They are similar, and most variability is in the leucine-rich regions. The number of leucine-rich domains can be more or less than two, and internal deletions are observed. Ellis used both constructed chimeric L alleles and naturally occurring intra-allelic recombinants to show convincingly that the leucine-rich domains are major determinants of specificity. In addition, he presented tantalizing data suggesting that while specificity is largely determined in the leucine-rich regions, intramolecular interaction with sequences in the TIR is required for full function. Roger Innes (Indiana University, Bloomington, IN) described the RPS5 LZ-NB-LRR gene in Arabidopsis encoding resistance to isolates of Pseudomonas syringae expressing the appropriate avr gene. Interestingly, an rps5 mutant allele was selected that also dampens the function of different R specificities recognizing either P. syringae or Peronospora (with Eric Holub, HRI-Wellesbourne, UK). This allele carries a missense mutation that Innes postulates will be critical in intermolecular interactions, and he suggests that its negative effects on other R functions is via titration of a critical signal component. The cellular localization of NB-LRR proteins and the role of their conserved structural domains in transducing the specificity of avr signals are still mysteries. A functional requirement for the NB was described by Barbara Baker (USDA Plant Gene Expression Center, Albany, California). Using the tobacco N gene, which encodes resistance against Tobacco Mosaic Virus, Dinesh Kumar in Baker's lab engineered P-loop mutations based on known Ras phenotypes. Some gave dominant-negative or weak allele phenotypes when transformed into N plants and were nonfunctional in n backgrounds. Many of the weak allele phenotypes are accompanied by a virus-induced, spreading hypersensitive cell death. This "rolling HR," as it has been dubbed by Chris Lamb, maintains the temperature sensitivity known to govern N function, lending credence to the notion that these are in fact weak alleles. The dominant-negative mutations raise the possibility that N functions as a dimer and/or that function or binding of auxiliary proteins are compromised by N mutations. TIR and LRR mutations also eliminated N function, demonstrating that the predicted structural domains are necessary for N function. Doug Boyes (Dangl lab, University of North Carolina, Chapel Hill, NC) presented immunoprecipitation data suggesting that the Arabidopsis LZ-NB-LRR protein RPM1 is peripherally membrane-associated. The fact that this first subcellular localization of an NB-LRR protein in a plant cell is noteworthy speaks to the amount of work still required. The Pto resistance protein of tomato is a cytoplasmic kinase defining an additional R gene class. It determines resistance to P. syringae isolates expressing the corresponding avrPto gene. Recent observations suggest that Pto function is triggered by direct AvrPto–Pto interaction (39Scofield S.R Tobias C.M Rathjen J.P Chang J.H Lavelle D.T Michelmore R.W Staskawicz B.J Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato.Science. 1996; 274: 2063-2065Crossref PubMed Scopus (428) Google Scholar, 42Tang X Frederick R.D Zhou J Halterman D.A Jia Y Martin G.B Physical interaction of avrPto and the Pto kinase defines a recognition event involved in plant disease resistance.Science. 1996; 274: 2060-2063Crossref PubMed Scopus (502) Google Scholar), utilizes a phosphorylation cascade involving a second kinase, Pti1, which interacts with Pto (46Zhou J Loh Y Bressan R.A Martin G.B The tomato gene Pti encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response.Cell. 1995; 83: 925-935Abstract Full Text PDF PubMed Scopus (310) Google Scholar), and requires an LZ-NB-LRR protein called Prf (37Salmeron J.M Oldroyd G.E.D Rommens C.M.T Scofield S.R Kim H.-S Lavelle D.T Dahlbeck D Staskawicz B.J Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster.Cell. 1996; 86: 123-133Abstract Full Text Full Text PDF PubMed Scopus (443) Google Scholar). Greg Martin (Purdue University, West Lafayette, IN) reported that AvrPto mediates interaction of two Pto molecules in a yeast three-hybrid system. While Pto does not phosphorylate AvrPto, Martin proposes that the bacterial protein is the molecular bridge that affects cross-phosphorylation of Pto monomers. Martin's lab has narrowed down the region of Pto that confers recognition specificity for AvrPto to two amino acids predicted to be near a hydrophobic pocket, consistent with structural data from other Ser-Thr kinases. Finally, he discussed Pto interactors in addition to Pti1 (47Zhou J Tang X Martin G.B The Pto kinase conferring resistance of tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes.EMBO J. 1997; 16: 3207-3218Crossref PubMed Scopus (380) Google Scholar). These belong to a DNA binding protein family that includes factors implicated in regulating ethylene response genes (EREB proteins). Pti5 and Pti6 bind the same cis element as the EREBs, and these cis sequences exist in some plant defense gene promoters. In Martin's current model, Pti1 may be involved in regulating the HR, with Pti5 and Pti6 utilized to regulate at least part of the defense gene battery (see below). But this model still needs to account for the clear genetic requirement for Prf. The final R gene structural class combines extracellular LRRs, like Cf proteins, with a Pto-like kinase domain. The prototype is Xa21, a rice receptor–like kinase determining resistance to Xanthomonas oryzae. There are seven Xa21 gene family members at the locus from which the gene was cloned. Pam Ronald (University of California, Davis) described a role for transposon insertion and duplication as generators of duplication and diversity at Xa21 (41Song W.-Y Pi L.-Y Wang G.-L Gardner J Holsten T Ronald P.C Evolution of the rice Xa21 disease resistance gene family.Plant Cell. 1997; 9: 1279-1287PubMed Google Scholar). Xa21 is effective against 29/32 X. oryzae field isolates and transgenic Xa21 expression in two high-yield rice cultivars planted on over 2.5 million hectares in Asia protects against infection. These two cultivars suffer serious losses due to X. oryzae infection, highlighting the agronomic relevance of this research. In an effort to recognize the importance of diverse germplasm sources (Xa21 was originally introgressed from a wild rice relative from West Africa), Ronald has reached an agreement with University of California, Davis whereby a portion of future royalties arising from this and other research at University of California, Davis reliant on imported germplasm will support training of scientists from developing countries. Other LRR-containing proteins play diverse roles in plant development and cell biology (20Jones D.A Jones J.D.G The roles of leucine rich repeats in plant defences.Adv. Bot. Res. Adv. Plant Pathol. 1996; 24: 90-167Google Scholar). Giulia DeLorenzo (University of Rome, Italy) summarized analyses of the polygalacturonase (PG) inhibitor proteins from tomato and bean (PGIPs; 11De Lorenzo G Cervone F Bellincampi D Caprari C Clark A.J Desiderio A Devoto A Forrest R Leckie F Nuss L Salvi G Polygalacturonase, PGIP, and oligogalacturonides in cell–cell communication.Biochem. Soc. Trans. 1994; 22: 394-397PubMed Google Scholar). These are extracellular, consist entirely of LRRs, and bind to and inhibit fungal PG proteins. The latter are plant cell wall–degrading enzymes and potential pathogenicity factors. Four PGIP genes have been isolated from bean. Two have been expressed in heterologous systems, and characterization of the proteins shows that amino acid substitution is sufficient to confer changed recognition of PGs. Analysis of the structural basis of PGIP–PG interaction may provide a model for how plants' LRR proteins have evolved to recognize pathogen-derived molecules. As alluded to above, R genes are commonly organized as clusters in plant genomes. These clusters presumably provide a selective advantage by pyramiding numerous specificities that will protect a host individual against many parasite genotypes, and benefit the host species by providing a reservoir of genetic material from which new specificities can evolve. Jones compared DNA sequence and genome organization of the Cf homologs (Hcf) at the locus containing either Cf-9, Cf-4, or the allelic position in tomato cultivars lacking known Cf function. The intergenic regions of allelic positions within the Hcr loci are divergent in organization, but homologous in sequence. This may provide templates for unequal recombination and may also inhibit homogenization of the coding sequences. Similar mechanisms probably exist at other complex loci. Scot Hulbert (Kansas State University, Manhattan, KS) described a cluster of Puccinia sorghi (rust) resistance genes in maize. From genetic evidence, the cluster contains at least three loci including the complex locus Rp1. This locus is a region of less than 1 cM that contains a variable number of R genes that recombine frequently, via both gene conversion and unequal crossing-over that can cause duplication and deletion of genes. New combinations of R genes from parental haplotypes as well as genes with altered phenotypes such as lesion mimics and novel resistance genes derived from two susceptible parents have been observed (32Richter T.E Pryor T.J Bennetzen J.B Hulbert S.H New rust resistance specificities associated with recombination in the Rp1 complex in maize.Genetics. 1995; 141: 373-381PubMed Google Scholar, 17Hu G Richter T.E Hulbert S.H Pryor T Disease lesion mimicry caused by mutations in the rust resistance gene rp1.Plant Cell. 1996; 8: 1367-1376PubMed Google Scholar). Evidence for unequal crossing-over driving the recent evolution of R-gene clusters has, however, not been found from extensive medium-range DNA sequencing at the Pto locus in tomato and in the major cluster of downy mildew resistance (Dm) genes in lettuce. Richard Michelmore (University of California, Davis) described a comparison among members of the Pto family from both resistant and susceptible haplotypes, and sequence comparisons between homologs of an NB-LRR gene cluster in cultivated and wild genotypes of lettuce. Sequence divergence among homologs within a given gene cluster appears to be ancient with no evidence of gene conversion events homogenizing family members. In addition, sequence comparisons of the NB regions from more than 50 NB-LRR gene fragments from lettuce (including a candidate Dm3 gene) and other plant species indicated the presence of ancient families of NB-LRR genes that perhaps predate the divergence between monocot and dicot species. The biotrophic oomycete Peronospora parasitica (downy mildew) is an excellent model eukaryotic parasite for genetic analysis of disease resistance in Arabidopsis, and more than twenty RPP specificities for downy mildew resistance have been identified genetically (reviewed by16Holub E.B Beynon J.L Symbiology of Mouse Ear Cress (Arabidopsis thaliana) and oomycetes.Adv. Bot. Res. 1996; 24: 228-273Google Scholar). Holub described how most of these reside in clusters, including two major RPP clusters on chromosomes 3 and 5 (MRC-F and MRC-J, respectively). MRC-F contains RPP1, which is in the first complex locus (<1 cM region) identified in Arabidopsis shown by genetic recombination, mutation, and transformation experiments to contain several R specificities. Genes for resistance to other pathogens have been identified in MRC-J by several groups, including resistance to viruses, three different bacterial species, and the oomycete Albugo candida. Holub also described F2 segregation data from two self-fertile isolates of Peronospora including evidence for a single avirulence gene corresponding to RPP1, both confirming that the gene-for-gene relationship exists in this pathosystem and opening the doors of genetics in this parasite. In this pathosystem, Jane Parker (Sainsbury Lab, Norwich, United Kingdom) described isolation of RPP5, encoding a TIR-NB-LRR protein (29Parker J.E Coleman M.J Szabo V Frost L.N Schmidt R van der Biezen E Moores T Dean C Daniels M.J Jones J.D.G The Arabidopsis downy mildew resistance gene Rpp5 shares similarity to the Toll and Interleukin-1 receptors with N and L6.Plant Cell. 1997; 9: 879-894Crossref PubMed Scopus (333) Google Scholar). In Arabidopsis accession Ler-0, which expresses RPP5, there is only one functional copy and six partial homologs. In addition, there is an expressed open reading frame encoding a protein identical to the amino-terminal region of RPP5 (termed homolog 1). This is a new twist on the alternative splice products encoding essentially the same domain observed by Ellis and Baker for L6 and N, respectively. Baker presented data suggesting that both are required for correct N function, but the identification of RPP5 via complementation did not include coexpression of the homolog 1. In the recipient accession for Parker's complementation test, Col-0, 7 of 8 rpp homologs are transcribable, but there is no obvious homolog 1 allele in the cluster. This suggests that homolog 1 is not required for RPP5 function, or that a redundant function is present in Col-0. Early signaling events following R gene engagement are calcium influx, K+–H+ exchange leading to alkalinization of the extracellular space, and an oxidative burst, all of which may have a direct role in halting further pathogen growth. These lead to transcriptional activation of a battery of defense-related genes in and surrounding the infected cell, resulting in alicylic cid (SA) biosynthesis, cell wall strengthening, lignification, production of various antimicrobial compounds, and the HR among others (reviewed by10Dangl J.L Dietrich R.A Richberg M.H Death don't have no mercy cell death programs in plant–microbe interactions.Plant Cell. 1996; 8: 1793-1807PubMed Google Scholar, 14Hammond-Kosack K.E Jones J.D.G Inducible plant defense mechanisms and resistance gene function.Plant Cell. 1996; 8 (a): 1773-1791PubMed Google Scholar). This local defense response stimulates establishment of pathogen-nonspecific ystemic cquired esistance (SAR; reviewed by36Ryals J.L Neuenschwander U.H Willits M.C Molina A Steiner H.-Y Hunt M.D Systemic acquired resistance.Plant Cell. 1996; 8: 1809-1819PubMed Google Scholar). SA accumulates to very high levels locally at infection sites undergoing HR. In at least tobacco and Arabidopsis, enzymatic blocking of salicylic acid (SA) accumulation subsequent to infection seriously impairs function of at least some R genes, and SA is required in distal tissues for SAR. It is unclear whether these signaling events are components of the same linear pathway or represent interdigitating signal pathways. Most importantly, it is unclear which of these events are causal mediators of R gene action, meaning that they lead directly to halting pathogen growth. Genetic screens have identified loci required for R gene action, and it is likely that some encode proteins that mediate the series of events outlined above. Parker described a mutation, eds1 for e nhanced d isease s usceptibility (30Parker J.E Holub E.B Frost L.N Falk A Gunn N.D Daniels M.J Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes.Plant Cell. 1996; 8: 2033-2046PubMed Google Scholar), that abolishes function of most known RPP specificities (except RPP8, which the Dangl lab has putatively identified as an LZ-NB-LRR) as well as P. syringae resistance conferred by RPS4. It also partially modifies "nonhost" resistance to isolates of Peronospora and Albugo candida (white blister) isolated from Brassica. In addition to its lack of effect on RPP8, eds1 also does not appear to abolish function of other P. syringae R genes encoding LZ-NB-LRR domains, suggesting that it may be specifically required by TIR domain containing R proteins. While most attention has focused on screens for loss of resistance, Fred Ausubel (Massachusetts General Hospital, Boston, MA) described mutants that express enhanced disease susceptibility following infection with subclinical doses of P. syringae (13Glazebrook J Zook M Mert F Kagan I Rogers E.E Crute I.R Holub E.B Ausubel F.M Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance.Genetics. 1997; 146: 381-392Crossref PubMed Google Scholar, 33Rogers E.E Ausubel F.M Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression.Plant Cell. 1997; 9: 305-316Crossref PubMed Scopus (191) Google Scholar). Twenty-seven eds mutants define at least 11 new loci required for limiting virulent pathogen growth. Some of these are impaired in SAR induction, including three new npr1/nim1 alleles (described below). However, at least one eds mutant impaired in local containment of pathogen spread is still able to efficiently induce SAR. Innes described additional mutants (termed pbs1–pbs3) from their screen for impaired RPS5 function, and Andrew Bent (University of Illinois, Champaign-Urbana, IL) described a mutant that expresses bacterial resistance without an HR. Holub described how many of these mutations also affect Peronospora resistance, demonstrating that a large number of genes can play a pathogen-nonspecific role in disease resistance. For example, in addition to alteration of bacterial resistance, at least 14 of the mutants available in the Col-0 impaired expression of Peronospora resistance conferred by RPP4. These mutational analyses of disease resistance and pathogen containment in Arabidopsis are strengthened by the availability of a standard set of Pseudomonas and Peronospora isolates that trigger resistance through different R genes. Further characterization of these mutants will address a long-standing question, namely whether or not the role of R genes is to temporally hasten a basic pathogen-nonspecific response intrinsic to all plant cells. If so, then the prediction is that some eds loci will also turn out to be modifiers of R action. This prediction is partially born out by the finding that some eds isolates are alleles of the previously identified pad mutants, which can modify RPP gene function (13Glazebrook J Zook M Mert F Kagan I Rogers E.E Crute I.R Holub E.B Ausubel F.M Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance.Genetics. 1997; 146: 381-392Crossref PubMed Google Scholar). Given the importance of SA in transducing pathogen signals, it is not surprising that several groups have sought mutants that are unable to establish SAR. Xinnian Dong (Duke University, Durham, NC) and Michelle Hunt (Novartis Crop Protection, Research Triangle Park, NC) described the independent isolations of the Arabidopsis NPR1/NIM1 gene. Mutants in this gene lose the ability to respond to either pathogen or chemical signals that normally induce SAR. Additionally, they are compromised for at least some R functions and for the ability to limit the spread of a virulent pathogen (see above). The NPR1/NIM1 protein contains repeated ankyrin domains (8Cao H Glazebrook J Clark J.D Volko S Dong X The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.Cell. 1997; 88: 57-64Abstract Full Text Full Text PDF PubMed Scopus (1067) Google Scholar) that may have broad similarity to IκB (35Ryals J Weymann K Lawton K Friedrich L Ellis D Steiner H.-Y Johnson J Delaney T.P Jesse T Vos P Uknes S The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB.Plant Cell. 1997; 9: 425-439PubMed Google Scholar). Dong provided evidence that overexpression of NPR1 can lead to resistance against otherwise virulent pathogens. She also showed that an NPR1-GFP fusion protein complements the mutant phenotype and is localized to the nucleus upon activation of the SA-dependent resistance pathway by either SAR-inducing chemicals or avirulent pathogen. Another class of mutants mimics either infection or the HR. Many of these mutants are constitutively "on" for conferring disease resistance to normally virulent pathogens when expressing lesions, arguing that they represent normal steps in the response to infection (reviewed by6Briggs S.P Johal G.S Genetic patterns of plant host–parasite interactions.Trends Genet. 1994; 10: 12-16Abstract Full Text PDF PubMed Scopus (32) Google Scholar, 10Dangl J.L Dietrich R.A Richberg M.H Death don't have no mercy cell death programs in plant–microbe interactions.Plant Cell. 1996; 8: 1793-1807PubMed Google Scholar). Jeff Dangl (University of North Carolina, Chapel Hill, NC) described the Arabidopsis LSD1 gene, which encodes a new subclass of GATA-1-like zinc-finger protein (12Dietrich R.A Richberg M.H Schmidt R Dean C Dangl J.L A novel zinc-finger protein is encoded by the Arabidopsis lsd1 gene and functions as a negative regulator of plant cell death.Cell. 1997; 88: 685-694Abstract Full Text Full Text PDF PubMed Scopus (352) Google Scholar). The lsd1 mutant is normal under permissive conditions, but either pathogen o
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