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PMID: 12566578 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

HLM1, an essential signaling component in the hypersensitive response, is a member of the cyclic nucleotide-gated channel ion channel family.

The Plant cell ·Vol. 15 ·No. 2 ·2003-02-00 ·Pages 365-79

Balagué C, Lin B, Alcon C, Flottes G, Malmström S, Köhler C, Neuhaus G, Pelletier G, Gaymard F, Roby D

Abstract

The hypersensitive response (HR) in plants is a programmed cell death that is commonly associated with disease resistance. A novel mutation in Arabidopsis, hlm1, which causes aberrant regulation of cell death, manifested by a lesion-mimic phenotype and an altered HR, segregated as a single recessive allele. Broad-spectrum defense mechanisms remained functional or were constitutive in the mutant plants, which also exhibited increased resistance to a virulent strain of Pseudomonas syringae pv tomato. In response to avirulent strains of the same pathogen, the hlm1 mutant showed differential abilities to restrict bacterial growth, depending on the avirulence gene expressed by the pathogen. The HLM1 gene encodes a cyclic nucleotide-gated channel, CNGC4. Preliminary study of the HLM1/CNGC4 gene pro-duct in Xenopus oocytes (inside-out patch-clamp technique) showed that CNGC4 is permeable to both K(+) and Na(+) and is activated by both cGMP and cAMP. HLM1 gene expression is induced in response to pathogen infection and some pathogen-related signals. Thus, HLM1 might constitute a common downstream component of the signaling pathways leading to HR/resistance.

MeSH Terms
Alleles Amino Acid Sequence Animals Apoptosis/genetics Arabidopsis/genetics,metabolism,microbiology Arabidopsis Proteins/genetics,metabolism Cloning, Molecular Cyclic AMP/pharmacology Cyclic GMP/pharmacology Cyclic Nucleotide-Gated Cation Channels Female Gene Expression Regulation, Plant Immunity, Innate/genetics Ion Channels/genetics,metabolism Molecular Sequence Data Mutation Oocytes/drug effects,physiology Patch-Clamp Techniques Phenotype Phylogeny Plant Diseases/genetics,microbiology Potassium/metabolism Pseudomonas/growth & development Signal Transduction/genetics Sodium/metabolism Xenopus
Chemicals
Arabidopsis Proteins Cyclic Nucleotide-Gated Cation Channels Ion Channels Sodium Cyclic AMP Cyclic GMP Potassium
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Balagué Claudine
Laboratoire de Biologie Moléculaire des Relations Plantes-Microorganismes, Unité Mixte de Recherche Centre National de la Recherche Scientifique/Institut National de la Recherche Agronomique 215, BP 27, 31326 Castanet-Tolosan cedex, France.
Lin Baiqing
Alcon Carine
Flottes Guylaine
Malmström Susanna
Köhler Claudia
Neuhaus Gunther
Pelletier Georges
Gaymard Frédéric
Roby Dominique
References (66)
66 references, click to expand
  1. 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
  2. Overexpression of Pto activates defense responses and confers broad resistance.
    Plant Cell. 1999 Jan;11(1):15-29 PMID: 9878629
  3. Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants.
    Cell. 1993 Jul 2;73(7):1255-66 PMID: 8324821
  4. 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 PMID: 10488236
  5. Involvement of plasma membrane calcium influx in bacterial induction of the k/h and hypersensitive responses in tobacco.
    Plant Physiol. 1990 Jan;92(1):215-21 PMID: 16667249
  6. The jasmonate signal pathway.
    Plant Cell. 2002;14 Suppl:S153-64 PMID: 12045275
  7. Identification of new early markers of the hypersensitive response in Arabidopsis thaliana(1).
    FEBS Lett. 1999 Oct 8;459(2):149-53 PMID: 10518009
  8. Environmentally sensitive, SA-dependent defense responses in the cpr22 mutant of Arabidopsis.
    Plant J. 2001 May;26(4):447-59 PMID: 11439131
  9. Genes controlling expression of defense responses in Arabidopsis--2001 status.
    Curr Opin Plant Biol. 2001 Aug;4(4):301-8 PMID: 11418339
  10. A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death.
    Cell. 1997 Mar 7;88(5):685-94 PMID: 9054508
  11. Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4800-5 PMID: 9114072
  12. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  13. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  14. Expression of a truncated tobacco NtCBP4 channel in transgenic plants and disruption of the homologous Arabidopsis CNGC1 gene confer Pb2+ tolerance.
    Plant J. 2000 Nov;24(4):533-42 PMID: 11115134
  15. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance.
    Plant Cell. 1994 Dec;6(12):1845-57 PMID: 7866028
  16. Arabidopsis mutants simulating disease resistance response.
    Cell. 1994 May 20;77(4):565-77 PMID: 8187176
  17. Preexisting systemic acquired resistance suppresses hypersensitive response-associated cell death in Arabidopsis hrl1 mutant.
    Plant Physiol. 2002 Apr;128(4):1234-44 PMID: 11950972
  18. Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging.
    Plant J. 1993 Aug;4(2):327-41 PMID: 8220484
  19. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance.
    Cell. 2000 Dec 22;103(7):1111-20 PMID: 11163186
  20. 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 PMID: 11532166
  21. Characterization of a new Arabidopsis mutant exhibiting enhanced disease resistance.
    Mol Plant Microbe Interact. 1999 Dec;12(12):1053-63 PMID: 10624014
  22. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance.
    Plant Cell. 1997 Sep;9(9):1573-84 PMID: 9338960
  23. A role for jasmonate in pathogen defense of Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7209-14 PMID: 9618564
  24. FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants.
    Nucleic Acids Res. 2002 Jan 1;30(1):94-7 PMID: 11752264
  25. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  26. Activation of a Bean Chitinase Promoter in Transgenic Tobacco Plants by Phytopathogenic Fungi.
    Plant Cell. 1990 Oct;2(10):999-1007 PMID: 12354948
  27. Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions.
    Cell. 1994 May 20;77(4):551-63 PMID: 8187175
  28. Structure and function of cyclic nucleotide-gated channels.
    Annu Rev Neurosci. 1996;19:235-63 PMID: 8833443
  29. Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels.
    Plant Physiol. 2002 Feb;128(2):400-10 PMID: 11842144
  30. The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes.
    EMBO J. 1997 Jun 2;16(11):3207-18 PMID: 9214637
  31. NF-kappaB and the innate immune response.
    Curr Opin Immunol. 2000 Feb;12(1):52-8 PMID: 10679399
  32. Toll signaling pathways in the innate immune response.
    Curr Opin Immunol. 2000 Feb;12(1):13-9 PMID: 10679407
  33. Genetically engineered broad-spectrum disease resistance in tomato.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10300-5 PMID: 9707642
  34. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  35. hxc2, an Arabidopsis mutant with an altered hypersensitive response to Xanthomonas campestris pv. campestris.
    Plant J. 2000 Dec;24(6):749-61 PMID: 11135109
  36. Resistance response physiology and signal transduction.
    Curr Opin Plant Biol. 1998 Aug;1(4):305-10 PMID: 10066609
  37. Characterization of a calmodulin-binding transporter from the plasma membrane of barley aleurone.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1944-9 PMID: 9465122
  38. The Arabidopsis gain-of-function mutant dll1 spontaneously develops lesions mimicking cell death associated with disease.
    Plant J. 2002 Apr;30(1):61-70 PMID: 11967093
  39. Salicylate-independent lesion formation in Arabidopsis lsd mutants.
    Mol Plant Microbe Interact. 1997 Jul;10(5):531-6 PMID: 9204559
  40. A new elicitor of the hypersensitive response in tobacco: a fungal glycoprotein elicits cell death, expression of defence genes, production of salicylic acid, and induction of systemic acquired resistance.
    Plant J. 1995 Oct;8(4):551-60 PMID: 7496401
  41. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9323-8 PMID: 10900264
  42. The hypersensitive response and the induction of cell death in plants.
    Cell Death Differ. 1997 Dec;4(8):671-83 PMID: 16465279
  43. PROGRAMMED CELL DEATH IN PLANT-PATHOGEN INTERACTIONS.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:525-545 PMID: 15012273
  44. 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
  45. 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
  46. How the olfactory system makes sense of scents.
    Nature. 2001 Sep 13;413(6852):211-8 PMID: 11557990
  47. Characterisation of a novel gene family of putative cyclic nucleotide- and calmodulin-regulated ion channels in Arabidopsis thaliana.
    Plant J. 1999 Apr;18(1):97-104 PMID: 10341447
  48. Cyclic nucleotide-gated cation channels molecular diversity, structure, and cellular functions.
    Trends Cardiovasc Med. 1996 Nov;6(8):274-80 PMID: 21232308
  49. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response.
    Curr Biol. 1996 Apr 1;6(4):427-37 PMID: 8723347
  50. Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel.
    Plant Physiol. 1999 Nov;121(3):753-61 PMID: 10557223
  51. Generalized Induction of Defense Responses in Bean Is Not Correlated with the Induction of the Hypersensitive Reaction.
    Plant Cell. 1993 Jan;5(1):49-56 PMID: 12271015
  52. Phylogenetic relationships within cation transporter families of Arabidopsis.
    Plant Physiol. 2001 Aug;126(4):1646-67 PMID: 11500563
  53. Expression of a cloned plant K+ channel in Xenopus oocytes: analysis of macroscopic currents.
    Plant J. 1995 Feb;7(2):321-32 PMID: 7704050
  54. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent.
    Plant Cell. 1999 Feb;11(2):191-206 PMID: 9927638
  55. NDR1, a pathogen-induced component required for Arabidopsis disease resistance.
    Science. 1997 Dec 12;278(5345):1963-5 PMID: 9395402
  56. 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
  57. A humidity-sensitive Arabidopsis copine mutant exhibits precocious cell death and increased disease resistance.
    Plant Cell. 2001 Oct;13(10):2225-40 PMID: 11595798
  58. A breakdown in defense signaling.
    Plant Cell. 2002;14 Suppl:S5-8 PMID: 12045266
  59. Dead cells do tell tales.
    Curr Opin Plant Biol. 1998 Dec;1(6):480-5 PMID: 10066637
  60. Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity.
    Plant J. 2000 Dec;24(5):569-82 PMID: 11123796
  61. Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture.
    Eur J Biochem. 2000 Aug;267(16):5005-13 PMID: 10931182
  62. Visual transduction in Drosophila.
    Nature. 2001 Sep 13;413(6852):186-93 PMID: 11557987
  63. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10306-11 PMID: 9707643
  64. 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 PMID: 11149948
  65. A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens.
    Plant J. 2001 Mar;25(5):563-74 PMID: 11309146
  66. 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 PMID: 10978297
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.006999
Published
2003-02-00
Pages
365-79
Language
English
Region
England
NLM ID
9208688
PMCID
PMC141207
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.006999 PMC Full Text View journal details
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