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This paper shows that virulent and non-host Pseudomonas-Arabidopsis interactions trigger a SAR response accompanied by systemic induction of SA and defense gene expression. As these responses were compromised in known SAR mutants, the authors concluded that the non HR-inducing bacteria induced true SAR. Localized application of PAMPs, including flg22, triggered very limited local and systemic induction of SA and defense gene expression, but nonetheless induced a state of significantly heightened resistance to virulent P. syringae in the systemic tissue.
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Mishina T.E., and Zeier J. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J 50 (2007) 500-513. This paper shows that virulent and non-host Pseudomonas-Arabidopsis interactions trigger a SAR response accompanied by systemic induction of SA and defense gene expression. As these responses were compromised in known SAR mutants, the authors concluded that the non HR-inducing bacteria induced true SAR. Localized application of PAMPs, including flg22, triggered very limited local and systemic induction of SA and defense gene expression, but nonetheless induced a state of significantly heightened resistance to virulent P. syringae in the systemic tissue.
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Data in this paper show that the development of both a visible HR and SAR correlates with the length of time that plants receive light immediately following infection of Arabidopsis with avirulent P. syringae. End-of-day inoculations resulted in delayed PR-1 induction and compromised SA accumulation in inoculated leaves as compared to start-of-day inoculations. The photoreceptor mutants cry1cry2, phot1phot2, and phyAphyB all displayed normal local defense responses, although SA accumulation and defense against virulent P. syringae might be partially compromised in the phyAphyB mutant. Contrary to wt-like SAR in cry1cry2 and phot1phot2 plants, SAR was completely abolished in the phyAphyB mutant.
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Griebel T., and Zeier J. Light regulation and daytime dependency of inducible plant defences in Arabidopsis: phytochrome signalling controls systemic acquired resistance rather than local defence. Plant Physiol 50 (2008) 500-513. Data in this paper show that the development of both a visible HR and SAR correlates with the length of time that plants receive light immediately following infection of Arabidopsis with avirulent P. syringae. End-of-day inoculations resulted in delayed PR-1 induction and compromised SA accumulation in inoculated leaves as compared to start-of-day inoculations. The photoreceptor mutants cry1cry2, phot1phot2, and phyAphyB all displayed normal local defense responses, although SA accumulation and defense against virulent P. syringae might be partially compromised in the phyAphyB mutant. Contrary to wt-like SAR in cry1cry2 and phot1phot2 plants, SAR was completely abolished in the phyAphyB mutant.
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Grafting experiments showed that the tobacco MeSA esterase SABP2 is required in the signal-perceiving/processing tissue, but not in the signal-generating tissue, to trigger SAR. The SAR-deficient phenotype of SABP2-silenced graft scions was complemented by expression of SABP2, but only if it was capable of converting MeSA to SA. Feedback inhibition of the MeSA esterase activity of SABP2 [8] in the signal-generating tissue is of biological significance as expression of a form of SABP2 with uninhibitable MeSA esterase activity in the graft rootstock abolished SAR. Silencing of the gene encoding a SA methyl transferase, SAMT1, similarly abolished SAR signal generation in graft rootstocks. Increases in MeSA levels in TMV-inoculated and systemic tissues, as well as in petiole (phloem) exudates of infected leaves, paralleled the development of SAR.
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Park S.-W., Kaimoyo E., Kumar D., Mosher S., and Klessig D.F. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318 (2007) 113-116. Grafting experiments showed that the tobacco MeSA esterase SABP2 is required in the signal-perceiving/processing tissue, but not in the signal-generating tissue, to trigger SAR. The SAR-deficient phenotype of SABP2-silenced graft scions was complemented by expression of SABP2, but only if it was capable of converting MeSA to SA. Feedback inhibition of the MeSA esterase activity of SABP2 [8] in the signal-generating tissue is of biological significance as expression of a form of SABP2 with uninhibitable MeSA esterase activity in the graft rootstock abolished SAR. Silencing of the gene encoding a SA methyl transferase, SAMT1, similarly abolished SAR signal generation in graft rootstocks. Increases in MeSA levels in TMV-inoculated and systemic tissues, as well as in petiole (phloem) exudates of infected leaves, paralleled the development of SAR.
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A rice carboxyl methyl transferase for SA and benzoic acid, OsBSMT1, was expressed in Arabidopsis. Since the transgenic plants accumulated elevated levels of MeSA and methyl benzoate, particularly in response to pathogen infection, but did not mount a significant defense response to pathogen infection or when treated with SA, the data confirm earlier findings that MeSA is not biologically active in defense [10]. Expression of PR-1 was induced in both wild type plants and in SA-deficient sid2-2 mutants when they were maintained in a container with OsBSMT1-over expressing plants that were treated with SA. Together, the data strengthen earlier findings that MeSA can act as an airborne, plant-to-plant defense signal that is converted to SA in the signal-perceiving plant [11].
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Koo Y.J., Kim M.A., Kim E.H., Song J.T., Jung C., Moon J.-K., Kim J.-H., Seo H.S., Song S.I., Kim J.-K., et al. Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64 (2007) 1-15. A rice carboxyl methyl transferase for SA and benzoic acid, OsBSMT1, was expressed in Arabidopsis. Since the transgenic plants accumulated elevated levels of MeSA and methyl benzoate, particularly in response to pathogen infection, but did not mount a significant defense response to pathogen infection or when treated with SA, the data confirm earlier findings that MeSA is not biologically active in defense [10]. Expression of PR-1 was induced in both wild type plants and in SA-deficient sid2-2 mutants when they were maintained in a container with OsBSMT1-over expressing plants that were treated with SA. Together, the data strengthen earlier findings that MeSA can act as an airborne, plant-to-plant defense signal that is converted to SA in the signal-perceiving plant [11].
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In addition to a mutation in the previously published SFD1 gene (SUPPRESSOR OF FATTY ACID DESATURASE 1) [14], mutations in three other genes involved in chloroplast galactolipid metabolism, FAD7 (FATTY ACID DESATURASE 7), MGD1 (MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE 1), and SFD2, abolished SAR without affecting basal resistance or the accumulation of SA in leaves infected with avirulent P. syringae. Petiole exudates from leaves of sfd1 or fad7 Arabidopsis infected with avirulent P. syringae failed to induce defense gene expression or pathogen resistance in Arabidopsis, tomato, and/or wheat, unlike those from comparable wild type plants. As defense signaling was restored by combining these petiole exudates with similar exudates from dir1 mutant plants, which lack a functional form of the lipid-transfer protein DIR1 and also do not generate or transmit the SAR signal
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Chaturvedi R., Krothapalli K., Makandar R., Nandi A., Sparks A.A., Roth M.R., Welti R., and Shah J. Plastid ω3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54 (2008) 106-117. In addition to a mutation in the previously published SFD1 gene (SUPPRESSOR OF FATTY ACID DESATURASE 1) [14], mutations in three other genes involved in chloroplast galactolipid metabolism, FAD7 (FATTY ACID DESATURASE 7), MGD1 (MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE 1), and SFD2, abolished SAR without affecting basal resistance or the accumulation of SA in leaves infected with avirulent P. syringae. Petiole exudates from leaves of sfd1 or fad7 Arabidopsis infected with avirulent P. syringae failed to induce defense gene expression or pathogen resistance in Arabidopsis, tomato, and/or wheat, unlike those from comparable wild type plants. As defense signaling was restored by combining these petiole exudates with similar exudates from dir1 mutant plants, which lack a functional form of the lipid-transfer protein DIR1 and also do not generate or transmit the SAR signal [12], it was concluded that a glycerolipid-derived factor and DIR1 may interact or act in parallel to trigger SAR. The glycerolipid-derived factor did not co-elute with JA from a gel filtration column, and JA did not restore the defense signaling potential of petiole exudates from infected sfd1 or fad7 mutant plants, indicating that the glycerolipid-derived SAR signal is not JA.
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A previously identified early PAMP-induced gene was transiently induced in systemic Arabidopsis tissues, peaking at around four hours after a localized infection of the plant with avirulent P. syringae. This observation was followed up with micro array analyses of systemic tissue of SAR-induced plants at four hours after infection. Genes of the phenylpropanoid pathway were strongly induced, and the authors suggested that phenolic compound-related defenses were primed. However, most of the systemically upregulated genes had roles in JA biosynthesis or had previously been characterized as JA responsive. JA was found in petiole exudates of infected leaves, and the JA biosynthetic mutant opr3 and the JA-insensitive mutant jin1 were SAR deficient. JA may therefore function as an early mobile signal triggering SAR, and the authors hypothesized that JA and SA might both affect SAR in a temporally or spatially separated manner.
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Truman W., Bennett M.H., Kubigsteltig I., Turnbull C., and Grant M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci U S A 104 (2007) 1075-1080. A previously identified early PAMP-induced gene was transiently induced in systemic Arabidopsis tissues, peaking at around four hours after a localized infection of the plant with avirulent P. syringae. This observation was followed up with micro array analyses of systemic tissue of SAR-induced plants at four hours after infection. Genes of the phenylpropanoid pathway were strongly induced, and the authors suggested that phenolic compound-related defenses were primed. However, most of the systemically upregulated genes had roles in JA biosynthesis or had previously been characterized as JA responsive. JA was found in petiole exudates of infected leaves, and the JA biosynthetic mutant opr3 and the JA-insensitive mutant jin1 were SAR deficient. JA may therefore function as an early mobile signal triggering SAR, and the authors hypothesized that JA and SA might both affect SAR in a temporally or spatially separated manner.
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2, JA-dependent defense gene expression, and expression of the gene encoding its own precursor, PROPEP1. PROPEP1 was also induced by MeJA, indicating the existence of a positive feedback loop. Together with five homologues, PROPEP1 makes up a small gene family, with PROPEP2 and 3 being strongly activated by pathogens which are capable of inducing SAR. Over expression of PROPEP1 in Arabidopsis induced resistance to the soil-borne fungal pathogen Pythium irregulare.
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2, JA-dependent defense gene expression, and expression of the gene encoding its own precursor, PROPEP1. PROPEP1 was also induced by MeJA, indicating the existence of a positive feedback loop. Together with five homologues, PROPEP1 makes up a small gene family, with PROPEP2 and 3 being strongly activated by pathogens which are capable of inducing SAR. Over expression of PROPEP1 in Arabidopsis induced resistance to the soil-borne fungal pathogen Pythium irregulare.
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•] was also seen here as AtPep1 and 2 strongly induced expression of the JA-responsive PDF1.2 gene, and AtPep1, 2, 3, 5, and 6 strongly activated expression of the SA-responsive PR-1 gene. Since PAMPs, such as flg22, induce PROPEP2 and 3, the authors proposed that the PROPEP gene family is involved in defense signaling by establishing a positive feedback loop.
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•] was also seen here as AtPep1 and 2 strongly induced expression of the JA-responsive PDF1.2 gene, and AtPep1, 2, 3, 5, and 6 strongly activated expression of the SA-responsive PR-1 gene. Since PAMPs, such as flg22, induce PROPEP2 and 3, the authors proposed that the PROPEP gene family is involved in defense signaling by establishing a positive feedback loop.
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Zhang X., Dai Y., Xiong Y., DeFraia C., Li J., Dong X., and Mou Z. Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J 52 (2007) 1066-1079. Arabidopsis over expressing MKK7 displayed constitutive accumulation of SA and SA-related defense gene transcripts, as well as enhanced resistance to pathogens. These phenotypes depended on the kinase activity of MKK7 as they did not occur in plants over expressing a kinase-inactive mutant. Analysis of MKK7::GUS reporter lines showed that MKK7 is expressed exclusively in the veins of leaves that have been infected with avirulent P. syringae. Interestingly, conditional expression of MKK7 from a dexamethasone-inducible transgene triggered defense gene expression and pathogen resistance in systemic non-MKK7 expressing tissues. Together, the data strongly argue that the MKK7 kinase is involved in SAR signal generation and/or transmission.
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Micro array analyses showed that the SA analog BTH induces several auxin-conjugating enzymes and represses a large group of auxin-response genes, most of which are also repressed in systemic tissues of SAR-induced plants. These transcriptional changes were not paralleled by changes in auxin levels. The morphological phenotypes of an auxin over producing mutant were compromised by introducing mutations which cause constitutive SA signaling, although auxin levels remained high. Reporter gene studies confirmed that SA antagonizes auxin signaling (rather than its metabolism) via SA-dependent stabilization of auxin repressor proteins. By contrast, application of an auxin enhanced susceptibility of Arabidopsis to pathogens whereas an auxin-insensitive mutant displayed enhanced resistance to P. syringae. Since insensitivity to auxin partially rescued the hypersusceptible phenotype of Arabidopsis expressing the SA-degrading enzyme encoded by NahG
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Zhang Z., Li Q., Li Z., Staswick P.E., Wang M., Zhu Y., and He Z. Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145 (2007) 450-464. GH3.5 can conjugate auxin and SA [51], and over expression of GH3.5 resulted in elevated auxin and SA levels after pathogen infection of Arabidopsis. In spite of enhanced SA levels, R gene-mediated resistance was compromised in the GH3.5 over expressor. A comparison of this disease resistance phenotype with that of Arabidopsis over expressing the closest homolog of GH3.5, GH3.6, which can only conjugate auxin and not SA, argued that elevated auxin levels likely antagonized SA signaling, which resulted in increased susceptibility. Basal and R gene-mediated resistance were not affected in the gh3.5 knock out mutant, but SAR was slightly compromised, which was accompanied by reduced systemic induction of PR-1. GH3.5 expression was induced by pathogens and SA, and transcript profiling of the GH3.5 over expressor revealed that GH3.5 might enhance IAA biosynthesis and activate auxin signaling. Expression of SA-dependent and other defense genes was also higher in the over expressor than in wild type plants, particularly after pathogen infection.
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This paper directly compares the effects of low and high concentrations of the defense-inducing compounds β-aminobutyric acid (BABA) and the SA analog BTH on pathogen resistance and plant growth/yield. Low concentrations of the compounds induced SAR-like priming of defense pathways that were activated faster and/or stronger than in non-treated plants upon pathogen infection. Higher concentrations of the compounds constitutively activated defense. The data show that defense through priming is equally effective as constitutively activated defense. However, contrary to constitutive activation of defense, priming did not cause significant plant growth retardation or loss of seed production. As plant growth and seed production were not affected in npr1 mutant plants after pathogen infection or treatment with high concentrations of BABA or BTH, it was concluded that the 'costs' of infection/constitutive defense were owing to NPR1-dependent defense responses.
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