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PMID: 27007252 Published · epublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Activation of Plant Innate Immunity by Extracellular High Mobility Group Box 3 and Its Inhibition by Salicylic Acid.

PLoS pathogens ·Vol. 12 ·No. 3 ·2016-03-00 ·Pages e1005518

Choi HW, Manohar M, Manosalva P, Tian M, Moreau M, Klessig DF

Abstract

Damage-associated molecular pattern molecules (DAMPs) signal the presence of tissue damage to induce immune responses in plants and animals. Here, we report that High Mobility Group Box 3 (HMGB3) is a novel plant DAMP. Extracellular HMGB3, through receptor-like kinases BAK1 and BKK1, induced hallmark innate immune responses, including i) MAPK activation, ii) defense-related gene expression, iii) callose deposition, and iv) enhanced resistance to Botrytis cinerea. Infection by necrotrophic B. cinerea released HMGB3 into the extracellular space (apoplast). Silencing HMGBs enhanced susceptibility to B. cinerea, while HMGB3 injection into apoplast restored resistance. Like its human counterpart, HMGB3 binds salicylic acid (SA), which results in inhibition of its DAMP activity. An SA-binding site mutant of HMGB3 retained its DAMP activity, which was no longer inhibited by SA, consistent with its reduced SA-binding activity. These results provide cross-kingdom evidence that HMGB proteins function as DAMPs and that SA is their conserved inhibitor.

MeSH Terms
Arabidopsis/genetics Arabidopsis Proteins/genetics,metabolism Botrytis/immunology,metabolism Cyclopentanes/metabolism Disease Resistance Ethylenes/metabolism Gene Expression Regulation, Plant Oxylipins/metabolism Plant Diseases/parasitology Plant Leaves/genetics Plants/immunology Pseudomonas syringae/metabolism Salicylic Acid/metabolism Signal Transduction/drug effects
Chemicals
Arabidopsis Proteins Cyclopentanes Ethylenes Oxylipins Salicylic Acid
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Choi Hyong Woo
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
Manohar Murli
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
Manosalva Patricia
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
Tian Miaoying
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
Moreau Magali
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
Klessig Daniel F
Boyce Thompson Institute for Plant Research, Ithaca, New York, United States of America.
References (64)
64 references, click to expand
  1. Callose deposition: a multifaceted plant defense response.
    Mol Plant Microbe Interact. 2011 Feb;24(2):183-93 PMID: 20955078
  2. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion.
    EMBO J. 2003 Oct 15;22(20):5551-60 PMID: 14532127
  3. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation.
    Plant Cell. 1999 Aug;11(8):1393-404 PMID: 10449575
  4. Salicylic Acid, a multifaceted hormone to combat disease.
    Annu Rev Phytopathol. 2009;47:177-206 PMID: 19400653
  5. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4.
    Cell Host Microbe. 2010 Feb 18;7(2):164-75 PMID: 20159621
  6. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.
    Cell Rep. 2012 Jun 28;1(6):639-47 PMID: 22813739
  7. Unexpected mobility of plant chromatin-associated HMGB proteins.
    Plant Signal Behav. 2011 Jun;6(6):878-80 PMID: 21543902
  8. Protein phosphatase 2A dephosphorylates phosphoserines in nucleocytoplasmic shuttling and secretion of high mobility group box 1.
    J Biochem. 2013 Sep;154(3):299-308 PMID: 23782844
  9. The expression level of the chromatin-associated HMGB1 protein influences growth, stress tolerance, and transcriptome in Arabidopsis.
    J Mol Biol. 2008 Dec 5;384(1):9-21 PMID: 18822296
  10. MAPK cascades in plant defense signaling.
    Trends Plant Sci. 2001 Nov;6(11):520-7 PMID: 11701380
  11. Plant pattern-recognition receptors.
    Trends Immunol. 2014 Jul;35(7):345-51 PMID: 24946686
  12. MD-2 is required for disulfide HMGB1-dependent TLR4 signaling.
    J Exp Med. 2015 Jan 12;212(1):5-14 PMID: 25559892
  13. An endogenous peptide signal in Arabidopsis activates components of the innate immune response.
    Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10098-103 PMID: 16785434
  14. Aspirin's Active Metabolite Salicylic Acid Targets High Mobility Group Box 1 to Modulate Inflammatory Responses.
    Mol Med. 2015;21:526-35 PMID: 26101955
  15. The infiltration-centrifugation technique for extraction of apoplastic fluid from plant leaves using Phaseolus vulgaris as an example.
    J Vis Exp. 2014;(94). doi: 10.3791/52113 PMID: 25549068
  16. The combined use of photoaffinity labeling and surface plasmon resonance-based technology identifies multiple salicylic acid-binding proteins.
    Plant J. 2012 Dec;72(6):1027-38 PMID: 23083132
  17. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance.
    Cell. 2000 Dec 22;103(7):1111-20 PMID: 11163186
  18. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal.
    Nat Rev Immunol. 2005 Apr;5(4):331-42 PMID: 15803152
  19. Identification of multiple salicylic acid-binding proteins using two high throughput screens.
    Front Plant Sci. 2015 Jan 12;5:777 PMID: 25628632
  20. HMG1 and 2, and related 'architectural' DNA-binding proteins.
    Trends Biochem Sci. 2001 Mar;26(3):167-74 PMID: 11246022
  21. Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense.
    Proc Natl Acad Sci U S A. 2013 Apr 2;110(14):5707-12 PMID: 23509266
  22. Purification and characterization of a soluble salicylic acid-binding protein from tobacco.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9533-7 PMID: 8415736
  23. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release.
    J Exp Med. 2012 Aug 27;209(9):1519-28 PMID: 22869893
  24. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways.
    Curr Biol. 2007 Jul 3;17(13):1109-15 PMID: 17600708
  25. Salicylic Acid biosynthesis and metabolism.
    Arabidopsis Book. 2011;9:e0156 PMID: 22303280
  26. Gene silencing in plants using artificial microRNAs and other small RNAs.
    Plant J. 2008 Feb;53(4):674-90 PMID: 18269576
  27. Protein kinase CK2 differentially phosphorylates maize chromosomal high mobility group B (HMGB) proteins modulating their stability and DNA interactions.
    J Biol Chem. 2002 Jan 11;277(2):1092-8 PMID: 11694523
  28. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance.
    Plant Physiol. 2011 Mar;155(3):1325-38 PMID: 21205619
  29. HMGB1 is a therapeutic target for sterile inflammation and infection.
    Annu Rev Immunol. 2011;29:139-62 PMID: 21219181
  30. High-mobility group box 1 and cancer.
    Biochim Biophys Acta. 2010 Jan-Feb;1799(1-2):131-40 PMID: 20123075
  31. Identification of a plant receptor for extracellular ATP.
    Science. 2014 Jan 17;343(6168):290-4 PMID: 24436418
  32. Plant immunity: towards an integrated view of plant-pathogen interactions.
    Nat Rev Genet. 2010 Aug;11(8):539-48 PMID: 20585331
  33. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  34. Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal.
    Proc Natl Acad Sci U S A. 2014 Aug 19;111(33):12157-62 PMID: 25097261
  35. HMGB1 promotes recruitment of inflammatory cells to damaged tissues by forming a complex with CXCL12 and signaling via CXCR4.
    J Exp Med. 2012 Mar 12;209(3):551-63 PMID: 22370717
  36. Highly specific gene silencing by artificial microRNAs in Arabidopsis.
    Plant Cell. 2006 May;18(5):1121-33 PMID: 16531494
  37. Simultaneous metal chelate affinity purification and endotoxin clearance of recombinant antibody fragments.
    J Immunol Methods. 2006 Jul 31;314(1-2):67-73 PMID: 16824538
  38. HMGB1 loves company.
    J Leukoc Biol. 2009 Sep;86(3):573-6 PMID: 19414536
  39. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.
    Mol Syst Biol. 2011;7:539 PMID: 21988835
  40. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation.
    Nature. 2002 Jul 11;418(6894):191-5 PMID: 12110890
  41. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens.
    Plant Cell. 2011 Jun;23(6):2440-55 PMID: 21693696
  42. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9452-7 PMID: 20439716
  43. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.
    Nature. 2012 Jun 14;486(7402):228-32 PMID: 22699612
  44. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi.
    Plant Cell. 2013 Oct;25(10):4227-41 PMID: 24104566
  45. JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation.
    Proc Natl Acad Sci U S A. 2014 Feb 25;111(8):3068-73 PMID: 24469805
  46. Salicylic Acid Inhibits the Replication of Tomato bushy stunt virus by Directly Targeting a Host Component in the Replication Complex.
    Mol Plant Microbe Interact. 2015 Apr;28(4):379-86 PMID: 25584724
  47. One for all: the receptor-associated kinase BAK1.
    Trends Plant Sci. 2009 Oct;14(10):535-41 PMID: 19748302
  48. Microheterogeneous Cytosolic High-Mobility Group Proteins from Broccoli Co-Purify with and Are Phosphorylated by Casein Kinase II.
    Plant Physiol. 1994 Jul;105(3):911-919 PMID: 12232253
  49. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1.
    PLoS Genet. 2011 Apr;7(4):e1002046 PMID: 21593986
  50. Human GAPDH Is a Target of Aspirin's Primary Metabolite Salicylic Acid and Its Derivatives.
    PLoS One. 2015;10(11):e0143447 PMID: 26606248
  51. Arabidopsis chromatin-associated HMGA and HMGB use different nuclear targeting signals and display highly dynamic localization within the nucleus.
    Plant Cell. 2006 Nov;18(11):2904-18 PMID: 17114349
  52. Phosphorylation of maize and Arabidopsis HMGB proteins by protein kinase CK2alpha.
    Biochemistry. 2003 Apr 1;42(12):3503-8 PMID: 12653554
  53. Characterization of transgenic Arabidopsis plants overexpressing high mobility group B proteins under high salinity, drought or cold stress.
    Plant Cell Physiol. 2007 Feb;48(2):221-31 PMID: 17169924
  54. Nucleocytoplasmic distribution of the Arabidopsis chromatin-associated HMGB2/3 and HMGB4 proteins.
    Plant Physiol. 2010 Dec;154(4):1831-41 PMID: 20940346
  55. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells.
    Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10104-9 PMID: 16785433
  56. Danger signals - damaged-self recognition across the tree of life.
    Front Plant Sci. 2014 Oct 31;5:578 PMID: 25400647
  57. Nucleocytoplasmic shuttling of HMGB1 is regulated by phosphorylation that redirects it toward secretion.
    J Immunol. 2006 Dec 1;177(11):7889-97 PMID: 17114460
  58. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11312-6 PMID: 7479986
  59. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors.
    Annu Rev Plant Biol. 2009;60:379-406 PMID: 19400727
  60. Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation.
    Plant Cell Physiol. 2005 Feb;46(2):268-78 PMID: 15769808
  61. The role of chromosomal HMGB proteins in plants.
    Biochim Biophys Acta. 2010 Jan-Feb;1799(1-2):171-4 PMID: 20123078
  62. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB.
    Plant Physiol. 2009 Jun;150(2):815-24 PMID: 19346440
  63. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis.
    Plant Cell. 2010 Feb;22(2):508-22 PMID: 20179141
  64. The hypersensitive induced reaction and leucine-rich repeat proteins regulate plant cell death associated with disease and plant immunity.
    Mol Plant Microbe Interact. 2011 Jan;24(1):68-78 PMID: 20635864
Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
DOI
10.1371/journal.ppat.1005518
Published
2016-03-00
Epub
2016-00-23
Pages
e1005518
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC4805298
Subset
IM
External Links
PubMed source DOI: 10.1371/journal.ppat.1005518 PMC Full Text View journal details
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