D F Klessig

Cornell University, Ithaca, New York, United States

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Publications (225)1596.27 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Salicylic acid (SA) plays a critical role in plant defense against pathogen invasion. SA-induced viral defense in plants is distinct from the pathways mediating bacterial and fungal defense and involves a specific pathway mediated by mitochondria; however, the underlying mechanisms remain largely unknown.The SA-binding activity of the recombinant tomato (Solanum lycopersicum) alpha-ketoglutarate dehydrogenase (Slα-kGDH) E2 subunit of the tricarboxylic acid (TCA) cycle was characterized. The biological role of this binding in plant defenses against tobacco mosaic virus (TMV) was further investigated via Slα-kGDH E2 silencing and transient overexpression in plants.Slα-kGDH E2 was found to bind SA in two independent assays. SA treatment, as well as Slα-kGDH E2 silencing, increased resistance to TMV. SA did not further enhance TMV defense in Slα-kGDH E2-silenced tomato plants but did reduce TMV susceptibility in Nicotiana benthamiana plants transiently overexpressing Slα-kGDH E2. Furthermore, Slα-kGDH E2-silencing-induced TMV resistance was fully blocked by bongkrekic acid application and alternative oxidase 1a silencing.These results indicated that binding by Slα-kGDH E2 of SA acts upstream of and affects the mitochondrial electron transport chain, which plays an important role in basal defense against TMV. The findings of this study help to elucidate the mechanisms of SA-induced viral defense.
    New Phytologist 11/2014; · 6.74 Impact Factor
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    ABSTRACT: Thimet oligopeptidase (TOP) is a zinc-dependent metallopeptidase. Recent studies suggest that Arabidopsis thaliana TOP1 and TOP2 are targets for salicylic acid (SA) binding and participate in SA-mediated plant innate immunity. The crystal structure of A. thaliana TOP2 has been determined at 3.0 Å resolution. Comparisons to the structure of human TOP revealed good overall structural conservation, especially in the active-site region, despite their weak sequence conservation. The protein sample was incubated with the photo-activated SA analog 4-azido-SA and exposed to UV irradiation before crystallization. However, there was no conclusive evidence for the binding of SA based on the X-ray diffraction data. Further studies are needed to elucidate the molecular mechanism of how SA regulates the activity of A. thaliana TOP1 and TOP2.
    Acta crystallographica. Section F, Structural biology communications. 05/2014; 70(Pt 5):555-9.
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    ABSTRACT: MORC1 and MORC2, two of the seven members of the Arabidopsis thaliana CRT1 (compromised recognition of TCV) subfamily of microrchidia (MORC) GHKL ATPases, were previously shown to be required in multiple layers of plant immunity. Here we show that the Hordeum vulgare MORCs also are involved in disease resistance. Genome-wide analyses identified five MORCs that are 37-48% identical on the protein level to AtMORC1. Unexpectedly, and in clear contrast to Arabidopsis, RNA interference-mediated knock-down (KD) of MORC in barley resulted in enhanced basal resistance and effector-triggered, MLA12-mediated resistance against the biotrophic powdery mildew fungus (Blumeria graminis f.sp. hordei), while MORC overexpression decreased resistance. Moreover, barley KD mutants also showed higher resistance to Fusarium graminearum. Barley MORCs, like their Arabidopsis homologs, contain the highly conserved GHKL ATPase and S5 domains, which identify them as members of the MORC superfamily. Like AtMORC1, barley MORC1 (HvMORC1) binds DNA and has Mn2+-dependent endonuclease activities, suggesting that the contrasting function of MORC1 homologs in barley vs. Arabidopsis is not due to differences in their enzyme activities. In contrast to AtMORCs, which are involved in silencing of transposons that are largely restricted to pericentromeric regions, barley MORC mutants did not show a loss of transposon gene silencing regardless of their genomic location. Reciprocal overexpression of MORC1 homologs in barley and Arabidopsis showed that AtMORC1 and HvMORC1 could not restore each other's function. Together these results suggest that MORC proteins function as modulators of immunity, which can act negatively (barley) or positively (Arabidopsis) dependent on the species.
    Plant physiology 01/2014; · 6.56 Impact Factor
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    ABSTRACT: Plant viruses often encode suppressors of host RNA silencing machinery, which occasionally function as avirulence factors that are recognized by host resistance (R) proteins. For example, the Arabidopsis R protein, hypersensitive response to TCV (HRT), recognizes the turnip crinkle virus (TCV) coat protein (CP). HRT-mediated resistance requires the RNA-silencing component double-stranded RNA-binding protein 4 (DRB4) even though it neither is associated with the accumulation of TCV-specific small RNA nor requires the RNA silencing suppressor function of CP. HRT interacts with the cytosolic fraction of DRB4. Interestingly, TCV infection both increases the cytosolic DRB4 pool and inhibits the HRT-DRB4 interaction. The virulent R8A CP derivative, which induces a subset of HRT-derived responses, also disrupts this interaction. The differential localization of DRB4 in the presence of wild-type and R8A CP implies the importance of subcellular compartmentalization of DRB4. The requirement of DRB4 in resistance to bacterial infection suggests a universal role in R-mediated defense signaling.
    Cell Reports 09/2013; · 7.21 Impact Factor
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    ABSTRACT: Arabidopsis thaliana CRT1 (compromised for recognition of Turnip Crinkle Virus) was previously shown to be required for effector-triggered immunity. Sequence analyses previously revealed that CRT1 contains the ATPase and S5 domains characteristic of Microchidia (MORC) proteins; these proteins are associated with DNA modification and repair. Here we show that CRT1 and its closest homologue, CRH1, are also required for pathogen-associated molecular pattern (PAMP)-triggered immunity, basal resistance, non-host resistance and systemic acquired resistance. Consistent with its role in PAMP-triggered immunity, CRT1 interacted with the PAMP recognition receptor FLS2. Subcellular fractionation and transmission electron microscopy detected a subpopulation of CRT1 in the nucleus, whose levels increased following PAMP treatment or infection with an avirulent pathogen. These results, combined with the demonstration that CRT1 binds DNA, exhibits endonuclease activity, and affects tolerance to the DNA-damaging agent mitomycin C, argue that this prototypic eukaryotic member of the MORC superfamily has important nuclear functions during immune response activation.
    Nature Communications 12/2012; 3:1297. · 10.74 Impact Factor
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    ABSTRACT: Salicylic acid (SA) is a small phenolic molecule that not only is the active ingredient in the multi-functional drug aspirin, but also serves as a plant hormone that affects diverse processes during growth, development, responses to abiotic stresses and disease resistance. Although a number of SA-binding proteins (SABPs) have been identified, the underlying mechanisms of action of SA remain largely unknown. Efforts to identify additional SA targets, and thereby elucidate the complex SA signaling network in plants, have been hindered by the lack of effective approaches. Here, we report two sensitive approaches that utilize SA analogs in conjunction with either a photoaffinity labeling technique or surface plasmon resonance-based technology to identify and evaluate candidate SABPs from Arabidopsis. Using these approaches, multiple proteins, including the E2 subunit of α-ketoglutarate dehydrogenase and the glutathione S-transferases GSTF2, GSTF8, GSTF10 and GSTF11, were identified as SABPs. Their association with SA was further substantiated by the ability of SA to inhibit their enzymatic activity. The photoaffinity labeling and surface plasmon resonance-based approaches appear to be more sensitive than the traditional approach for identifying plant SABPs using size-exclusion chromatography with radiolabeled SA, as these proteins exhibited little to no SA-binding activity in such an assay. The development of these approaches therefore complements conventional techniques and helps dissect the SA signaling network in plants, and may also help elucidate the mechanisms through which SA acts as a multi-functional drug in mammalian systems.
    The Plant Journal 10/2012; · 6.58 Impact Factor
  • D'Maris Amick Dempsey, Daniel F Klessig
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    ABSTRACT: Following pathogen infection, activation of systemic acquired resistance (SAR) in uninfected tissues requires transmission of a signal(s) from the infected tissue via the vasculature. Several candidates for this long-distance signal have been identified, including methyl salicylate (MeSA), an SFD1/GLY1-derived glycerol-3-phosphate (G3P)-dependent signal, the lipid-transfer protein DIR1, the dicarboxylic acid azelaic acid (AzA), the abietane diterpenoid dehydroabietinal (DA), jasmonic acid (JA), and the amino acid-derivative pipecolic acid (Pip). Some of these signals work cooperatively to activate SAR and/or regulate MeSA metabolism. However, Pip appears to activate SAR via an independent pathway that may impinge on these other signaling pathway(s) during de novo salicylic acid (SA) biosynthesis in the systemic tissue. Thus, a complex web of cross-interacting signals appears to activate SAR.
    Trends in Plant Science 06/2012; 17(9):538-45. · 11.81 Impact Factor
  • Magali Moreau, Miaoying Tian, Daniel F Klessig
    Cell Research 06/2012; · 10.53 Impact Factor
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    ABSTRACT: Phytopathogens can manipulate plant hormone signaling to access nutrients and counteract defense responses. Pseudomonas syringae produces coronatine, a toxin that mimics the plant hormone jasmonic acid isoleucine and promotes opening of stomata for bacterial entry, bacterial growth in the apoplast, systemic susceptibility, and disease symptoms. We examined the mechanisms underlying coronatine-mediated virulence and show that coronatine activates three homologous NAC transcription factor (TF) genes, ANAC019, ANAC055, and ANAC072, through direct activity of the TF, MYC2. Genetic characterization of NAC TF mutants demonstrates that these TFs mediate coronatine-induced stomatal reopening and bacterial propagation in both local and systemic tissues by inhibiting the accumulation of the key plant immune signal salicylic acid (SA). These NAC TFs exert this inhibitory effect by repressing ICS1 and activating BSMT1, genes involved in SA biosynthesis and metabolism, respectively. Thus, a signaling cascade by which coronatine confers its multiple virulence activities has been elucidated.
    Cell Host & Microbe 06/2012; 11(6):587-596. · 12.61 Impact Factor
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    ABSTRACT: Phytopathogens can manipulate plant hormone signaling to access nutrients and counteract defense responses. Pseudomonas syringae produces coronatine, a toxin that mimics the plant hormone jasmonic acid isoleucine and promotes opening of stomata for bacterial entry, bacterial growth in the apoplast, systemic susceptibility, and disease symptoms. We examined the mechanisms underlying coronatine-mediated virulence and show that coronatine activates three homologous NAC transcription factor (TF) genes, ANAC019, ANAC055, and ANAC072, through direct activity of the TF, MYC2. Genetic characterization of NAC TF mutants demonstrates that these TFs mediate coronatine-induced stomatal reopening and bacterial propagation in both local and systemic tissues by inhibiting the accumulation of the key plant immune signal salicylic acid (SA). These NAC TFs exert this inhibitory effect by repressing ICS1 and activating BSMT1, genes involved in SA biosynthesis and metabolism, respectively. Thus, a signaling cascade by which coronatine confers its multiple virulence activities has been elucidated.
    Cell host & microbe 06/2012; 11(6):587-96. · 13.02 Impact Factor
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    ABSTRACT: Plant defense responses to pathogens are influenced by abiotic factors, including temperature. Elevated temperatures often inhibit the activities of disease resistance proteins and the defense responses they mediate. A mutant screen with an Arabidopsis thaliana temperature-sensitive autoimmune mutant bonzai1 revealed that the abscisic acid (ABA)-deficient mutant aba2 enhances resistance mediated by the resistance (R) gene suppressor of npr1-1 constitutive1 (SNC1) at high temperature. ABA deficiency promoted nuclear accumulation of SNC1, which was essential for it to function at low and high temperatures. Furthermore, the effect of ABA deficiency on SNC1 protein accumulation is independent of salicylic acid, whose effects are often antagonized by ABA. ABA deficiency also promotes the activity and nuclear localization of R protein resistance to Pseudomonas syringae4 at higher temperature, suggesting that the effect of ABA on R protein localization and nuclear activity is rather broad. By contrast, mutations that confer ABA insensitivity did not promote defense responses at high temperature, suggesting either tissue specificity of ABA signaling or a role of ABA in defense regulation independent of the core ABA signaling machinery. Taken together, this study reveals a new intersection between ABA and disease resistance through R protein localization and provides further evidence of antagonism between abiotic and biotic responses.
    The Plant Cell 03/2012; 24(3):1271-84. · 9.25 Impact Factor
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    Po-Pu Liu, Caroline C von Dahl, Daniel F Klessig
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    ABSTRACT: Systemic acquired resistance (SAR) is a state of heightened defense to a broad spectrum of pathogens that is activated throughout a plant following local infection. Development of SAR requires the translocation of one or more mobile signals from the site of infection through the vascular system to distal (systemic) tissues. The first such signal identified was methyl salicylate (MeSA) in tobacco (Nicotiana tabacum). Subsequent studies demonstrated that MeSA also serves as a SAR signal in Arabidopsis (Arabidopsis thaliana) and potato (Solanum tuberosum). By contrast, another study suggested that MeSA is not required for SAR in Arabidopsis and raised questions regarding its signaling role in tobacco. Differences in experimental design, including the developmental age of the plants, the light intensity, and/or the strain of bacterial pathogen, were proposed to explain these conflicting results. Here, we demonstrate that the length of light exposure that plants receive after the primary infection determines the extent to which MeSA is required for SAR signaling. When the primary infection occurred late in the day and as a result infected plants received very little light exposure before entering the night/dark period, MeSA and its metabolizing enzymes were essential for SAR development. In contrast, when infection was done in the morning followed by 3.5 h or more of exposure to light, SAR developed in the absence of MeSA. However, MeSA was generally required for optimal SAR development. In addition to resolving the conflicting results concerning MeSA and SAR, this study underscores the importance of environmental factors on the plant's response to infection.
    Plant physiology 12/2011; 157(4):2216-26. · 6.56 Impact Factor
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    Plant physiology 02/2011; 155(4):1762-8. · 6.56 Impact Factor
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    ABSTRACT: Salicylic acid (SA) has been shown to regulate various aspects of growth and development; it also serves as a critical signal for activating disease resistance in Arabidopsis thaliana and other plant species. This review surveys the mechanisms involved in the biosynthesis and metabolism of this critical plant hormone. While a complete biosynthetic route has yet to be established, stressed Arabidopsis appear to synthesize SA primarily via an isochorismate-utilizing pathway in the chloroplast. A distinct pathway utilizing phenylalanine as the substrate also may contribute to SA accumulation, although to a much lesser extent. Once synthesized, free SA levels can be regulated by a variety of chemical modifications. Many of these modifications inactivate SA; however, some confer novel properties that may aid in long distance SA transport or the activation of stress responses complementary to those induced by free SA. In addition, a number of factors that directly or indirectly regulate the expression of SA biosynthetic genes or that influence the rate of SA catabolism have been identified. An integrated model, encompassing current knowledge of SA metabolism in Arabidopsis, as well as the influence other plant hormones exert on SA metabolism, is presented.
    The Arabidopsis Book 01/2011; 9:e0156.
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    ABSTRACT: Whether salicylic acid (SA) plays a role in systemic acquired resistance (SAR) signaling in potato is currently unclear because potato, unlike tobacco and Arabidopsis, contains highly elevated levels of endogenous SA. Recent studies have indicated that the SA derivative methyl salicylate (MeSA) serves as a long-distance phloem-mobile SAR signal in tobacco and Arabidopsis. Once in the distal, uninfected tissue of these plant species, MeSA must be converted into biologically active SA by the esterase activity of SA-binding protein 2 (SABP2) in tobacco or members of the AtMES family in Arabidopsis. In this study, we have identified the potato ortholog of tobacco SABP2 (StMES1) and shown that the recombinant protein converts MeSA to SA; this MeSA esterase activity is feedback inhibited by SA or its synthetic analog, 2, 2, 2, 2'-tetra-fluoroacetophenone (tetraFA). Potato plants (cv. Désirée) in which StMES1 activity was suppressed, due to either tetraFA treatment or silencing of StMES1 expression, were compromised for arachidonic acid (AA)-induced SAR development against Phytophthora infestans. Presumably due to the inability of these plants to convert MeSA to SA, the SAR-defective phenotype correlated with elevated levels of MeSA and reduced expression of pathogenesis-related (PR) genes in the untreated distal tissue. Together, these results strongly suggest that SAR signaling in potato requires StMES1, its corresponding MeSA esterase activity, and MeSA. Furthermore, the similarities between SAR signaling in potato, tobacco, and Arabidopsis suggest that at least certain SAR signaling components are conserved among plants, regardless of endogenous SA levels.
    Molecular Plant-Microbe Interactions 09/2010; 23(9):1151-63. · 4.31 Impact Factor
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    ABSTRACT: Light harvested by plants is essential for the survival of most life forms. This light perception ability requires the activities of proteins termed photoreceptors. We report a function for photoreceptors in mediating resistance (R) protein-derived plant defense. The blue-light photoreceptors, cryptochrome (CRY) 2 and phototropin (PHOT) 2, are required for the stability of the R protein HRT, and thereby resistance to Turnip Crinkle virus (TCV). Exposure to darkness or blue-light induces degradation of CRY2, and in turn HRT, resulting in susceptibility. Overexpression of HRT can compensate for the absence of PHOT2 but not CRY2. HRT does not directly associate with either CRY2 or PHOT2 but does bind the CRY2-/PHOT2-interacting E3 ubiquitin ligase, COP1. Application of the proteasome inhibitor, MG132, prevents blue-light-dependent degradation of HRT, consequently these plants show resistance to TCV under blue-light. We propose that CRY2/PHOT2 negatively regulate the proteasome-mediated degradation of HRT, likely via COP1, and blue-light relieves this repression resulting in HRT degradation.
    Proceedings of the National Academy of Sciences 07/2010; 107(30):13538-43. · 9.81 Impact Factor
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    ABSTRACT: Resistance gene-mediated immunity confers protection against pathogen infection in a wide range of plants. A genetic screen for Arabidopsis thaliana mutants compromised for recognition of turnip crinkle virus previously identified CRT1, a member of the GHKL ATPase/kinase superfamily. Here, we demonstrate that CRT1 interacts with various resistance proteins from different structural classes, and this interaction is disrupted when these resistance proteins are activated. The Arabidopsis mutant crt1-2 crh1-1, which lacks CRT1 and its closest homolog, displayed compromised resistance to avirulent Pseudomonas syringae and Hyaloperonospora arabidopsidis. Additionally, resistance-associated hypersensitive cell death was suppressed in Nicotiana benthamiana silenced for expression of CRT1 homolog(s). Thus, CRT1 appears to be a general factor for resistance gene-mediated immunity. Since elevation of cytosolic calcium triggered by avirulent P. syringae was compromised in crt1-2 crh1-1 plants, but cell death triggered by Nt MEK2(DD) was unaffected in CRT1-silenced N. benthamiana, CRT1 likely functions at an early step in this pathway. Genome-wide transcriptome analysis led to identification of CRT1-Associated genes, many of which are associated with transport processes, responses to (a)biotic stress, and the endomembrane system. Confocal microscopy and subcellular fractionation revealed that CRT1 localizes to endosome-like vesicles, suggesting a key process in resistance protein activation/signaling occurs in this subcellular compartment.
    The Plant Cell 03/2010; 22(3):918-36. · 9.25 Impact Factor
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    ABSTRACT: A number of Arabidopsis (Arabidopsis thaliana) lesion-mimic mutants exhibit alterations in both abiotic stress responses and pathogen resistance. One of these mutants, constitutive expresser of PR genes22 (cpr22), which has a mutation in two cyclic nucleotide-gated ion channels, is a typical lesion-mimic mutant exhibiting elevated levels of salicylic acid (SA), spontaneous cell death, constitutive expression of defense-related genes, and enhanced resistance to various pathogens; the majority of its phenotypes are SA dependent. These defense responses in cpr22 are suppressed under high-humidity conditions and enhanced by low humidity. After shifting plants from high to low humidity, the cpr22 mutant, but not the wild type, showed a rapid increase in SA levels followed by an increase in abscisic acid (ABA) levels. Concomitantly, genes for ABA metabolism were up-regulated in the mutant. The expression of a subset of ABA-inducible genes, such as RD29A and KIN1/2, was down-regulated, but that of other genes, like ABI1 and HAB1, was up-regulated in cpr22 after the humidity shift. cpr22 showed reduced responsiveness to ABA not only in abiotic stress responses but also in germination and stomatal closure. Double mutant analysis with nahG plants that degrade SA indicated that these alterations in ABA signaling were attributable to elevated SA levels. Furthermore, cpr22 displayed suppressed drought responses by long-term drought stress. Taken together, these results suggest an effect of SA on ABA signaling/abiotic stress responses during the activation of defense responses in cpr22.
    Plant physiology 02/2010; 152(4):1901-13. · 6.56 Impact Factor
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    ABSTRACT: On infection by pathogens, plants initiate defence responses that are able to curtail infection locally. These responses are mediated either by receptor-like proteins that recognize pathogen-associated molecular patterns or by the protein products of disease resistance (R) genes. At the same time, primary defence responses often result in the generation of signals that induce what is known as systemic acquired resistance (SAR), such that defence responses are enhanced on secondary pathogen challenge in distal tissues. R protein-mediated SAR induction is normally accompanied by a type of programmed cell death known as the hypersensitive response (HR) and, in some instances, cell death alone has been implicated in the induction of SAR. This has raised the question of whether R protein-mediated signalling per se induces SAR or whether SAR is an indirect result of the induction of HR. Using the Rx gene of potato, which confers resistance to Potato Virus X in the absence of cell death, we have shown that the HR is dispensable for R protein-mediated induction of SAR and that Rx-induced SAR is mediated by the same salicylate-dependent pathway induced by other R proteins.
    Molecular Plant Pathology 01/2010; 11(1):155-60. · 4.49 Impact Factor
  • Po-Pu Liu, Yue Yang, Eran Pichersky, Daniel F Klessig
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    ABSTRACT: Methyl salicylate (MeSA), which is synthesized in plants from salicylic acid (SA) by methyltransferases, has roles in defense against microbial and insect pests. Most of the MeSA that accumulates after pathogen attack is synthesized by benzoic acid/SA carboxyl methyltransferase 1 (AtBSMT1). To investigate the role of AtBSMT1 in plant defense, transgenic Arabidopsis with altered AtBSMT1 function or expression were assessed for their ability to resist pathogen infection. A knockout mutant (Atbsmt1) failed to accumulate MeSA following pathogen infection; these plants also failed to accumulate SA or its glucoside in the uninoculated leaves and did not develop systemic acquired resistance (SAR). However, the Atbsmt1 mutant exhibited normal levels of effector-triggered immunity and pathogen-associated molecular pattern (PAMP)-triggered immunity to Pseudomonas syringae and Hyaloperonospora arabidopsidis. Analyses of transgenic Arabidopsis plants overexpressing AtBSMT1 revealed that they accumulate elevated levels of MeSA in pathogen-infected leaves but fail to develop SAR. Since the levels of SA and its glucoside were reduced in uninoculated systemic leaves of these plants whereas MeSA levels were elevated, AtBSMT1-mediated conversion of SA to MeSA probably compromised SAR development by suppressing SA accumulation in uninoculated leaves. PAMP-triggered immunity also was compromised in the AtBSMT1 overexpressing plants, although effector-triggered immunity was not.
    Molecular Plant-Microbe Interactions 01/2010; 23(1):82-90. · 4.31 Impact Factor

Publication Stats

18k Citations
1,596.27 Total Impact Points

Institutions

  • 2003–2013
    • Cornell University
      • Department of Plant Biology
      Ithaca, New York, United States
    • University of Kentucky
      • Department of Plant Pathology
      Lexington, KY, United States
  • 2012
    • Texas State University
      San Marcos, Texas, United States
  • 2001–2012
    • Thompson Institute
      Ithaca, New York, United States
  • 1995–2012
    • Duke University
      • Department of Biology
      Durham, NC, United States
  • 2009
    • Max Planck Institute for Plant Breeding Research
      Köln, North Rhine-Westphalia, Germany
  • 2008
    • East Tennessee State University
      Johnson City, Tennessee, United States
    • Yale University
      New Haven, Connecticut, United States
  • 2007
    • Syracuse University
      • Department of Biology
      Syracuse, NY, United States
  • 2005–2007
    • Columbia University
      • Department of Biological Sciences
      New York City, NY, United States
  • 2004
    • Colgate University
      Hamilton, New York, United States
  • 1988–2002
    • Rutgers, The State University of New Jersey
      • Department of Molecular Biology and Biochemistry
      New Brunswick, New Jersey, United States
  • 2000–2001
    • University of Missouri
      • Department of Biochemistry
      Columbia, MO, United States
  • 1998
    • State University of New York
      New York City, New York, United States
    • University of California, Riverside
      Riverside, California, United States
  • 1997
    • Massachusetts General Hospital
      Boston, Massachusetts, United States
  • 1982–1986
    • University of Utah
      • School of Medicine
      Salt Lake City, UT, United States
  • 1979–1980
    • Cold Spring Harbor Laboratory
      Cold Spring Harbor, New York, United States