Home LiteratureArticle Details
PMID: 19214217 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae.

PLoS pathogens ·Vol. 5 ·No. 2 ·2009-02-00 ·Pages e1000301

Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J

Abstract

Salicylic acid (SA)-induced defense responses are important factors during effector triggered immunity and microbe-associated molecular pattern (MAMP)-induced immunity in plants. This article presents evidence that a member of the Arabidopsis CBP60 gene family, CBP60g, contributes to MAMP-triggered SA accumulation. CBP60g is inducible by both pathogen and MAMP treatments. Pseudomonas syringae growth is enhanced in cbp60g mutants. Expression profiles of a cbp60g mutant after MAMP treatment are similar to those of sid2 and pad4, suggesting a defect in SA signaling. Accordingly, cbp60g mutants accumulate less SA when treated with the MAMP flg22 or a P. syringae hrcC strain that activates MAMP signaling. MAMP-induced production of reactive oxygen species and callose deposition are unaffected in cbp60g mutants. CBP60g is a calmodulin-binding protein with a calmodulin-binding domain located near the N-terminus. Calmodulin binding is dependent on Ca(2+). Mutations in CBP60g that abolish calmodulin binding prevent complementation of the SA production and bacterial growth defects of cbp60g mutants, indicating that calmodulin binding is essential for the function of CBP60g in defense signaling. These studies show that CBP60g constitutes a Ca(2+) link between MAMP recognition and SA accumulation that is important for resistance to P. syringae.

MeSH Terms
Analysis of Variance Arabidopsis/genetics,immunology,metabolism,microbiology Arabidopsis Proteins/genetics,physiology Calmodulin/metabolism Calmodulin-Binding Proteins/genetics,physiology Cluster Analysis Gene Expression Profiling Glucans/metabolism Immunity, Innate Intramolecular Transferases/metabolism Mutagenesis, Insertional Mutagenesis, Site-Directed Oligonucleotide Array Sequence Analysis Plant Diseases/genetics,immunology,microbiology Pseudomonas syringae/physiology Reactive Oxygen Species/metabolism Salicylic Acid/metabolism Signal Transduction
Chemicals
Arabidopsis Proteins Calmodulin Calmodulin-Binding Proteins Glucans Reactive Oxygen Species callose Intramolecular Transferases isochorismate synthase Salicylic Acid
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wang Lin
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, St Paul, Minnesota, United States of America.
Tsuda Kenichi
Sato Masanao
Cohen Jerry D
Katagiri Fumiaki
Glazebrook Jane
References (85)
85 references, click to expand
  1. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis.
    Plant Cell. 2008 Feb;20(2):471-81 PMID: 18263776
  2. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance.
    Genetics. 1997 May;146(1):381-92 PMID: 9136026
  3. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception.
    Plant Cell. 2006 Feb;18(2):465-76 PMID: 16377758
  4. PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis.
    Plant Cell. 1998 Jun;10(6):1021-30 PMID: 9634589
  5. The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance.
    Plant Physiol. 2006 Aug;141(4):1666-75 PMID: 16778014
  6. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  7. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
    Genetics. 1996 Jun;143(2):973-82 PMID: 8725243
  8. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence.
    Nature. 2007 Jul 26;448(7152):497-500 PMID: 17625569
  9. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling.
    Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13583-8 PMID: 10557364
  10. Unconventional myosins.
    Curr Opin Cell Biol. 1992 Feb;4(1):27-35 PMID: 1558751
  11. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells.
    Plant Cell. 2002 Oct;14(10):2627-41 PMID: 12368509
  12. Biotic interactions: towards a unifying and balanced view.
    Curr Opin Plant Biol. 2006 Aug;9(4):347-50 PMID: 16753330
  13. Characterization of the hrpC and hrpRS operons of Pseudomonas syringae pathovars syringae, tomato, and glycinea and analysis of the ability of hrpF, hrpG, hrcC, hrpT, and hrpV mutants to elicit the hypersensitive response and disease in plants.
    J Bacteriol. 1998 Sep;180(17):4523-31 PMID: 9721291
  14. Arabidopsis ubiquitin-specific protease 6 (AtUBP6) interacts with calmodulin.
    FEBS Lett. 2005 Jul 18;579(18):3885-90 PMID: 15987637
  15. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  16. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases.
    Curr Biol. 2008 Jan 8;18(1):74-80 PMID: 18158241
  17. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.
    Cell. 2003 Jun 27;113(7):935-44 PMID: 12837250
  18. A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells.
    Plant Physiol. 2007 Jun;144(2):673-81 PMID: 17142489
  19. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4.
    EMBO J. 2001 Oct 1;20(19):5400-11 PMID: 11574472
  20. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants.
    Plant Cell. 1990 Jun;2(6):513-23 PMID: 2152173
  21. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals.
    Cell. 1996 May 31;85(5):673-81 PMID: 8646776
  22. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  23. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway.
    Planta. 2002 Nov;216(1):187-92 PMID: 12430030
  24. Proteinaceous and oligosaccharidic elicitors induce different calcium signatures in the nucleus of tobacco cells.
    Cell Calcium. 2005 Dec;38(6):527-38 PMID: 16198416
  25. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings.
    Mol Plant. 2008 May;1(3):423-45 PMID: 19825551
  26. Calcium/calmodulin-mediated signal network in plants.
    Trends Plant Sci. 2003 Oct;8(10):505-12 PMID: 14557048
  27. Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis.
    Plant J. 2007 Jan;49(1):159-72 PMID: 17144898
  28. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.
    Science. 1998 May 15;280(5366):1091-4 PMID: 9582125
  29. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis.
    Nature. 1999 Aug 12;400(6745):667-71 PMID: 10458161
  30. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping.
    Plant J. 2003 Apr;34(2):217-28 PMID: 12694596
  31. Plant-specific calmodulin-binding proteins.
    Annu Rev Plant Biol. 2005;56:435-66 PMID: 15862103
  32. Plant immunity: the EDS1 regulatory node.
    Curr Opin Plant Biol. 2005 Aug;8(4):383-9 PMID: 15939664
  33. A versatile and reliable two-component system for tissue-specific gene induction in Arabidopsis.
    Plant Physiol. 2006 Aug;141(4):1194-204 PMID: 16896232
  34. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis.
    Plant Cell. 2003 Aug;15(8):1846-58 PMID: 12897257
  35. Interplay between MAMP-triggered and SA-mediated defense responses.
    Plant J. 2008 Mar;53(5):763-75 PMID: 18005228
  36. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants.
    Plant Physiol. 2007 Feb;143(2):661-9 PMID: 17142480
  37. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.
    Annu Rev Phytopathol. 2005;43:205-27 PMID: 16078883
  38. 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
  39. Calcium at the crossroads of signaling.
    Plant Cell. 2002;14 Suppl:S401-17 PMID: 12045291
  40. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions.
    Cell Microbiol. 2007 Jun;9(6):1385-96 PMID: 17451411
  41. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae.
    Plant Cell. 2003 Feb;15(2):317-30 PMID: 12566575
  42. Plant stomata function in innate immunity against bacterial invasion.
    Cell. 2006 Sep 8;126(5):969-80 PMID: 16959575
  43. Characterization of a pathogen-induced calmodulin-binding protein: mapping of four Ca2+-dependent calmodulin-binding domains.
    Plant Mol Biol. 2003 May;52(1):143-59 PMID: 12825696
  44. Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley.
    Plant Cell. 2000 Aug;12(8):1425-40 PMID: 10948260
  45. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes.
    Biochem J. 2008 Jul 15;413(2):217-26 PMID: 18570633
  46. NPR1, all things considered.
    Curr Opin Plant Biol. 2004 Oct;7(5):547-52 PMID: 15337097
  47. A high-performance, small-scale microarray for expression profiling of many samples in Arabidopsis-pathogen studies.
    Plant J. 2007 Feb;49(3):565-77 PMID: 17181774
  48. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death.
    Plant J. 2000 Aug;23(4):441-50 PMID: 10972870
  49. Recognition and response in the plant immune system.
    Annu Rev Genet. 2003;37:579-609 PMID: 14616074
  50. The genetic network controlling the Arabidopsis transcriptional response to Pseudomonas syringae pv. maculicola: roles of major regulators and the phytotoxin coronatine.
    Mol Plant Microbe Interact. 2008 Nov;21(11):1408-20 PMID: 18842091
  51. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis.
    J Biol Chem. 2007 Nov 2;282(44):32338-48 PMID: 17761682
  52. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance.
    Plant Cell. 2003 Nov;15(11):2647-53 PMID: 14576289
  53. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants.
    Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12217-22 PMID: 17626179
  54. Isolation and characterization of powdery mildew-resistant Arabidopsis mutants.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1897-902 PMID: 10677553
  55. Use of real-time PCR for determining copy number and zygosity in transgenic plants.
    Plant Cell Rep. 2004 Nov;23(5):263-71 PMID: 15368076
  56. Arabidopsis Mutants Selected for Resistance to the Phytotoxin Coronatine Are Male Sterile, Insensitive to Methyl Jasmonate, and Resistant to a Bacterial Pathogen.
    Plant Cell. 1994 May;6(5):751-759 PMID: 12244256
  57. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis.
    Plant Cell. 2007 Jan;19(1):63-73 PMID: 17259259
  58. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.
    Cell. 2006 May 19;125(4):749-60 PMID: 16713565
  59. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  60. Sequence motifs for calmodulin recognition.
    FASEB J. 1997 Apr;11(5):331-40 PMID: 9141499
  61. A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin.
    J Biol Chem. 2003 Nov 14;278(46):45248-54 PMID: 12949074
  62. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  63. Microbe-associated molecular patterns (MAMPs) probe plant immunity.
    Curr Opin Plant Biol. 2007 Aug;10(4):335-41 PMID: 17652011
  64. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control.
    Curr Biol. 2007 Jul 3;17(13):1116-22 PMID: 17583510
  65. Differential expression of genes encoding calmodulin-binding proteins in response to bacterial pathogens and inducers of defense responses.
    Plant Mol Biol. 2003 Apr;51(6):803-15 PMID: 12777041
  66. Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis.
    Plant J. 2007 May;50(3):500-13 PMID: 17419843
  67. Calmodulin target database.
    J Struct Funct Genomics. 2000;1(1):8-14 PMID: 12836676
  68. Genes encoding calmodulin-binding proteins in the Arabidopsis genome.
    J Biol Chem. 2002 Mar 22;277(12):9840-52 PMID: 11782485
  69. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  70. Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant.
    Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7819-24 PMID: 9636234
  71. Characterization of the basic amphiphilic alpha-helix calmodulin-binding domain of a 61.5 kDa tobacco calmodulin-binding protein.
    Biochemistry. 1997 Feb 25;36(8):2025-9 PMID: 9047300
  72. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  73. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  74. Bacterial disease resistance in Arabidopsis through flagellin perception.
    Nature. 2004 Apr 15;428(6984):764-7 PMID: 15085136
  75. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19613-8 PMID: 18042724
  76. Mlo, a modulator of plant defense and cell death, is a novel calmodulin-binding protein. Isolation and characterization of a rice Mlo homologue.
    J Biol Chem. 2002 May 31;277(22):19304-14 PMID: 11904292
  77. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family.
    Plant Cell. 2002 Jan;14(1):275-86 PMID: 11826312
  78. A novel target recognition revealed by calmodulin in complex with Ca2+-calmodulin-dependent kinase kinase.
    Nat Struct Biol. 1999 Sep;6(9):819-24 PMID: 10467092
  79. The PredictProtein server.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W321-6 PMID: 15215403
  80. Loss of a callose synthase results in salicylic acid-dependent disease resistance.
    Science. 2003 Aug 15;301(5635):969-72 PMID: 12920300
  81. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants.
    Cell Host Microbe. 2007 May 17;1(3):175-85 PMID: 18005697
  82. Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity.
    Plant Cell. 2007 Mar;19(3):1081-95 PMID: 17384171
  83. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis.
    Plant Physiol. 2004 Jun;135(2):1113-28 PMID: 15181213
  84. MAP kinase signalling cascade in Arabidopsis innate immunity.
    Nature. 2002 Feb 28;415(6875):977-83 PMID: 11875555
  85. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3292-7 PMID: 10077677
Article Info
Journal
PLoS pathogens
Abbr.
PLoS Pathog
ISSN
1553-7374
Published
2009-02-00
Epub
2009-00-13
Pages
e1000301
Language
English
Region
United States
NLM ID
101238921
PMCID
PMC2633612
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com