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PMID: 21490299 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane.

Gao Z, Gao Z, Chung EH, Eitas TK, Dangl JL

Abstract

Plants deploy intracellular innate immune receptors to recognize pathogens and initiate disease resistance. These nucleotide-binding, leucine-rich repeat (NB-LRR) proteins are activated by pathogen effector proteins that are delivered into the host cell to suppress host defense responses. Little is known about the sites and mechanisms of NB-LRR activation, but some NB-LRR proteins can function inside the plant nucleus. We demonstrate that RPM1 is activated on the plasma membrane and does not relocalize to the nucleus. An autoactive RPM1(D505V) allele that recapitulates key features of normal RPM1 activation also resides on the plasma membrane. There is no detectable relocalization of activated RPM1 to the nucleus. Hindering potential nuclear entry of RPM1-Myc did not affect either its effector-triggered hypersensitive-response (HR) cell death or its disease resistance functions, further suggesting that nuclear translocation is not required for RPM1 function. RPM1 tethered onto the plasma membrane with a dual acylated N-terminal epitope tag retained the ability to mediate HR, consistent with this RPM1 function being activated on the plasma membrane. Plant NB-LRR proteins can thus function at various locations in the cell.

MeSH Terms
Arabidopsis/genetics,immunology Arabidopsis Proteins/immunology,metabolism Cell Membrane/metabolism Genetic Vectors/genetics Immunity, Innate/genetics Leucine-Rich Repeat Proteins Microscopy, Confocal Plant Diseases/immunology Proteins/immunology,metabolism
Chemicals
Arabidopsis Proteins Leucine-Rich Repeat Proteins Proteins RPM1 protein, Arabidopsis
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Gao Zhiyong
Department of Biology, and Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, NC 27599, USA.
Gao Zhiyoug
Chung Eui-Hwan
Eitas Timothy K
Dangl Jeffery L
References (43)
43 references, click to expand
  1. Elicitor-mediated oligomerization of the tobacco N disease resistance protein.
    Plant Cell. 2006 Feb;18(2):491-501 PMID: 16387833
  2. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae.
    Cell. 2000 May 12;101(4):353-63 PMID: 10830163
  3. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.
    Proc Natl Acad Sci U S A. 2006 Jun 6;103(23):8888-93 PMID: 16731621
  4. AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana.
    Plant Mol Biol. 1997 May;34(1):175-80 PMID: 9177324
  5. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis.
    PLoS Pathog. 2010 Nov 18;6(11):e1001202 PMID: 21124938
  6. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4.
    Cell. 2003 Feb 7;112(3):369-77 PMID: 12581526
  7. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15849-54 PMID: 9861059
  8. A defect in the nuclear translocation of CIITA causes a form of type II bare lymphocyte syndrome.
    Immunity. 1999 Feb;10(2):163-71 PMID: 10072069
  9. Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains.
    Plant Cell. 2010 Dec;22(12):4195-215 PMID: 21177483
  10. Large-scale structure-function analysis of the Arabidopsis RPM1 disease resistance protein.
    Plant Cell. 2002 Feb;14(2):435-50 PMID: 11884685
  11. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense.
    Curr Biol. 2007 Dec 4;17(23):2023-9 PMID: 17997306
  12. The HSP90-SGT1 chaperone complex for NLR immune sensors.
    Annu Rev Plant Biol. 2009;60:139-64 PMID: 19014346
  13. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.
    Science. 2007 Feb 23;315(5815):1098-103 PMID: 17185563
  14. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance.
    Cell. 2003 Feb 7;112(3):379-89 PMID: 12581527
  15. Transcriptional scaffold: CIITA interacts with NF-Y, RFX, and CREB to cause stereospecific regulation of the class II major histocompatibility complex promoter.
    Mol Cell Biol. 2000 Aug;20(16):6051-61 PMID: 10913187
  16. NLRs at the intersection of cell death and immunity.
    Nat Rev Immunol. 2008 May;8(5):372-9 PMID: 18362948
  17. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis.
    Plant Cell. 2009 Aug;21(8):2503-16 PMID: 19700630
  18. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis.
    Cell. 2002 Mar 22;108(6):743-54 PMID: 11955429
  19. A high-throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana.
    Plant J. 2001 Nov;28(4):475-81 PMID: 11737784
  20. RAR1 positively controls steady state levels of barley MLA resistance proteins and enables sufficient MLA6 accumulation for effective resistance.
    Plant Cell. 2004 Dec;16(12):3480-95 PMID: 15548741
  21. RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function.
    Plant Cell. 2010 Dec;22(12):4176-94 PMID: 21169509
  22. Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis.
    Plant Cell. 2008 May;20(5):1346-62 PMID: 18502848
  23. A novel role for the TIR domain in association with pathogen-derived elicitors.
    PLoS Biol. 2007 Mar;5(3):e68 PMID: 17298188
  24. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1.
    Plant Cell. 2004 Oct;16(10):2822-35 PMID: 15361584
  25. To nibble at plant resistance proteins.
    Science. 2009 May 8;324(5928):744-6 PMID: 19423813
  26. NB-LRR proteins: pairs, pieces, perception, partners, and pathways.
    Curr Opin Plant Biol. 2010 Aug;13(4):472-7 PMID: 20483655
  27. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system.
    Cell Host Microbe. 2009 Jul 23;6(1):10-21 PMID: 19616762
  28. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance.
    Science. 1995 Aug 11;269(5225):843-6 PMID: 7638602
  29. The NOD2-RICK complex signals from the plasma membrane.
    J Biol Chem. 2007 May 18;282(20):15197-207 PMID: 17355968
  30. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming.
    Cell Host Microbe. 2008 Mar 13;3(3):126-35 PMID: 18329612
  31. Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death.
    EMBO J. 2002 Sep 2;21(17):4511-9 PMID: 12198153
  32. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity.
    Cell Host Microbe. 2010 May 20;7(5):362-75 PMID: 20478538
  33. Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation.
    Cell Host Microbe. 2011 Mar 17;9(3):200-211 PMID: 21402359
  34. GTP binding by class II transactivator: role in nuclear import.
    Science. 1999 Aug 27;285(5432):1402-5 PMID: 10464099
  35. Plant immunity: towards an integrated view of plant-pathogen interactions.
    Nat Rev Genet. 2010 Aug;11(8):539-48 PMID: 20585331
  36. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants.
    Cell Host Microbe. 2011 Feb 17;9(2):125-36 PMID: 21320695
  37. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  38. Nod1 and Nod2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry.
    Nat Immunol. 2010 Jan;11(1):55-62 PMID: 19898471
  39. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death.
    Cell Host Microbe. 2011 Mar 17;9(3):187-199 PMID: 21402358
  40. Structure-function analysis of the NB-ARC domain of plant disease resistance proteins.
    J Exp Bot. 2008;59(6):1383-97 PMID: 18390848
  41. Resistance proteins: molecular switches of plant defence.
    Curr Opin Plant Biol. 2006 Aug;9(4):383-90 PMID: 16713729
  42. Arabidopsis is susceptible to infection by a downy mildew fungus.
    Plant Cell. 1990 May;2(5):437-45 PMID: 2152169
  43. Prf immune complexes of tomato are oligomeric and contain multiple Pto-like kinases that diversify effector recognition.
    Plant J. 2010 Feb 1;61(3):507-18 PMID: 19919571
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-05-03
Epub
2011-00-13
Pages
7619-24
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3088580
Subset
IM
Corrections
ErratumIn
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