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Jean Greenberg

Professor
jgreenbe@uchicago.edu
Research Summary
Research My broad interest is in how organisms adapt to a changing environment. My lab studies this in the context of pathogen-host interactions using the gram negative pathogen Pseudomonas syringae and its interaction with several plants: the non-crop models Arabidopsis thaliana and Nicotiana benthamiana, and the crop plants tomato and snap beans. In response to infection, plants mount a complex local defense response involving cell suicide, changes at the plasma membrane, the crosslinking of cell wall components, production of antimicrobials and defense gene activation. Some leaf infections induce a primed state that allows plants to respond faster when a second infection occurs on distal leaves (systemic acquired resistance, SAR). Interactions of roots with beneficial microbes also induces a primed state in the aerial part of the plant (and induced systemic resistance, ISR). Although SAR and ISR were considered different immune programs, we have found that some of the same are proteins required for both systemic programs. These proteins are involved in mobilizing small molecule signals. The lab investigates plant defense and pathogen virulence mechanisms. We study how plants regulate their responses to pathogens by (1) using plant mutants that express one or more aspects of the defense response in the absence of pathogens or are compromised for local defense activation or SAR, (2) discovering and tracking the production and movement of novel defense signals and pathogen-derived molecules, and (3) exploiting secreted virulence effector proteins from the pathogen to discover immune components and discern how they are modified. This involves combining genetic analysis (including mosaic plants in which only some cells/tissues express specific defense components) with biochemistry and cell biology. We are very interested in how the defense response is coordinated and towards this end, we are investigating the sites of action at the tissue and subcellular levels of key SAR/ISR proteins. On the pathogen side, we are also characterizing how P. syringae uses its type III secretion apparatus and secreted effectors to modulate immunity and colonize plant tissue, including the surfaces of a leaf, a unique niche. We are using proteomic approaches to discern how pathogen effectors post-translationally modify both other pathogen effectors and host immune complexes to suppress signaling. We are interested in exploiting what we learn about P. syringae effectors to study orthologous effectors from diverse pathogens of both plants and animals. A recent additional interest is in peptide trafficking and signal output as it relates to development and microbial interactions. Our lab welcomes participants from all over the world and at many levels of education (high school, college, predoctoral, postdoctoral and teachers). Professional Activities and Service I have been a Senior Editor of The Plant Cell, a Reviewing Editor of eLIFE and Secretary to the Board of Directors of the International Society of Plant-Microbe Interactions. I am a member of the American Society of Plant Biology and the Society for Experimental Biology. I participated in developing and writing a recently published white paper concerning the promotion of plant heath: "Foundational and translational research opportunities to improve plant health." Currently I am a member of the Plant Biology Advisory Board for Landmarks. I am a strong advocate for diversity in science and serve on the University of Chicago Division of Biology's Diversity Committee and on the steering committee of the Molecular Genetics and Cell Biology Department's National Science Foundation-sponsored Research Education for Undergraduates program.
Keywords
plant immunity, type III pathogen effector, Posttranslational Modifications, systemic acquired resistance, induced systemic resistance, Pseudomonas syringae
Education
  • Barnard College, Columbia University, New York City, BA Biochemistry 06/1983
  • Harvard University, Cambridge, MA, PhD Biophysics 06/1989
  • Massachussetts General Hospital, Boston, MA, postdoc training Plant Biology 12/1994
Biosciences Graduate Program Association
Awards & Honors
  • 1983 - Magna Cum Laude Barnard College, Columbia University
  • 1989 - 1992 Postdoctoral Fellowship National Science Foundation
  • 1996 - 1999 Faculty Research Fellow American Cancer Society
  • 1996 - 2001 Biomedical Scholar Pew Foundation
Publications

  1. Banday ZZ, Cecchini NM, Speed DJ, Scott AT, Parent C, Hu CT, Filzen RC, Agbo E, Greenberg JT. Friend or Foe: Hybrid proline-rich proteins determine how plants respond to beneficial and pathogenic microbes. Plant Physiol. 2022 Jun 01. View in: PubMed

  2. Erickson OA, Cole RB, Isaacs JM, Alvarez-Clare S, Arnold J, Augustus-Wallace A, Ayoob JC, Berkowitz A, Branchaw J, Burgio KR, Cannon CH, Ceballos RM, Cohen CS, Coller H, Disney J, Doze VA, Eggers MJ, Farina S, Ferguson EL, Gray JJ, Greenberg JT, Hoffmann A, Jensen-Ryan D, Kao RM, Keene AC, Kowalko JE, Lopez SA, Mathis C, Minkara M, Murren CJ, Ondrechen MJ, Ordoñez P, Osano A, Padilla-Crespo E, Palchoudhury S, Qin H, Ramírez-Lugo J, Reithel J, Shaw CA, Smith A, Smith R, Summers AP, Tsien F, Dolan EL. "How Do We Do This at a Distance?!" A Descriptive Study of Remote Undergraduate Research Programs during COVID-19. CBE Life Sci Educ. 2022 03; 21(1):ar1. View in: PubMed

  3. Jelenska J, Lee J, Manning AJ, Wolfgeher DJ, Ahn Y, Walters-Marrah G, Lopez IE, Garcia L, McClerklin SA, Michelmore RW, Kron SJ, Greenberg JT. Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation. PLoS Pathog. 2021 11; 17(11):e1010017. View in: PubMed

  4. Cecchini NM, Song Y, Roychoudhry S, Greenberg JT, Haney CH. An Improved Bioassay to Study Arabidopsis Induced Systemic Resistance (ISR) Against Bacterial Pathogens and Insect Pests. Bio Protoc. 2019 May 20; 9(10):e3236. View in: PubMed

  5. Jiang SC, Engle NL, Banday ZZ, Cecchini NM, Jung HW, Tschaplinski TJ, Greenberg JT. ALD1 accumulation in Arabidopsis epidermal plastids confers local and non-autonomous disease resistance. J Exp Bot. 2021 03 29; 72(7):2710-2726. View in: PubMed

  6. Cecchini NM, Speed DJ, Roychoudhry S, Greenberg JT. Kinases and protein motifs required for AZI1 plastid localization and trafficking during plant defense induction. Plant J. 2021 03; 105(6):1615-1629. View in: PubMed

  7. Cecchini NM, Roychoudhry S, Speed DJ, Steffes K, Tambe A, Zodrow K, Konstantinoff K, Jung HW, Engle NL, Tschaplinski TJ, Greenberg JT. Underground Azelaic Acid-Conferred Resistance to Pseudomonas syringae in Arabidopsis. Mol Plant Microbe Interact. 2019 01; 32(1):86-94. View in: PubMed

  8. Seguel A, Jelenska J, Herrera-Vásquez A, Marr SK, Joyce MB, Gagesch KR, Shakoor N, Jiang SC, Fonseca A, Wildermuth MC, Greenberg JT, Holuigue L. PROHIBITIN3 Forms Complexes with ISOCHORISMATE SYNTHASE1 to Regulate Stress-Induced Salicylic Acid Biosynthesis in Arabidopsis. Plant Physiol. 2018 03; 176(3):2515-2531. View in: PubMed

  9. Manning AJ, Lee J, Wolfgeher DJ, Kron SJ, Greenberg JT. Simple strategies to enhance discovery of acetylation post-translational modifications by quadrupole-orbitrap LC-MS/MS. Biochim Biophys Acta Proteins Proteom. 2018 Feb; 1866(2):224-229. View in: PubMed

  10. Jelenska J, Davern SM, Standaert RF, Mirzadeh S, Greenberg JT. Flagellin peptide flg22 gains access to long-distance trafficking in Arabidopsis via its receptor, FLS2. J Exp Bot. 2017 03 01; 68(7):1769-1783. View in: PubMed

  11. Michelmore R, Coaker G, Bart R, Beattie G, Bent A, Bruce T, Cameron D, Dangl J, Dinesh-Kumar S, Edwards R, Eves-van den Akker S, Gassmann W, Greenberg JT, Hanley-Bowdoin L, Harrison RJ, Harvey J, He P, Huffaker A, Hulbert S, Innes R, Jones JDG, Kaloshian I, Kamoun S, Katagiri F, Leach J, Ma W, McDowell J, Medford J, Meyers B, Nelson R, Oliver R, Qi Y, Saunders D, Shaw M, Smart C, Subudhi P, Torrance L, Tyler B, Valent B, Walsh J. Foundational and Translational Research Opportunities to Improve Plant Health. Mol Plant Microbe Interact. 2017 07; 30(7):515-516. View in: PubMed

  12. Zhang Z, Tateda C, Jiang SC, Shrestha J, Jelenska J, Speed DJ, Greenberg JT. A Suite of Receptor-Like Kinases and a Putative Mechano-Sensitive Channel Are Involved in Autoimmunity and Plasma Membrane-Based Defenses in Arabidopsis. Mol Plant Microbe Interact. 2017 02; 30(2):150-160. View in: PubMed

  13. Davern SM, McKnight TE, Standaert RF, Morrell-Falvey JL, Shpak ED, Kalluri UC, Jelenska J, Greenberg JT, Mirzadeh S. Carbon Nanofiber Arrays: A Novel Tool for Microdelivery of Biomolecules to Plants. PLoS One. 2016; 11(4):e0153621. View in: PubMed

  14. Lu H, Greenberg JT, Holuigue L. Editorial: Salicylic Acid Signaling Networks. Front Plant Sci. 2016; 7:238. View in: PubMed

  15. Lee J, Manning AJ, Wolfgeher D, Jelenska J, Cavanaugh KA, Xu H, Fernandez SM, Michelmore RW, Kron SJ, Greenberg JT. Acetylation of an NB-LRR Plant Immune-Effector Complex Suppresses Immunity. Cell Rep. 2015 Nov 24; 13(8):1670-82. View in: PubMed

  16. Tateda C, Zhang Z, Greenberg JT. Linking pattern recognition and salicylic acid responses in Arabidopsis through ACCELERATED CELL DEATH6 and receptors. Plant Signal Behav. 2015; 10(10):e1010912. View in: PubMed

  17. Cecchini NM, Steffes K, Schläppi MR, Gifford AN, Greenberg JT. Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nat Commun. 2015 Jul 23; 6:7658. View in: PubMed

  18. Jelenska J, Kang Y, Greenberg JT. Plant pathogenic bacteria target the actin microfilament network involved in the trafficking of disease defense components. Bioarchitecture. 2014; 4(4-5):149-53. View in: PubMed

  19. Cecchini NM, Jung HW, Engle NL, Tschaplinski TJ, Greenberg JT. ALD1 Regulates Basal Immune Components and Early Inducible Defense Responses in Arabidopsis. Mol Plant Microbe Interact. 2015 Apr; 28(4):455-66. View in: PubMed

  20. Tateda C, Zhang Z, Shrestha J, Jelenska J, Chinchilla D, Greenberg JT. Salicylic acid regulates Arabidopsis microbial pattern receptor kinase levels and signaling. Plant Cell. 2014 Oct; 26(10):4171-87. View in: PubMed

  21. Bi FC, Liu Z, Wu JX, Liang H, Xi XL, Fang C, Sun TJ, Yin J, Dai GY, Rong C, Greenberg JT, Su WW, Yao N. Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts. Plant Cell. 2014 Aug; 26(8):3449-67. View in: PubMed

  22. Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW, Kovar DR, Greenberg JT. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog. 2014 Jun; 10(6):e1004232. View in: PubMed

  23. Zhang Z, Shrestha J, Tateda C, Greenberg JT. Salicylic acid signaling controls the maturation and localization of the arabidopsis defense protein ACCELERATED CELL DEATH6. Mol Plant. 2014 Aug; 7(8):1365-1383. View in: PubMed

  24. Lee J, Teitzel GM, Greenberg JT. SGT1b is required for HopZ3-mediated suppression of the epiphytic growth of Pseudomonas syringae on N. benthamiana. Plant Signal Behav. 2012 Sep 01; 7(9):1129-31. View in: PubMed

  25. Lee J, Teitzel GM, Munkvold K, del Pozo O, Martin GB, Michelmore RW, Greenberg JT. Type III secretion and effectors shape the survival and growth pattern of Pseudomonas syringae on leaf surfaces. Plant Physiol. 2012 Apr; 158(4):1803-18. View in: PubMed

  26. Pattanayak GK, Venkataramani S, Hortensteiner S, Kunz L, Christ B, Moulin M, Smith AG, Okamoto Y, Tamiaki H, Sugishima M, Greenberg JT. Accelerated cell death 2 suppresses mitochondrial oxidative bursts and modulates cell death in Arabidopsis. Plant J. 2012 Feb; 69(4):589-600. View in: PubMed

  27. Bi FC, Zhang QF, Liu Z, Fang C, Li J, Su JB, Greenberg JT, Wang HB, Yao N. A conserved cysteine motif is critical for rice ceramide kinase activity and function. PLoS One. 2011 Mar 31; 6(3):e18079. View in: PubMed

  28. Jelenska J, van Hal JA, Greenberg JT. Pseudomonas syringae hijacks plant stress chaperone machinery for virulence. Proc Natl Acad Sci U S A. 2010 Jul 20; 107(29):13177-82. View in: PubMed

  29. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, Xu H, Kozik A, Ochoa O, McHale LK, Lahre K, Jelenska J, Castillo JA, Blumenthal D, Vinatzer BA, Greenberg JT, Michelmore RW. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 2009 Aug; 150(4):1733-49. View in: PubMed

  30. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT. Priming in systemic plant immunity. Science. 2009 Apr 03; 324(5923):89-91. View in: PubMed

  31. Lu H, Salimian S, Gamelin E, Wang G, Fedorowski J, LaCourse W, Greenberg JT. Genetic analysis of acd6-1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis. Plant J. 2009 May; 58(3):401-12. View in: PubMed

  32. Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF. Signaling pathways that regulate the enhanced disease resistance of Arabidopsis "defense, no death" mutants. Mol Plant Microbe Interact. 2008 Oct; 21(10):1285-96. View in: PubMed

  33. Lee MW, Jelenska J, Greenberg JT. Arabidopsis proteins important for modulating defense responses to Pseudomonas syringae that secrete HopW1-1. Plant J. 2008 May; 54(3):452-65. View in: PubMed

  34. Lee MW, Lu H, Jung HW, Greenberg JT. A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. Mol Plant Microbe Interact. 2007 Oct; 20(10):1192-200. View in: PubMed

  35. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT. A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol. 2007 Mar 20; 17(6):499-508. View in: PubMed

  36. Castillo JA, Greenberg JT. Evolutionary dynamics of Ralstonia solanacearum. Appl Environ Microbiol. 2007 Feb; 73(4):1225-38. View in: PubMed

  37. Vinatzer BA, Greenberg JT. Whole-genome analysis to identify type III-secreted effectors. Methods Mol Biol. 2007; 354:19-34. View in: PubMed

  38. Vinatzer BA, Teitzel GM, Lee MW, Jelenska J, Hotton S, Fairfax K, Jenrette J, Greenberg JT. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol Microbiol. 2006 Oct; 62(1):26-44. View in: PubMed

  39. Gabriel DW, Allen C, Schell M, Denny TP, Greenberg JT, Duan YP, Flores-Cruz Z, Huang Q, Clifford JM, Presting G, González ET, Reddy J, Elphinstone J, Swanson J, Yao J, Mulholland V, Liu L, Farmerie W, Patnaikuni M, Balogh B, Norman D, Alvarez A, Castillo JA, Jones J, Saddler G, Walunas T, Zhukov A, Mikhailova N. Identification of open reading frames unique to a select agent: Ralstonia solanacearum race 3 biovar 2. Mol Plant Microbe Interact. 2006 Jan; 19(1):69-79. View in: PubMed

  40. Yao N, Greenberg JT. Arabidopsis ACCELERATED CELL DEATH2 modulates programmed cell death. Plant Cell. 2006 Feb; 18(2):397-411. View in: PubMed

  41. Lu H, Liu Y, Greenberg JT. Structure-function analysis of the plasma membrane- localized Arabidopsis defense component ACD6. Plant J. 2005 Dec; 44(5):798-809. View in: PubMed

  42. Vinatzer BA, Jelenska J, Greenberg JT. Bioinformatics correctly identifies many type III secretion substrates in the plant pathogen Pseudomonas syringae and the biocontrol isolate P. fluorescens SBW25. Mol Plant Microbe Interact. 2005 Aug; 18(8):877-88. View in: PubMed

  43. Greenberg JT. Degrade or die: a dual function for autophagy in the plant immune response. Dev Cell. 2005 Jun; 8(6):799-801. View in: PubMed

  44. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, Dangl JL, Greenberg JT, Mansfield JW, Guttman DS. Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact. 2005 Apr; 18(4):275-82. View in: PubMed

  45. Yao N, Eisfelder BJ, Marvin J, Greenberg JT. The mitochondrion--an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J. 2004 Nov; 40(4):596-610. View in: PubMed

  46. Song JT, Lu H, McDowell JM, Greenberg JT. A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 2004 Oct; 40(2):200-12. View in: PubMed

  47. Greenberg JT. PROGRAMMED CELL DEATH IN PLANT-PATHOGEN INTERACTIONS. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun; 48:525-545. View in: PubMed

  48. Greenberg JT, Yao N. The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 2004 Mar; 6(3):201-11. View in: PubMed

  49. Song JT, Lu H, Greenberg JT. Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, aberrant growth and death2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell. 2004 Feb; 16(2):353-66. View in: PubMed

  50. Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT. Ceramides modulate programmed cell death in plants. Genes Dev. 2003 Nov 01; 17(21):2636-41. View in: PubMed

  51. Lu H, Rate DN, Song JT, Greenberg JT. ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell. 2003 Oct; 15(10):2408-20. View in: PubMed

  52. Greenberg JT, Vinatzer BA. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol. 2003 Feb; 6(1):20-8. View in: PubMed

  53. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science. 2002 Mar 01; 295(5560):1722-6. View in: PubMed

  54. Vanacker H, Lu H, Rate DN, Greenberg JT. A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J. 2001 Oct; 28(2):209-16. View in: PubMed

  55. Rate DN, Greenberg JT. The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J. 2001 Aug; 27(3):203-11. View in: PubMed

  56. Guttman DS, Greenberg JT. Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol Plant Microbe Interact. 2001 Feb; 14(2):145-55. View in: PubMed

  57. Mach JM, Castillo AR, Hoogstraten R, Greenberg JT. The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Natl Acad Sci U S A. 2001 Jan 16; 98(2):771-6. View in: PubMed

  58. Greenberg JT, Silverman FP, Liang H. Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics. 2000 Sep; 156(1):341-50. View in: PubMed

  59. Greenberg JT. Positive and negative regulation of salicylic acid-dependent cell death and pathogen resistance in Arabidopsis lsd6 and ssi1 mutants. Mol Plant Microbe Interact. 2000 Aug; 13(8):877-81. View in: PubMed

  60. Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell. 1999 Sep; 11(9):1695-708. View in: PubMed

  61. Butt A, Mousley C, Morris K, Beynon J, Can C, Holub E, Greenberg JT, Buchanan-Wollaston V. Differential expression of a senescence-enhanced metallothionein gene in Arabidopsis in response to isolates of Peronospora parasitica and Pseudomonas syringae. Plant J. 1998 Oct; 16(2):209-21. View in: PubMed

  62. Greenberg JT. Programmed cell death: a way of life for plants. Proc Natl Acad Sci U S A. 1996 Oct 29; 93(22):12094-7. View in: PubMed

  63. Greenberg JT, Ausubel FM. Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. Plant J. 1993 Aug; 4(2):327-41. View in: PubMed

  64. Greenberg JT, Guo A, Klessig DF, Ausubel FM. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell. 1994 May 20; 77(4):551-63. View in: PubMed

  65. Chou JH, Greenberg JT, Demple B. Posttranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus. J Bacteriol. 1993 Feb; 175(4):1026-31. View in: PubMed

  66. Greenberg JT, Demple B. Glutathione in Escherichia coli is dispensable for resistance to H2O2 and gamma radiation. J Bacteriol. 1986 Nov; 168(2):1026-9. View in: PubMed

  67. Greenberg JT, Demple B. Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxyR-mutants. EMBO J. 1988 Aug; 7(8):2611-7. View in: PubMed

  68. Greenberg JT, Demple B. A global response induced in Escherichia coli by redox-cycling agents overlaps with that induced by peroxide stress. J Bacteriol. 1989 Jul; 171(7):3933-9. View in: PubMed

  69. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci U S A. 1990 Aug; 87(16):6181-5. View in: PubMed

  70. Greenberg JT, Chou JH, Monach PA, Demple B. Activation of oxidative stress genes by mutations at the soxQ/cfxB/marA locus of Escherichia coli. J Bacteriol. 1991 Jul; 173(14):4433-9. View in: PubMed
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