Phone: (office) 607-254-4560;  (lab) 607-254-1255
Cornell affiliation: Adjunct Professor, Section of Plant Pathology & Plant-Microbe Biology, School of Integrative Plant Science, Cornell University
Graduate fields: Plant Biology; Plant Pathology & Plant-Microbe Biology
Our research is focused on understanding, at the biochemical, molecular and cellular levels, how plants protect themselves against microbial pathogens. The major goal is to determine the mechanisms of action of salicylic acid (SA) in activation and regulation of the plant’s immune responses. We also are now employing the technology developed and knowledge gained from our work on SA and plant immunity to identify the targets of aspirin (acetyl SA) and its major metabolite SA in humans. The molecular/biochemical function of CRT1/MORC1 in multiple levels of plant immunity is also being deciphered. In addition, in collaboration with Frank Schroeder the induction of plant immune responses by nematode ascarosides is being investigated.
A. Systemic acquired resistance (SAR) in Arabidopsis, tobacco, and potato
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 translocation of one or more mobile signals from the site of infection through the vascular system to distal (systemic) tissues. Between 2007 and 2011 we reported the identification of the first long-distance mobile signal, methyl salicylate, in several plant species in a series of five papers. In 2011 we published the inter-relationship between methyl salicylate and lipid signal(s). More recently several other mobile signals have been reported in addition to methyl salicylate and a DIR1/GLY1-dependent lipid signal. These include the dicarboxylic acid azelaic acid, the abietane diterpenoid dehydroabietinal, jasmonic acid, and the amino acid-derivative pipecolic acid. Our 2012 mini-review (Dempsey and Klessig) entitled “SOS – too many signals for systemic acquired resistance?” attempts to make sense of these newly discovered mobile signals.
B. Identification and characterization of new SA-binding proteins (SABPs).
In addition to disease resistance, SA affects many other plant processes, including flowering, seed germination, adventitious root initiation, and thermogenesis. In order to identify new SABPs through which SA exerts its many effects, we developed during the past several years two high throughput screens to identify candidate SABPS (cSABPs). The first utilizes SA analogs 4-azido SA (4AzSA) or 3-aminoethyl SA (3AESA), in conjunction with either a photoaffinity labeling technique or surface plasmon resonance (SPR)-based technology, to identify and evaluate cSABPs from Arabidopsis. The photoaffinity labeling and SPR-based approaches appear to be more sensitive than the traditional approach for identifying plant SA-binding activity using size exclusion chromatography with radiolabeled SA, as these proteins exhibited little to no SA-binding activity in such an assay. These novel approaches therefore complement conventional techniques and has help dissect the SA signaling network in plants. Our first results were reported in 2012 (Tian et al., Plant J 72:1027, 2012).
The second high throughput screen utilizes a protein microarray (PMA) to identify proteins that bind SA analogs. The initial screen, which used a 5,000 PMA (developed by S. Popescu, S. Dinesh-Kumar and M. Snyder) in conjunction with photoaffinity crosslinking to 4AzSA, yielded several dozen cSABPs, most of these were false positives. After further optimization we screened a new 10,000 PMA. Bioinformatic analysis indicated that the results were much more reproducible from microarray to microarray than in the previous screen. Using a stringent cutoff of P < 0.01, 41 cSABPs were identified. A subset of these, together with a subset from the 4AzSA crosslinking – immuno-selection screen were further characterized. The results were reported in Manohar et al., 2015, which revealed the identity of nine new SA-binding proteins (SABPs) and summarized the results from our two new, powerful screens for SABPs, which led to the discovery of a total of 23 new SABPs.
Several members of the Arabidopsis GAPDH family, including two chloroplast-localized and two cytosolic isoforms, were identified as SABPs. Since cytosolic GAPDH is an important host factor involved in Tomato Bushy Stunt Virus (TBSV) replication, the effects of SA on its replication were evaluated in collaboration with Peter Nagy using three different replication system. SA inhibited TBSV replication by disrupting the binding of cytosolic GAPDH to the negative (-) RNA strand of TBSV. Thus, this study reveals a novel mechanism through which SA mediates resistance by targeting host factors used for virus replication (Tian et al., 2015).
Our results indicate that, as in humans, Arabidopsis HMGB3 functions as a Damage-Associated Molecular Pattern (DAMP), and that SA modulates this function. We discovered that extracellular HMGB3 induced a series of innate immune responses, including i) MAPK activation, ii) enhanced defense-related gene expression, iii) callose deposition, and iv) enhanced resistance to Botrytis cinerea, that are activated via a pathway that is depended on the receptor-like kinases BAK1 and BKK1. Further supporting its role as a DAMP, HMGB3 was released into the apoplast following B. cinerea infection. In addition, silencing multiple HMGB genes in transgenic plants reduced resistance to B. cinerea. HMGB3 exhibited authentic SA-binding activity in vitro, and its ability to activate MAPKs, induce callose deposition, and enhance resistance was inhibited by SA in vivo. These findings are consistent with our recent discovery that SA binds human HMGB1 (HsHMGB1), thereby inhibiting its pro-inflammatory activities (see below – Choi et al., 2015). Sequence alignment revealed that SA-binding sites in HsHMGB1 are conserved in the HMG box domain of Arabidopsis HMGB proteins. An SA-binding site mutant of HMGB3 retained its DAMP activity, but this activity was no longer inhibited by SA, consistent with its reduced ability to bind SA. Together these results provide cross-kingdom evidence that HMGB proteins function as DAMPs and that SA is their conserved inhibitor.
C. Human SAPBs
During the past three years, more of our focus has been on identifying and characterizing novel targets of SA, the active ingredient of aspirin that mediates aspirin’s multiple pharmacological effects, such as reduction in fever, pain, and inflammation, as well as the risk of stroke, heart attack, and cancer. We have discovered that SA binds to human High Mobility Group Box 1 (HMGB1) and Glyceraldehyde 3-Phosphate Dehydrogenase (GAPDH) and alters their activities.
We demonstrated that HMGB1 is a novel SA-binding protein using affinity chromatography, 4AzSA crosslinking, SPR, and NMR. SA-binding sites on HMGB1 were identified in the HMG-box domains by NMR and confirmed by mutational analysis. Extracellular HMGB1 is a DAMP, with multiple redox states. SA suppresses both the chemo-attractant activity of fully reduced HMGB1 and the increased expression of pro-inflammatory cytokine genes and COX-2 gene induced by disulfide HMGB1. Natural and synthetic SA derivatives with stronger binding affinity for HMGB1 than SA and greater potency for inhibition of HMGB1 were identified, providing proof-of-concept that new SA-based molecules with high efficacy against inflammation are attainable. An HMGB1 protein mutated in one of the SA-binding sites identified by NMR chemical shift perturbation studies retained chemo-attractant activity, but lost binding of and inhibition by SA and its derivatives, thereby firmly establishing that SA binding to HMGB1 directly suppresses its pro-inflammatory activities. Identification of HMGB1 as a pharmacological target of SA/aspirin provides new insights into the mechanisms of action of one of the world’s longest and most used natural and synthetic drugs (Choi et al., 2015). We are trying to extend this work to animal model systems for various diseases including arthritis, cancer, and Alzheimer’s disease with collaborators. In addition, HMGB1 and GAPDH are being used to identify new, more potent SA derivatives – either synthetic or from medicinal plants. For more information, see the interview in MedicalResearch.com.
In addition to its central role in glycolysis, GAPDH is a major participant in disease. GAPDH is a prime suspect in several neurodegenerative disorders, including Alzheimer’s, Parkinson’s, and Huntington’s diseases. In collaboration with Sol Snyder at Johns Hopkins, we found that SA and its more potent derivatives suppress nuclear translocation of GAPDH, induced by oxidative stress-like conditions, and the resulting cell death, just like the anti-Parkinson’s disease drug deprenyl (Choi et al., 2015). For additional information, see the interview in MedicalResearch.com.
D. CRT1/MORC1 characterization
Over the past several years we have characterized CRT1/MORC1 (Microrchidia) family, a subset of the GHKL ATPase superfamily, and discovered that it interacts with multiple immune receptors (R proteins and PAMP Recognition Receptors) and functions in multiple layers of plant immunity in Arabidopsis. CRT1/MORC1 localizes to endosomal-like vesicles but a small subpopulation translocates to the nucleus upon activation of immune responses (Kang et al., 2008, 2010, 2012). While the CRT1/MORC1 family positively modulates resistance in Arabidopsis and potato, in barley (Langen et al., 2014) and tomato this family negatively affects resistance, since its silencing results in enhanced resistance. To understand this species-specific effect of altering expression of CRT1/MORC1 on immunity, we took advantage of the differential effects in closely related tomato and potato. Using domain swapping and site-directed mutagenesis we determined that this species specificity is due to differences in the proteins themselves rather than the cellular environment in which these proteins function. This species specificity is determined by just four amino acid differences in the C-t region of these 650 amino acid proteins. We found that this C-t region also is required for i) protein dimerization and ii) interaction with 14 other proteins, iii) is phosphorylated, and iv) displays signaling activity (Manosalva et al., 2015). We suspect the species-specific effect is controlled by differential interaction of the C-t of the potato vs. tomato MORC1 with other proteins , which is being assessed using proteomics. We are also characterizing a new enzyme activity, which likely will provide insight into the function of MORCs in gene silencing.
E. Modulation of plant immunity by nematode ascarosides
This is our newest area of research and one that holds considerable commercial promise. It is done in collaboration with Frank Schroeder. We discovered that plant parasitic nematodes produce small molecules called ascarosides, an evolutionarily conserved family of nematode pheromones, and that plants respond to these nematode-specific molecular patterns by activating systemic defenses against a broad spectrum of pathogens. Picomolar to micromolar concentrations of ascr#18, the most abundant ascaroside in plant parasitic nematodes, induced hallmark defense responses, including the expression of genes associated with Microbe-Associated Molecular Pattern (MAMP)-triggered immunity and activation of MAPKs. Ascr#18 induced both SA- and JA-mediated defense signaling pathways, enhanced resistance to virulent viral and bacterial pathogens, and reduced cyst nematode infection in Arabidopsis. Furthermore, we found that ascr#18 perception via roots or leaves increases resistance in tomato, potato, and barley to foliar bacterial, oomycete, or fungal pathogens. Our results indicate that monocots and dicots recognize ascarosides as a conserved molecular signature of nematodes that triggers conserved plant defense signaling pathways, similar to perception of MAMPs (Manosalva et al., 2015).
Murli ManoharPostdoctoral scientist Office/Lab: 225/206 firstname.lastname@example.org Office: Lab: (607) 254-1255
Klessig, D. F., Tian, M., and Choi H.-W. 2016. Multiple targets of salicylic acid and its derivatives in plants and animals. Immunology (in review). [Full Text ...]
Choi, H.W., Manohar, M., Manosalva, P., Tian, M., Moreau, M., and Klessig, D.F. 2016. Activation of Plant Innate Immunity by Extracellular High Mobility Group Box 3 and Its Inhibition by Salicylic Acid. PLOS Pathog. 12, e1005518. [Full Text ...]
Klessig, D.F. 2016. Newly identified targets of Aspirin and its primary metabolite, salicylic acid. DNA Cell Biol. 35, 163-166. [Full Text ...]
Choi, H.W., Tian, M., Song, F., Venereau, E., Preti, A., Park, S.W., Hamilton, K., Swapna, G.V.T., Manohar, M., Moreau, M., Agresti, A., Gorzanelli, A., De Marchis, F., Wang, H., Antonyak, M., Micikas, R., Gentile, D.R., Cerione, R.A., Schroeder, F.C., Montelione, G.T., Bianchi, M.E., and Klessig, D.F. 2015. Aspirin’s Active Metabolite Salicylic Acid Targets Human High Mobility Group Box 1 to Modulate Inflammatory Responses. Mol. Med. 21:526-535 [Full Text ...]
Choi, H.W., Tian, M., Manohar, M., Harraz, M.M., Park, S.-W., Schroeder, F.C., Snyder, S.H., and Klessig, D.F. 2015. Human GAPDH is a target of aspirin’s primary metabolite salicylic acid and its derivatives. PLOS ONE 10:e0143447 [Full Text ...]
Manohar, M., Tian, M., Moreau, M., Park, S-W., Choi, H.W., Fei, Z., Friso, G., Asif, M., Manosalva, P., von Dahl, C.C., Shi, K., Ma, S., Dinesh-Kumar, S.P., O'Doherty, I., Schroeder, F.C., van Wijk, K.J., and Klessig, D.F. 2015. Identification of multiple salicylic acid-binding proteins using two high throughput screens. Front. Plant Sci., 5, 777. [Full Text ...]
Tian, M., Sasvani, Z., Gonzalez, P.A., Friso, G., Rowland, E., Liu, X-M., van Wijk, K.J., Nagy, P.D., and Klessig, D. 2015. Salicylic acid inhibits the replication of Tomato Bushy Stunt Virus by directly targeting a host component in the replication complex. Molecular Plant-Microbe Interactions [Full Text ...]
Manosalva, P., Manohar, M., von Reuss, S.H., Chen, S., Micikas, R.J., Koch, A., Choe, A., Kaplan, F., Xiaohong Wang, X., Kogel, K-H., Sternberg, P.W., Williamson, V. M., Schroeder, F.C., and Klessig, D.F. 2015. Conserved nematode signaling molecules elicit plant defenses and pathogen resistance. Nature Comm 6:7795 [Full Text ...]
Manosalva, P., Manohar, M., Kogel, K-H., Kang, H-G., and Klessig, D.F. 2015. The GHKL ATPase MORC1 modulates species-specific plant immunity in Solanaceae.
Langen, G., von Einem, S., Koch, A.,Imani, J., Pai, S.B., Manohar, M., Ehlers, K., Choi, H.W., Claar, M., Schmidt, R., Mang, H-G., Bordiya, Y., Kang, H-G., Klessig, D.F., and Kogel, K-H. 2014. The Compromised Recognition of Turnip Crinkle Virus1 Subfamily of Microrchidia ATPases Regulates Disease Resistance in Barley to Biotrophic and Necrotrophic Pathogens. Plant Physiology, 164(2), 866-878. [Full Text ...]
Liao, Y., Tian, M., Zhang, H., Li, X., Xia, X., Zhou, J., Zhou, Y., Yul, J., Shi, K., and Klessig, D.F. 2014. Salicylic acid binding of mitochondrial alpha-ketoglutarate dehydrogenase E2, which interacts with the downstream mitochondrial electron transport chain, plays a crucial role in basal defense against TMV in tomato. New Phytologist, doi: 10.1111/nph13137. [Full Text ...]
Wang, R., Rajagopalan, K., Sadre-Bazzaz, K., Moreau, M., Klessig, D.F., and Tong, L. 2014. Crystal structure of the Arabidopsis thaliana TOP2 oligopeptidase. Acta. Crystallogr. F. Struct. Biol. Commun., 70, 555. [Full Text ...]
Dempsey, D.A., and Klessig, D.F. 2012. SOS – too many signals for systemic acquired resistance?. Trends Plant Sci., 17, 538-545. [Full Text ...]
Wang, R., Rajagopalan, K., Sadre-Bazzaz, K., Moreau, M., Klessig, D.F., and Tong, L. 2014. Structure of the Arabidopsis thaliana TOP2 oligopeptidase. Acta Cryst., F70, 555–559. [Full Text ...]
Kang, H.G., Hyong, W.C., von Einem, S., Manosalva, P., Ehlers, K., Liu, P.P., Buxa, S.V., Moreau, M., Mang, H.G., Kachroo, P., Kogel, K.H., and Klessig, D.F. 2012. CRT1 is a nuclear-translocated MORC endonuclease that participates in multiple levels of plant immunity. Nature Communications, 3, 1297. [Full Text ...]
Mang, H.G., Qian, W.Q., Zhu, Y., Qian, J., Kang, H.G., Klessig, D.F., and Hua, J. 2012. Abscisic acid deficiency antagonizes high-temperature inhibition of disease resistance through enhancing nuclear accumulation of resistance proteins SNC1 and RPS4 in Arabidopsis. Plant Cell, 24, 1271-1284. [Full Text ...]
Moreau, M., Tian, M., and Klessig, D.F. 2012. Salicylic acid binds NPR3 and NPR4 to regulate NPR1-dependent defense responses. Cell Res., 22, 1631-1633. [Full Text ...]
Tian, M., von Dahl, C.C., Liu, P.P., Friso, G., van Wijk, K.J., and Klessig, D.F. 2012. The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins. Plant J., 72, 1027-1038. [Full Text ...]
Zheng, X.Y., Spivey, N.W., Zeng, W.Q., Liu, P.P., Fu, Z.Q., Klessig, D.F., He, S.Y., and Dong, X.N . 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe, 11, 587-596. [Full Text ...]
Liu, P.P., von Dahl, C.C., and Klessig, D.F. 2011. The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiology, 157, 2216-2226. [Full Text ...]
Liu, P.P., von Dahl, C.C., Park, S.W., and Klessig, D.F. 2011. Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiology, 155, 1762-1768. [Full Text ...]
Dempsey, D.A., Vlot, A.C., Wildermuth, M.C., and Klessig, D.F. 2011. Salicylic acid biosynthesis and metabolism. In The Arabidopsis Book American Society of Plant Biologists, e0156. [Full Text ...]
Moreau, M., Lindermayr, C., Durner, J., and Klessig, D.F. 2010. NO synthesis and signaling in plants–where do we stand?. Physiol. Plant, 138, 372-383. [Full Text ...]
Mosher, S., Moeder, W., Nishimura, N., Jikumaru, Y., Joo, S.H., Urquhart, W., Klessig, D.F., Kim, S.K., Nambara, E., and Yoshioka, K. 2010. The lesion-mimic mutant cpr22 shows alterations in abscisic acid signaling and abscisic acid insensitivity in a salicylic acid-dependent manner. Plant Physiology, 152, 1901-1913. [Full Text ...]
Manosalva, P.M., Park, S.W., Forouhar, F., Tong, L., Fry , W.E., and Klessig, D.F. 2010. Methyl esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol. Plant Microbe Interact., 23, 1151-1163. [Full Text ...]
Kang, H.G., Oh, C.S., Sato, M., Katagiri, F., Glazebrook, J., Takahashi, H., Kachroo, P., Martin, G.B., and Klessig, D.F. 2010. Endosome-associated CRT1 functions early in resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell, 22, 918-936. [Full Text ...]
Liu, P.P., Yang, Y., Pichersky, E., and Klessig, D.F. 2010. Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in arabidopsis. Mol. Plant Microbe Interact., 23, 82-90. [Full Text ...]
Liu, P.P., Bhattacharjee, S., Klessig, D.F., and Moffett, P. 2010. Systemic acquired resistance is induced by R gene-mediated responses independent of cell death. Mol. Plant Pathol., 11, 155-160. [Full Text ...]
Jeong, R.D., Chandra-Shekara, A.C., Barman, S.R., Navarre, D., Klessig, D.F., Kachroo, A., and Kachroo, P. 2010. Cryptochrome 2 and phototropin 2 regulate resistance protein-mediated viral defense by negatively regulating an E3 ubiquitin ligase. P. Natl. Acad. Sci. U S A, 107, 13538-13543. [Full Text ...]
Vlot, A.C., Dempsey, D.A., and Klessig, D.F. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol., 47, 177-206. [Full Text ...]
Park, S.W., Liu, P.P., Forouhar, F., Vlot, A.C., Tong, L., Tietjen, K., and Klessig, D.F. 2009. Use of a synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. Journal of Biological Chemistry, 284, 7307-7317. [Full Text ...]
Kawamura, Y., Takenaka, S., Hase, S., Kubota, M., Ichinose, Y., Kanayama, Y., Nakaho, K., Klessig, D.F., and Takahashi, H. 2009. Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1. Plant Cell Physiol., 50, 924-934. [Full Text ...]
Vlot, A.C., Liu, P.P., Cameron, R.K., Park, S.W., Yang, Y., Kumar, D., Zhou, F.S., Padukkavidana, T., Gustafsson, C., Pichersky, E., and Klessig, D.F. 2008. Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J., 56, 445-456. [Full Text ...]
Vlot, A.C., Klessig, D.F., and Park, S.W. 2008. Systemic acquired resistance: the elusive signal(s). Curr. Opin. Plant Biol., 11, 436-442. [Full Text ...]
Sudhamsu, J., Lee, G.I., Klessig, D.F., and Crane, B.R. 2008. The Structure of YqeH: An AtNOS1/AtNOA1 ortholog that couples GTP hydrolysis to molecular recognition. Journal of Biological Chemistry, 283, 32968-32976. [Full Text ...]
Sekine, K.T., Kawakami, S., Hase, S., Kubota, M., Ichinose, Y., Shah, J., Kang, H.G., Klessig, D.F., and Takahashi, H. 2008. High level expression of a virus resistance gene, RCY1, confers extreme resistance to Cucumber mosaic virus in Arabidopsis thaliana. Mol. Plant Microbe Interact., 21, 1398-1407. [Full Text ...]
Moreau, M., Lee, G.I., Wang, Y., Crane, B.R., and Klessig, D.F. 2008. AtNOS/AtNOA1 Is a Functional Arabidopsis thaliana cGTPase and Not a Nitric-oxide Synthase. Journal of Biological Chemistry, 283, 32957-32967. [Full Text ...]
Moffett, P., and Klessig, D.F. 2008. Plant resistance to viruses: Natural resistance associated with dominant genes. In Encyclopedia of Virology (Mahy, B.W.J. and van Regenmortel, M. eds). Oxford 0: Elsevier. [Full Text ...]
Park, S.-W., Kaiyomo, E., Kumar, D., Mosher, S.L., and Klessig, D.F. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science, 318, 113-116. [Full Text ...]
Kumar, D., and Klessig, D.F. 2008. The search for the salicylic acid receptor led to discovery of the SAR signal receptor. Plant Signal Behav., 3, 691-692. [Full Text ...]
Kang, H.G., Kuhl, J.C., Kachroo, P., and Klessig, D.F. 2008. CRT1, an Arabidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to turnip crinkle virus. Cell Host & Microbe, 3, 48-57. [Full Text ...]
Jeong, R.D., Chandra-Shekara, A.C., Kachroo, A., Klessig, D.F., and Kachroo, P. 2008. HRT-mediated hypersensitive response and resistance to Turnip crinkle virus in Arabidopsis does not require the function of TIP, the presumed guardee protein. Mol. Plant Microbe Interact., 21, 1316-1324. [Full Text ...]
Kang, H.G., and Klessig, D.F. 2008. The involvement of the Arabidopsis CRT1 ATPase family in disease resistance protein-mediated signaling. Plant Signal Behav., 3, 689-690. [Full Text ...]
Yang, Y., Xu, R., Ma, C.J., Vlot, A.C., Klessig, D.F., and Pichersky, E. 2008. Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiology, 147, 1034-1045. [Full Text ...]
Zhou, F.S., Mosher, S., Tian, M.Y., Sassi, G., Parker, J., and Klessig, D.F. 2008. The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol. Plant Microbe Interact., 21, 40-49. [Full Text ...]
Kumar, D., Gustafsson, C., and Klessig, D.F. 2006. Validation of RNAi Silencing Specificity Using Synthetic Genes: Salicylic Acid-binding Protein 2 is Required for Innate Immunity in Plants. Plant J., 45, 863-868. [Full Text ...]
Yoshioka, K., Moeder, W., Kang, H.-G., Kachroo, P., Masmoudi, K., Berkowitz, G., and Klessig, D.F. 2006. The Chimeric Arabidopsis CYCLIC NUCLEOTIDE-GATED ION CHANNEL11/12 Activates Multiple Pathogen Resistance Responses. Plant Cell, 18, 747-763. [Full Text ...]
Forouhar, F., Yang, Y., Kumar, D., Chen, Y., Fridman, E., Park, S.W., Chiang, Y., Acton, T.B., Montelione, G.T., Pichersky, E., Klessig, D.F., and Tong, L. 2005. Crystal structure and biochemical studies identify tobacco SABP2 as a methylsalicylate esterase and further implicate it in plant innate immunity. P. Natl. Acad. Sci. U S A, 102, 1773-1778. [Full Text ...]
Menke, F.L.H., van Pelt, J.A., Pieterse, C.M.J., and Klessig, D.F. 2004. Silencing of the Mitogen-activated Protein Kinase MPK6 Compromises Disease Resistance in Arabidopsis. Plant Cell, 16, 897-907. [Full Text ...]
Liu, P.-P., von Dahl, C. C., Park, S.-W., and Klessig, D. F. 2001. Interconnection between methyl salicylate and lipid-based long-distance signaling during systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol., 155, 1762-1768. [Full Text ...]
Zhu, S.F., Jeong, R.D., Lim, G.H., Yu, K.S., Wang, C.X., Chandra-Shekara, A.C., Navarre, D., Klessig, D.F., Kachroo, A., and Kachroo, P. 2013. Double-Stranded RNA-Binding Protein 4 Is Required for Resistance Signaling against Viral and Bacterial Pathogens. Cell Reports, 4, 1168-1184. [Full Text ...]
|Technology Area||Title||US Patent/ Appl||Publication|
|Biotic Stress - Disease||Salicylic acid induced map kinase and its use for enhanced disease resistance in plants||5,977,442||Plant Cell 1997PNAS 1998|
|Biotic Stress - Disease||Salicylic Acid Binding Protein (SABP2)||7,169,966||PNAS 2003|
|Enabling Technology||Methods for determining specificity of RNA silencing and for genetic analysis of the silenced gene or protein||7,592,504||Plant J 2006|
|Biotic Stress - Disease||Methods and compositions for improving salicylic acid-independent systemic acquired disease resistance in plants||6,495,737||Plant J 1998|
|Biotic Stress - Disease||Method of using a pathogen-activatable map kinase to enhance disease resistance in plants||6,765,128||PNAS 1998|
|Biotic Stress - Disease||High-affinity salicylic acid-binding protein and methods of use||6,136,552||Plant Physiol 1997|
|Biotic Stress - Disease||Genes Associated with enhanced disease resistance in plants||5,939,601||PNAS 1996|
|Biotic Stress - Disease||Compositions and methods for the generation of disease-resistant crops||PCT/US2012/043976||NONE|
|Biotic Stress - Disease||Compositions and method for modulating immunity in plants||Provisional||No publications or other links at this time|
|Biotic Stress - Disease||Assays to identify inducers of plant defense resistance||5,989,846||Science 1993|
In The News
The Spring 2016 issue of the Parkinson's Disease Foundation newsletter featured recent work by Dan Klessig. The newsletter highlighted his recent PLOS ONE paper on salicylic acid and human GAPDH. Read More
Research from the Klessig lab shows that HMGB3 signals to the plant immune system when tissues are damaged and makes plants more resistant to certain infections. Read More
The active ingredient in aspirin blocks an enzyme that triggers cell death in Alzheimer's, Parkinson's and Huntington's diseases, offering hope for novel treatments. Read More
Researchers have found that salicylic acid targets the activities of HMGB1, an inflammatory protein associated with a wide variety of diseases, offering hope that more powerful aspirin-like drugs may be developed. Read More
When plants detect pheromones given off by nematode worms, they activate their immune system for protection. The chemical warning not only triggers defenses against nematodes, but also against bacterial, fungal and viral infection. Read More
Drs. Harrison, Klessig, and Jander honored Read More
Over the past decade we have hosted 10 undergraduate research interns. All have worked closely with senior postdoctoral fellows or research associates, with most of them studying various aspects of SA-mediated defense signaling in plants. In addition, two helped characterize CRT1/MORC1.