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PMID: 19706796 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The Colletotrichum orbiculare SSD1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway.

The Plant cell ·Vol. 21 ·No. 8 ·2009-08-00 ·Pages 2517-26

Tanaka S, Ishihama N, Yoshioka H, Huser A, O'Connell R, Tsuji G, Tsuge S, Kubo Y

Abstract

Plant basal resistance is activated by virulent pathogens in susceptible host plants. A Colletotrichum orbiculare fungal mutant defective in the SSD1 gene, which regulates cell wall composition, is restricted by host basal resistance responses. Here, we identified the Nicotiana benthamiana signaling pathway involved in basal resistance by silencing the defense-related genes required for restricting the growth of the C. orbiculare mutant. Only silencing of MAP Kinase Kinase2 or of both Salicylic Acid Induced Protein Kinase (SIPK) and Wound Induced Protein Kinase (WIPK), two mitogen-activated protein (MAP) kinases, allowed the mutant to infect and produce necrotic lesions similar to those of the wild type on inoculated leaves. The fungal mutant penetrated host cells to produce infection hyphae at a higher frequency in SIPK WIPK-silenced plants than in nonsilenced plants, without inducing host cellular defense responses. Immunocomplex kinase assays revealed that SIPK and WIPK were more active in leaves inoculated with mutant fungus than with the wild type, suggesting that induced resistance correlates with MAP kinase activity. Infiltration of heat-inactivated mutant conidia induced both SIPK and WIPK more strongly than did those of the wild type, while conidial exudates of the wild type did not suppress MAP kinase induction by mutant conidia. Therefore, activation of a specific MAP kinase pathway by fungal cell surface components determines the effective level of basal plant resistance.

MeSH Terms
Colletotrichum/genetics,metabolism,physiology Fungal Proteins/genetics,metabolism,physiology Gene Expression Regulation, Plant/genetics,physiology Host-Pathogen Interactions/genetics,physiology Immunity, Innate/genetics,physiology Immunoblotting MAP Kinase Signaling System/genetics,physiology Models, Biological Molecular Sequence Data Plant Diseases/immunology,microbiology Plant Leaves/genetics,metabolism,microbiology Plant Proteins/genetics,metabolism,physiology Plants, Genetically Modified/genetics,metabolism,microbiology Tobacco/genetics,metabolism,microbiology
Chemicals
Fungal Proteins Plant Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Tanaka Shigeyuki
Laboratory of Plant Pathology, Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto 606-8522, Japan.
Ishihama Nobuaki
Yoshioka Hirofumi
Huser Aurélie
O'Connell Richard
Tsuji Gento
Tsuge Seiji
Kubo Yasuyuki
References (29)
29 references, click to expand
  1. A diterpene as an endogenous signal for the activation of defense responses to infection with tobacco mosaic virus and wounding in tobacco.
    Plant Cell. 2003 Apr;15(4):863-73 PMID: 12671083
  2. Saccharomyces cerevisiae SSD1 orthologues are essential for host infection by the ascomycete plant pathogens Colletotrichum lagenarium and Magnaporthe grisea.
    Mol Microbiol. 2007 Jun;64(5):1332-49 PMID: 17542924
  3. Fungal avirulence genes: structure and possible functions.
    Fungal Genet Biol. 1998 Aug;24(3):285-97 PMID: 9756710
  4. The structure and function of a soybean beta-glucan-elicitor-binding protein.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):1029-34 PMID: 9023377
  5. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor.
    Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):11086-91 PMID: 16829581
  6. Establishing compatibility between plants and obligate biotrophic pathogens.
    Curr Opin Plant Biol. 2003 Aug;6(4):320-6 PMID: 12873525
  7. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  8. 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
  9. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  10. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis.
    Proc Natl Acad Sci U S A. 2008 Apr 8;105(14):5638-43 PMID: 18378893
  11. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
  12. MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana.
    Plant Cell. 2008 May;20(5):1390-406 PMID: 18515503
  13. Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance.
    Plant Physiol. 2006 Feb;140(2):681-92 PMID: 16407438
  14. Spore surface glycoproteins of Colletotrichum lindemuthianum are recognized by a monoclonal antibody which inhibits adhesion to polystyrene.
    Microbiology (Reading). 1999 Aug;145 ( Pt 8):1927-1936 PMID: 10463159
  15. Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules.
    Curr Opin Immunol. 2004 Feb;16(1):48-62 PMID: 14734110
  16. Innate immunity in plants and animals: striking similarities and obvious differences.
    Immunol Rev. 2004 Apr;198:249-66 PMID: 15199967
  17. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.
    Plant Cell. 2003 Mar;15(3):706-18 PMID: 12615943
  18. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin.
    Plant J. 1999 May;18(3):265-76 PMID: 10377992
  19. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants.
    Plant Cell. 2004 Dec;16(12):3496-507 PMID: 15548740
  20. Colletotrichum: A model genus for studies on pathology and fungal-plant interactions.
    Fungal Genet Biol. 1999 Jul-Aug;27(2-3):186-98 PMID: 10441444
  21. Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance.
    Plant J. 2007 Dec;52(6):1066-79 PMID: 17908155
  22. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  23. Surface attachment and pre-penetration stage development by plant pathogenic fungi.
    Annu Rev Phytopathol. 2001;39:385-417 PMID: 11701871
  24. How plants recognize pathogens and defend themselves.
    Cell Mol Life Sci. 2007 Nov;64(21):2726-32 PMID: 17876517
  25. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco.
    Proc Natl Acad Sci U S A. 2001 Jan 16;98(2):741-6 PMID: 11209069
  26. Fresh insights into processes of nonhost resistance.
    Curr Opin Plant Biol. 2003 Aug;6(4):351-7 PMID: 12873530
  27. Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes.
    New Phytol. 2006;171(4):699-718 PMID: 16918543
  28. Non-host resistance in plants: new insights into an old phenomenon.
    Mol Plant Pathol. 2005 May 1;6(3):335-45 PMID: 20565662
  29. A Saccharomyces cerevisiae mutant with increased virulence.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2766-70 PMID: 12589024
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2009-08-00
Epub
2009-00-25
Pages
2517-26
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2751964
Subset
IM
Databases
GENBANK
AB079498, AB079499, AB098729, AB245428, AB360635, AB360636, AB373025, AF480487, AF494083, AY368904
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