Home LiteratureArticle Details
PMID: 18267075 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector.

Cell ·Vol. 132 ·No. 3 ·2008-02-08 ·Pages 449-62

Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP

Abstract

Plant innate immunity relies on the recognition of pathogen effector molecules by nucleotide-binding-leucine-rich repeat (NB-LRR) immune receptor families. Previously we have shown the N immune receptor, a member of TIR-NB-LRR family, indirectly recognizes the 50 kDa helicase (p50) domain of Tobacco mosaic virus (TMV) through its TIR domain. We have identified an N receptor-interacting protein, NRIP1, that directly interacts with both N's TIR domain and p50. NRIP1 is a functional rhodanese sulfurtransferase and is required for N to provide complete resistance to TMV. Interestingly, NRIP1 that normally localizes to the chloroplasts is recruited to the cytoplasm and nucleus by the p50 effector. As a consequence, NRIP1 interacts with N only in the presence of the p50 effector. Our findings show that a chloroplastic protein is intimately involved in pathogen recognition. We propose that N's activation requires a prerecognition complex containing the p50 effector and NRIP1.

MeSH Terms
Adaptor Proteins, Signal Transducing/analysis,immunology,metabolism Antigens, Viral/immunology Cell Nucleus/chemistry Chloroplasts/chemistry Cytoplasm/chemistry Immunity, Innate Nuclear Proteins/analysis,immunology,metabolism Nuclear Receptor Interacting Protein 1 Plant Diseases/immunology Plant Proteins/analysis,immunology,metabolism Protein Structure, Tertiary Receptors, Virus/analysis,immunology,metabolism Thiosulfate Sulfurtransferase/metabolism Tobacco/immunology,virology Tobacco Mosaic Virus/immunology Two-Hybrid System Techniques
Chemicals
Adaptor Proteins, Signal Transducing Antigens, Viral Nuclear Proteins Nuclear Receptor Interacting Protein 1 Plant Proteins Receptors, Virus Thiosulfate Sulfurtransferase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Caplan Jeffrey L
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06520, USA.
Mamillapalli Padmavathi
Burch-Smith Tessa M
Czymmek Kirk
Dinesh-Kumar S P
References (42)
42 references, click to expand
  1. Induction of a hypersensitive response by chimeric helicase sequences of tobamoviruses U1 and Ob in N-carrying tobacco.
    Mol Plant Microbe Interact. 2001 Sep;14(9):1086-95 PMID: 11551073
  2. Cysteine 254 can cooperate with active site cysteine 247 in reactivation of 5,5'-dithiobis(2-nitrobenzoic acid)-inactivated rhodanese as determined by site-directed mutagenesis.
    J Biol Chem. 1994 Apr 29;269(17):12414-8 PMID: 8175646
  3. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance.
    Science. 2005 Jun 17;308(5729):1783-6 PMID: 15845874
  4. The SEN1 gene of Arabidopsis is regulated by signals that link plant defence responses and senescence.
    Plant Physiol Biochem. 2005 Oct-Nov;43(10-11):997-1005 PMID: 16325410
  5. 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
  6. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  7. The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations.
    EMBO Rep. 2002 Aug;3(8):741-6 PMID: 12151332
  8. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation.
    Mol Cell. 2002 Apr;9(4):789-98 PMID: 11983170
  9. Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants.
    Plant Mol Biol. 2006 May;61(1-2):31-45 PMID: 16786290
  10. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  11. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence.
    J Mol Biol. 2000 Jul 21;300(4):1005-16 PMID: 10891285
  12. 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
  13. Characterization of a sulfurtransferase from Arabidopsis thaliana.
    Eur J Biochem. 2000 Jan;267(1):145-54 PMID: 10601861
  14. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance.
    EMBO J. 2000 Aug 1;19(15):4004-14 PMID: 10921881
  15. Ntdin, a tobacco senescence-associated gene, is involved in molybdenum cofactor biosynthesis.
    Plant Cell Physiol. 2003 Oct;44(10):1037-44 PMID: 14581628
  16. Plastids and stromules interact with the nucleus and cell membrane in vascular plants.
    Plant Cell Rep. 2004 Oct;23(4):188-95 PMID: 15252692
  17. Temperature-sensitive formation of chloroplast protrusions and stromules in mesophyll cells of Arabidopsis thaliana.
    Protoplasma. 2007;230(1-2):23-30 PMID: 17351732
  18. Nitric oxide signaling in plants.
    Vitam Horm. 2005;72:339-98 PMID: 16492476
  19. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.
    Plant Cell. 2003 Apr;15(4):809-34 PMID: 12671079
  20. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9.
    J Biol Chem. 1999 Apr 23;274(17):11549-56 PMID: 10206961
  21. 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
  22. 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
  23. Mechanisms of plant resistance to viruses.
    Nat Rev Microbiol. 2005 Oct;3(10):789-98 PMID: 16132037
  24. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11640-5 PMID: 12185253
  25. A novel role for the TIR domain in association with pathogen-derived elicitors.
    PLoS Biol. 2007 Mar;5(3):e68 PMID: 17298188
  26. Reactive oxygen species: metabolism, oxidative stress, and signal transduction.
    Annu Rev Plant Biol. 2004;55:373-99 PMID: 15377225
  27. Intracellular localization of Arabidopsis sulfurtransferases.
    Plant Physiol. 2004 Jun;135(2):916-26 PMID: 15181206
  28. Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction.
    Plant Cell. 2000 Jun;12(6):917-32 PMID: 10852937
  29. Silencing of a gene encoding a protein component of the oxygen-evolving complex of photosystem II enhances virus replication in plants.
    Virology. 2002 Apr 10;295(2):307-19 PMID: 12033790
  30. Cleavage of Arabidopsis PBS1 by a bacterial type III effector.
    Science. 2003 Aug 29;301(5637):1230-3 PMID: 12947197
  31. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  32. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):8024-9 PMID: 12788974
  33. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity.
    Plant Cell. 2006 Oct;18(10):2792-806 PMID: 17028203
  34. Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus.
    Mol Plant Microbe Interact. 2003 Dec;16(12):1135-44 PMID: 14651347
  35. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus.
    Plant J. 2002 May;30(4):415-29 PMID: 12028572
  36. Significance of inducible defense-related proteins in infected plants.
    Annu Rev Phytopathol. 2006;44:135-62 PMID: 16602946
  37. Are innate immune signaling pathways in plants and animals conserved?
    Nat Immunol. 2005 Oct;6(10):973-9 PMID: 16177805
  38. Stromules: a characteristic cell-specific feature of plastid morphology.
    J Exp Bot. 2005 Mar;56(413):787-97 PMID: 15699062
  39. Multiple pathways of cytochrome c release from mitochondria in apoptosis.
    Biochim Biophys Acta. 2006 May-Jun;1757(5-6):639-47 PMID: 16678785
  40. An inhibitor of viral RNA replication is encoded by a plant resistance gene.
    Proc Natl Acad Sci U S A. 2007 Aug 21;104(34):13833-8 PMID: 17699618
  41. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2531-6 PMID: 17277084
  42. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development.
    Dev Cell. 2002 Jun;2(6):807-17 PMID: 12062092
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
Published
2008-02-08
Pages
449-62
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC2267721
Subset
IM
Grants
NIGMS NIH HHS · R01 GM062625 · United States
NIGMS NIH HHS · R01 GM062625-06A1 · United States
NIGMS NIH HHS · GM62625 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]