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Plant Physiology 142:809-811 (2006) © 2006 American Society of Plant Biologists Plant Response to Bacterial Pathogens. Overlap between Innate and Gene-for-Gene Defense ResponseUniversity of Illinois, Urbana, IL 61801
The immune system's role as defense from opportunistic microbes also necessitated the ability to distinguish between "self" and "non-self" to ensure that an immune response is not mounted against the organism's own tissues. This discrimination is partially achieved by the recognition of an invader's chemical motifs by host surface receptors. Consequently, potential pathogens have adapted numerous ways to overcome host immune systems while the hosts respond with new defenses. In plants, this ongoing "battle" against pathogens has led to two types of immune responses: an older, basal response to pathogen-associated molecular patterns (PAMPs) and a gene-for-gene response specific to a pathogen. This month's selection for High Impact examines the immune response of Arabidopsis (Arabidopsis thaliana) to one such PAMP and the interaction between the two immune responses. The article is "The Transcriptional Innate Immune Response to flg22. Interplay and Overlap with Avr Gene-Dependent Defense Responses and Bacterial Pathogenesis" by Lionel Navarro, Cyril Zipfel, Owen Rowland, Ingo Keller, Silke Robatzek, Thomas Boller, and Jonathan D.G. Jones. It appeared in our June 2004 issue in the section "Plants Interacting with Other Organisms." As of September 2006, it had been cited 35 times according to Thompson ISI (Thompson ISI Web of Science, http://www.isinet.com).
Plants have evolved multiple defense strategies for combating invading pathogens. The exterior surfaces of plants have waxy cuticles and preformed antimicrobials to prevent the entry of many would-be invaders. Cell walls provide an effective second barrier to any invaders that are able to gain access to interior spaces. Any invaders that overcome both barriers must still face the formidable task of overcoming the plant immune response. Plant immunity can be broken down into two components operating on different time scales. The basal defense system appears early in pathogen interaction, while the resistance (R) gene-mediated defense operates on the time scale of hours.
The early basal response is mediated by PAMPs, which include lipopolysaccharide, peptidoglycan, bacterial flagellin, and mannans of yeast (for review, see Nurnberger et al., 2004
Flagellin, the major protein of flagella as well as a well characterized PAMP, has been shown to be recognized by the Leu-rich repeat receptor kinase FLS2 in Arabidopsis. FLS2, located in the plasma membrane, is believed to be involved in early bacterial-plant interaction by recognizing and binding flagellin. Bacterial effector proteins are an array of bacterial proteins shown to be involved in overcoming of host defense systems. Included among bacterial effector proteins are avirulence (Avr) factors that can interact with host R proteins, if present, as part of the gene-for-gene interaction (Dangl and McDowell, 2006
An effective virulence strategy of plant (and animal) pathogens is to secrete effector proteins or DNA into the host cell to attempt to overcome plant defense systems. In phytopathogenic bacteria, there are three types of secretion systems. Type II, found in the genus Erwinia, is used for the secretion of cell wall-degrading enzymes causing soft-rot, while type IV transfers proteins and DNA of Agrobacterium. A third type, type III (T3SS), typical of Pseudomonas pathovars, secretes effector proteins into the plant cell (for review, see Abramovitch et al., 2006 Gene-for-gene-mediated defense is inherited and is specific to a particular pathogen. Plants have dominant R genes whose products recognize those of the pathogen's complementary Avr alleles. Avr proteins are effector proteins secreted into the plant cell to promote pathogen virulence and to overcome host defenses. Localized programmed cell death, the hypersensitive response, is a hallmark of R gene-mediated defense and also a target of effector proteins.
Navarro et al. (2004)  were interested in investigating the "possible connections between innate immunity, race-specific, and nonhost types of resistance responses." Arabidopsis cell cultures (Landsberg erecta [Ler]) and seedlings (Columbia [Col-0]) were treated with flg22, a 22-amino acid epitope of the flagellin protein, and the major protein component of bacteria flagella.
Transcripts isolated from both systems were used for microarray analysis using high-density oligonucleotide arrays. Expression of 3.0% of transcripts was found to be altered due to the exposure of the cell culture or seedling to flg22. The majority of these Flagellin Rapidly Elicited (FLARE) genes were up-regulated, and 80% encoded proteins of known or predicted function. Not surprisingly, included in the up-regulated genes were those involved in stopping pathogen growth. The FLARE genes were functionally classified as belonging to one of the following groups: signal transduction-related, signal perception-related, effector proteins, or others. Many of the signal transduction-related genes include transcription factors and those involved in regulation of protein turnover. Among the signal transduction-related genes was a R gene to AvrRpt2 (a Pseudomonas syringae Avr protein) along with receptor-like kinases. One surprising result was the inclusion of many auxin signaling-related genes with the down-regulated genes. A recent study by Navarro et al. (2006) Although there was significant overlap in gene expression between the cell culture and the seedlings, some differences were observed. This could potentially arise from the dissimilar concentrations of flg22 used, differential response of the ecotypes, or due to differences between the cell culture and seedling systems. To address these possibilities, cell cultures of Col-0 and Ler were treated with the same concentration of flg22, followed by reverse transcription-PCR on three genes that were up-regulated in the Ler cultures in the previous experiment. Both cell cultures had similar patterns of induction and transcript levels, suggesting the difference was due to experimental system used and not due to ecotype variation.
Among the signal transduction-related genes, many were found to encode transcription factors, including several WRKY transcription factors. The WRKY superfamily of transcription factors is unique to plants and is involved in regulating diverse plant functions, including pathogen defense, senescence, and trichome development (for review, see Eulgem et al., 2000
When tobacco cell cultures are exposed to the Cladosporium fulvum effector protein Avr9, there is a rapid induction of a group of genes called Avr9/Cf-9 rapidly elicited (ACRE; Durrant et al., 2000 The FLARE gene set was compared with genes induced by different pathovars of P. syringae from both the innate and gene-for-gene interaction genes. A modest overlap (12%) between FLARE and nonhost-specific genes was found 3 h postinfection that then increased to 34% after 6 h. Less overlap was observed between "compatible interactions" and FLARE genes. The authors hypothesized that, in this instance, the initial response to flagellin could have been repressed. In Arabidopsis seedlings exposed to the antibiotic cycloheximide prior to flg22 treatment, a majority (70%) of FLARE genes had similar transcription changes. When the seedlings were treated with cycloheximide alone, 82% of FLARE genes were induced. Together, this suggested negative regulation of FLARE genes by rapidly turned-over repressor proteins. A potential model of early signaling events in Arabidopsis bacterial response was suggested by the work from this study. In the model, the detection of bacterial PAMPs in the apoplastic space by receptors such as FLS2 elicit early defense response inducing the expression of FLARE genes, including those potentially involved in the "rapid and transient induction of signaling-related genes." This study indicated that this can be achieved by the degradation of highly turned-over negative regulators since treatment of seedling with cycloheximide induced expression of FLARE genes. To counter this defensive response, bacteria "inject" effector proteins into the host cell via the T3SS. Such effectors include Avr proteins as well as those that potentially interfere with the early defense-signaling pathway. If the plant contains the R proteins corresponding to the bacterial Avr protein, the host gene-for-gene defense pathway is activated. Both of these plant responses to pathogen attack include ion fluxes, production of reactive oxygen species, and activation of MAPKs and CDPKs. Bacterial effector proteins would also target the gene-for-gene defense pathway to "suppress this elicitation."
The activities of bacterial effector proteins are currently being elucidated, and studies in plants have indicated they are able to allow a nonpathogen to overcome some host defense systems as well as possibly function both as suppressors and inducers of plant resistance to the pathogen, as recently shown in tomato (Solanum lycopersicum) and bean (Phaseolus vulgaris; de Torres et al., 2006 ).
The study by de Torres et al. (2006)
What are the proteins involved in early basal resistance? It is known that membrane receptors are involved, but are there soluble factors? The apoplastic fluid of tobacco leaf parenchyma was sampled to isolate such soluble proteins potentially involved in early resistance to pathogens (Ott et al., 2006
As more details of plant immunity become known, the contributions of basal and gene-for-gene-mediated responses to bacterial pathogens are slowly becoming elucidated, and the distinction between them is becoming more vague. Studies such as the one by Navarro et al. (2004) are lending support to the idea of overlap between the two responses. A recent review by Abramovitch et al. (2006) suggests that it might be useful to reclassify the two responses by their timing and location in the plant to "early, extracellular defenses and later, intracellular defenses."
www.plantphysiol.org/cgi/doi/10.1104/pp.106.900207
Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7: 601–611[CrossRef][Web of Science][Medline] Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gómez-Gómez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977–983[CrossRef][Medline] Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973–979[CrossRef][Web of Science][Medline] Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814[CrossRef][Web of Science][Medline] Dangl JL, McDowell JM (2006) Two modes of pathogen recognition by plants. Proc Natl Acad Sci USA 103: 8575–8576 de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, Tsiamis G, Forsyth A, Robatzek S, Grant M, Boch J (2006) Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant J 47: 368–382[CrossRef][Web of Science][Medline] Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDG (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12: 963–977 Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199–206[CrossRef][Web of Science][Medline] Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7: 251–256[CrossRef][Web of Science][Medline] Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496–3507 Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312: 436–439 Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135: 1113–1128 Nurnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266[CrossRef][Web of Science][Medline] Ott PG, Varga GJ, Szatmári Á, Bozsó Z, Klement É, Medzihradszky KF, Besenyei E, Czelleng A, Klement Z (2006) Novel extracellular chitinases rapidly and specifically induced by general bacterial elicitors and suppressed by virulent bacteria as a marker of early basal resistance in tobacco. Mol Plant Microbe Interact 19: 161–172[Web of Science][Medline] Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767[CrossRef][Medline] This article has been cited by other articles:
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