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PMID: 23335625 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis.

Plant physiology ·Vol. 161 ·No. 3 ·2013-03-00 ·Pages 1433-44

Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA

Abstract

A common response by plants to fungal attack is deposition of callose, a (1,3)-β-glucan polymer, in the form of cell wall thickenings called papillae, at site of wall penetration. While it has been generally believed that the papillae provide a structural barrier to slow fungal penetration, this idea has been challenged in recent studies of Arabidopsis (Arabidopsis thaliana), where fungal resistance was found to be independent of callose deposition. To the contrary, we show that callose can strongly support penetration resistance when deposited in elevated amounts at early time points of infection. We generated transgenic Arabidopsis lines that express POWDERY MILDEW RESISTANT4 (PMR4), which encodes a stress-induced callose synthase, under the control of the constitutive 35S promoter. In these lines, we detected callose synthase activity that was four times higher than that in wild-type plants 6 h post inoculation with the virulent powdery mildew Golovinomyces cichoracearum. The callose synthase activity was correlated with enlarged callose deposits and the focal accumulation of green fluorescent protein-tagged PMR4 at sites of attempted fungal penetration. We observed similar results from infection studies with the nonadapted powdery mildew Blumeria graminis f. sp. hordei. Haustoria formation was prevented in resistant transgenic lines during both types of powdery mildew infection, and neither the salicylic acid-dependent nor jasmonate-dependent pathways were induced. We present a schematic model that highlights the differences in callose deposition between the resistant transgenic lines and the susceptible wild-type plants during compatible and incompatible interactions between Arabidopsis and powdery mildew.

MeSH Terms
Adaptation, Physiological Arabidopsis/genetics,immunology,microbiology Arabidopsis Proteins/genetics,metabolism Ascomycota/physiology Cyclopentanes/metabolism Disease Resistance/immunology Gene Expression Profiling Gene Expression Regulation, Plant Genes, Plant/genetics Glucans/metabolism Green Fluorescent Proteins/metabolism Models, Biological Oxylipins/metabolism Phenotype Plant Diseases/immunology,microbiology Plants, Genetically Modified Salicylic Acid/metabolism Time Factors Transcription, Genetic
Chemicals
Arabidopsis Proteins Cyclopentanes Glucans Oxylipins Green Fluorescent Proteins jasmonic acid callose Salicylic Acid
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ellinger Dorothea
Phytopathology and Biochemistry, Biocenter Klein Flottbek, University of Hamburg, 22609 Hamburg, Germany.
Naumann Marcel
Falter Christian
Zwikowics Claudia
Jamrow Torsten
Manisseri Chithra
Somerville Shauna C
Voigt Christian A
References (31)
31 references, click to expand
  1. Ultrastructure of the Host-Pathogen Relationship in Entomosporium Leaf Spot Disease of Photinia.
    Int J Plant Sci. 2000 Mar;161(2):291-295 PMID: 10777453
  2. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine.
    Proc Natl Acad Sci U S A. 2008 May 13;105(19):7100-5 PMID: 18458331
  3. Tryptophan-derived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant.
    Plant Physiol. 2010 Mar;152(3):1544-61 PMID: 20023151
  4. A comprehensive view on organ-specific callose synthesis in wheat (Triticum aestivum L.): glucan synthase-like gene expression, callose synthase activity, callose quantification and deposition.
    Plant Physiol Biochem. 2006 Apr;44(4):242-7 PMID: 16777426
  5. Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola.
    Plant J. 2008 Apr;54(1):81-92 PMID: 18088307
  6. Conserved requirement for a plant host cell protein in powdery mildew pathogenesis.
    Nat Genet. 2006 Jun;38(6):716-20 PMID: 16732289
  7. Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose.
    Plant J. 2004 Apr;38(1):119-30 PMID: 15053765
  8. Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis.
    Plant J. 2004 Dec;40(5):633-46 PMID: 15546348
  9. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1.
    Proc Natl Acad Sci U S A. 2012 Jul 10;109(28):11443-8 PMID: 22733775
  10. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis.
    Cell Res. 2012 Feb;22(2):413-24 PMID: 21826108
  11. 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
  12. The role of abscisic acid in plant-pathogen interactions.
    Curr Opin Plant Biol. 2005 Aug;8(4):409-14 PMID: 15939661
  13. Callose deposition: a multifaceted plant defense response.
    Mol Plant Microbe Interact. 2011 Feb;24(2):183-93 PMID: 20955078
  14. An Arabidopsis Callose Synthase, GSL5, Is Required for Wound and Papillary Callose Formation.
    Plant Cell. 2003 Nov;15(11):2503-13 PMID: 14555698
  15. Plant innate immunity: perception of conserved microbial signatures.
    Annu Rev Plant Biol. 2012;63:451-82 PMID: 22404464
  16. Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis.
    Plant Cell. 2008 May;20(5):1289-302 PMID: 18460606
  17. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  18. Fresh insights into processes of nonhost resistance.
    Curr Opin Plant Biol. 2003 Aug;6(4):351-7 PMID: 12873530
  19. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana.
    Plant J. 1999 May;18(3):277-84 PMID: 10377993
  20. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration.
    Plant Cell. 2006 Mar;18(3):731-46 PMID: 16473969
  21. A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation.
    Fungal Genet Biol. 1999 Feb;26(1):19-32 PMID: 10072317
  22. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  23. Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3718-23 PMID: 10737809
  24. Hidden robbers: the role of fungal haustoria in parasitism of plants.
    Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7654-5 PMID: 11438718
  25. Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments.
    Plant J. 2009 Mar;57(6):986-99 PMID: 19000165
  26. Systemic Acquired Resistance.
    Plant Cell. 1996 Oct;8(10):1809-1819 PMID: 12239363
  27. 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
  28. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean.
    Plant Cell. 1991 Jan;3(1):49-59 PMID: 1824334
  29. The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ROR2 syntaxin-dependent preinvasive basal defense in barley.
    Plant Cell. 2010 Nov;22(11):3831-44 PMID: 21057060
  30. Loss of a callose synthase results in salicylic acid-dependent disease resistance.
    Science. 2003 Aug 15;301(5635):969-72 PMID: 12920300
  31. THE OXIDATIVE BURST IN PLANT DISEASE RESISTANCE.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:251-275 PMID: 15012264
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2013-03-00
Epub
2013-00-18
Pages
1433-44
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3585607
Subset
IM
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