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PMID: 15598806 Published · ppublish English Journal Article

Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato.

The Plant cell ·Vol. 17 ·No. 1 ·2005-01-00 ·Pages 295-310

Rowland O, Ludwig AA, Merrick CJ, Baillieul F, Tracy FE, Durrant WE, Fritz-Laylin L, Nekrasov V, Sjölander K, Yoshioka H, Jones JD

Abstract

Tomato (Lycopersicon esculentum) Cf genes confer resistance to the fungal pathogen Cladosporium fulvum through recognition of secreted avirulence (Avr) peptides. Plant defense responses, including rapid alterations in gene expression, are immediately activated upon perception of the pathogen. Previously, we identified a collection of Avr9/Cf-9 rapidly (15 to 30 min) elicited (ACRE) genes from tobacco (Nicotiana tabacum). Many of the ACRE genes encode putative signaling components and thus may play pivotal roles in the initial development of the defense response. To assess the requirement of 42 of these genes in the hypersensitive response (HR) induced by Cf-9/Avr9 or by Cf-4/Avr4, we used virus-induced gene silencing (VIGS) in N. benthamiana. Three genes were identified that when silenced compromised the Cf-mediated HR. We further characterized one of these genes, which encodes a Ser/Thr protein kinase called Avr9/Cf-9 induced kinase 1 (ACIK1). ACIK1 mRNA was rapidly upregulated in tobacco and tomato upon elicitation by Avr9 and by wounding. Silencing of ACIK1 in tobacco resulted in a reduced HR that correlated with loss of ACIK1 transcript. Importantly, ACIK1 was found to be required for Cf-9/Avr9- and Cf-4/Avr4-mediated HRs but not for the HR or resistance mediated by other resistance/Avr systems, such as Pto/AvrPto, Rx/Potato virus X, or N/Tobacco mosaic virus. Moreover, VIGS of LeACIK1 in tomato decreased Cf-9-mediated resistance to C. fulvum, showing the importance of ACIK1 in disease resistance.

MeSH Terms
DNA Virus Infections/genetics Fungal Proteins/genetics,pharmacology Gene Expression Regulation, Plant/drug effects,genetics Gene Silencing/drug effects Genes, Plant/genetics Immunity, Innate/genetics Lycopersicon esculentum/enzymology,genetics,microbiology Molecular Sequence Data Plant Diseases/genetics,microbiology Plant Proteins/genetics,isolation & purification,metabolism Plant Viruses/genetics Protein Serine-Threonine Kinases/genetics,isolation & purification,metabolism RNA, Messenger/metabolism,pharmacology Time Factors Tobacco/enzymology,genetics,microbiology Up-Regulation/drug effects,physiology
Chemicals
AVR4 protein, Cladosporium fulvum Fungal Proteins Plant Proteins RNA, Messenger AVR9 protein, Cladosporium fulvum Protein Serine-Threonine Kinases
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Rowland Owen
Sainsbury Laboratory, John Ines Centre, Norwich NR4 7UH, United Kingdom.
Ludwig Andrea A
Merrick Catherine J
Baillieul Fabienne
Tracy Frances E
Durrant Wendy E
Fritz-Laylin Lillian
Nekrasov Vladimir
Sjölander Kimmen
Yoshioka Hirofumi
Jones Jonathan D G
References (70)
70 references, click to expand
  1. Novel protein kinase of Arabidopsis thaliana (APK1) that phosphorylates tyrosine, serine and threonine.
    Plant Mol Biol. 1992 Nov;20(4):653-62 PMID: 1450380
  2. RFLP linkage analysis of the Cf-4 and Cf-9 genes for resistance toCladosporium fulvum in tomato.
    Theor Appl Genet. 1994 Aug;88(6-7):691-700 PMID: 24186164
  3. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8807-14 PMID: 10922039
  4. Comprehensive transcript profiling of Pto- and Prf-mediated host defense responses to infection by Pseudomonas syringae pv. tomato.
    Plant J. 2002 Nov;32(3):299-315 PMID: 12410809
  5. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling.
    Science. 2004 Mar 5;303(5663):1516-9 PMID: 15001779
  6. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily.
    Plant J. 2001 Apr;26(1):101-12 PMID: 11359614
  7. A serine/threonine protein kinase gene isolated by an in vivo binding procedure using the Arabidopsis floral homeotic gene product, AGAMOUS.
    Plant Cell Physiol. 1997 Mar;38(3):248-58 PMID: 9150601
  8. SCF and Cullin/Ring H2-based ubiquitin ligases.
    Annu Rev Cell Dev Biol. 1999;15:435-67 PMID: 10611969
  9. Over-expression of a scopoletin glucosyltransferase in Nicotiana tabacum leads to precocious lesion formation during the hypersensitive response to tobacco mosaic virus but does not affect virus resistance.
    Plant Mol Biol. 2004 Jan;54(1):137-46 PMID: 15159640
  10. The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response.
    Cell. 1995 Dec 15;83(6):925-35 PMID: 8521516
  11. Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants.
    Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10865-9 PMID: 12119413
  12. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis.
    Science. 2002 Apr 26;296(5568):744-7 PMID: 11976458
  13. Rapid Avr9- and Cf-9 -dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses.
    Plant Cell. 1999 Feb;11(2):273-87 PMID: 9927644
  14. Virus-induced gene silencing in tomato.
    Plant J. 2002 Sep;31(6):777-86 PMID: 12220268
  15. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance.
    EMBO J. 2003 Nov 3;22(21):5690-9 PMID: 14592968
  16. The Rx gene from potato controls separate virus resistance and cell death responses.
    Plant Cell. 1999 May;11(5):781-92 PMID: 10330465
  17. The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9
    Plant Cell. 1998 Aug;10(8):1251-66 PMID: 9707527
  18. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis.
    Plant Physiol. 2002 Jun;129(2):661-77 PMID: 12068110
  19. An EDS1 orthologue is required for N-mediated resistance against tobacco mosaic virus.
    Plant J. 2002 Mar;29(5):569-79 PMID: 11874570
  20. Size constraints for targeting post-transcriptional gene silencing and for RNA-directed methylation in Nicotiana benthamiana using a potato virus X vector.
    Plant J. 2001 Feb;25(4):417-25 PMID: 11260498
  21. Comparison of the hypersensitive response induced by the tomato Cf-4 and Cf-9 genes in Nicotiana spp.
    Mol Plant Microbe Interact. 2000 Apr;13(4):465-9 PMID: 10755310
  22. Flagellin perception: a paradigm for innate immunity.
    Trends Plant Sci. 2002 Jun;7(6):251-6 PMID: 12049921
  23. cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles.
    Plant Cell. 2000 Jun;12(6):963-77 PMID: 10852940
  24. No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum.
    Mol Plant Microbe Interact. 2001 Jul;14(7):867-76 PMID: 11437260
  25. Drosophila innate immunity: an evolutionary perspective.
    Nat Immunol. 2002 Feb;3(2):121-6 PMID: 11812988
  26. Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum.
    Philos Trans R Soc Lond B Biol Sci. 1998 Sep 29;353(1374):1413-24 PMID: 9800204
  27. Ubiquitin, proteasomes, and the regulation of intracellular protein degradation.
    Curr Opin Cell Biol. 1995 Apr;7(2):215-23 PMID: 7612274
  28. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  29. Recent advances in the study of tomato Cf resistance genes.
    Mol Plant Pathol. 2002 Jul 1;3(4):277-82 PMID: 20569335
  30. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.
    Nucleic Acids Res. 2002 Jul 15;30(14):3059-66 PMID: 12136088
  31. Understanding the functions of plant disease resistance proteins.
    Annu Rev Plant Biol. 2003;54:23-61 PMID: 14502984
  32. Total silencing by intron-spliced hairpin RNAs.
    Nature. 2000 Sep 21;407(6802):319-20 PMID: 11014180
  33. Identification of Two Genes Required in Tomato for Full Cf-9-Dependent Resistance to Cladosporium fulvum.
    Plant Cell. 1994 Mar;6(3):361-374 PMID: 12244240
  34. Fast forward genetics based on virus-induced gene silencing.
    Curr Opin Plant Biol. 1999 Apr;2(2):109-13 PMID: 10322199
  35. Resistance gene-dependent activation of a calcium-dependent protein kinase in the plant defense response.
    Plant Cell. 2000 May;12(5):803-16 PMID: 10810151
  36. Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening.
    Genetics. 1996 Jun;143(2):973-82 PMID: 8725243
  37. Map-based cloning of a protein kinase gene conferring disease resistance in tomato.
    Science. 1993 Nov 26;262(5138):1432-6 PMID: 7902614
  38. An Arabidopsis thaliana root-specific kinase homolog is induced by dehydration, ABA, and NaCl.
    Plant J. 1995 Jul;8(1):37-43 PMID: 7655506
  39. 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
  40. CDPK-mediated signalling pathways: specificity and cross-talk.
    J Exp Bot. 2004 Jan;55(395):181-8 PMID: 14623901
  41. Pfam: multiple sequence alignments and HMM-profiles of protein domains.
    Nucleic Acids Res. 1998 Jan 1;26(1):320-2 PMID: 9399864
  42. Construction of an intron-containing marker gene: splicing of the intron in transgenic plants and its use in monitoring early events in Agrobacterium-mediated plant transformation.
    Mol Gen Genet. 1990 Jan;220(2):245-50 PMID: 2325623
  43. 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
  44. SCF(HOS) ubiquitin ligase mediates the ligand-induced down-regulation of the interferon-alpha receptor.
    EMBO J. 2003 Oct 15;22(20):5480-90 PMID: 14532120
  45. Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis.
    Plant Cell. 2004 Apr;16(4):897-907 PMID: 15020743
  46. Technical Advance. Tobacco rattle virus as a vector for analysis of gene function by silencing.
    Plant J. 2001 Jan;25(2):237-45 PMID: 11169199
  47. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis.
    Mol Cell. 2000 Jun;5(6):1003-11 PMID: 10911994
  48. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene.
    Nature. 1994 Jan 27;367(6461):384-6 PMID: 8114941
  49. PLANT PROTEIN SERINE/THREONINE KINASES: Classification and Functions.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:97-131 PMID: 15012205
  50. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.
    Plant Cell. 2004 May;16(5):1220-34 PMID: 15105442
  51. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9.
    Plant Cell. 1997 Dec;9(12):2209-24 PMID: 9437864
  52. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21.
    Science. 1995 Dec 15;270(5243):1804-6 PMID: 8525370
  53. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato.
    Plant J. 2003 Dec;36(6):905-17 PMID: 14675454
  54. Scopoletin expression in elicitor-treated and tobacco mosaic virus-infected tobacco plants.
    Physiol Plant. 2002 Jun;115(2):228-235 PMID: 12060240
  55. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  56. Toll-like receptors: key mediators of microbe detection.
    Curr Opin Immunol. 2002 Feb;14(1):103-10 PMID: 11790539
  57. Phylogenetic inference in protein superfamilies: analysis of SH2 domains.
    Proc Int Conf Intell Syst Mol Biol. 1998;6:165-74 PMID: 9783222
  58. CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence.
    EMBO J. 2004 May 19;23(10):2156-65 PMID: 15131698
  59. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10763-8 PMID: 11526204
  60. Function of a mitogen-activated protein kinase pathway in N gene-mediated resistance in tobacco.
    Plant J. 2003 Feb;33(4):719-31 PMID: 12609044
  61. Virus-induced silencing of WIPK and SIPK genes reduces resistance to a bacterial pathogen, but has no effect on the INF1-induced hypersensitive response (HR) in Nicotiana benthamiana.
    Mol Genet Genomics. 2003 Aug;269(5):583-91 PMID: 12838412
  62. AvrPto-dependent Pto-interacting proteins and AvrPto-interacting proteins in tomato.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8836-40 PMID: 10922043
  63. Toll-like receptors: critical proteins linking innate and acquired immunity.
    Nat Immunol. 2001 Aug;2(8):675-80 PMID: 11477402
  64. Molecular cloning of two novel protein kinase genes from Arabidopsis thaliana.
    Biochim Biophys Acta. 1993 Oct 19;1216(1):9-14 PMID: 8218420
  65. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases.
    Plant Physiol. 1993 Sep;103(1):91-6 PMID: 8208859
  66. K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction.
    Plant J. 1999 Aug;19(4):453-62 PMID: 10504567
  67. A High-Affinity Binding Site for the AVR9 Peptide Elicitor of Cladosporium fulvum Is Present on Plasma Membranes of Tomato and Other Solanaceous Plants.
    Plant Cell. 1996 May;8(5):929-938 PMID: 12239406
  68. Virus-induced gene silencing in plants.
    Methods. 2003 Aug;30(4):296-303 PMID: 12828943
  69. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4985-90 PMID: 10781109
  70. Calcium-dependent protein kinases play an essential role in a plant defence response.
    EMBO J. 2001 Oct 15;20(20):5556-67 PMID: 11597999
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.104.026013
Published
2005-01-00
Epub
2004-00-14
Pages
295-310
Language
English
Region
England
NLM ID
9208688
PMCID
PMC544506
Subset
IM
Databases
GENBANK
AAL07094, AF332960, AY220481
RefSeq
NP_198408
External Links
PubMed source DOI: 10.1105/tpc.104.026013 PMC Full Text View journal details
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