Home LiteratureArticle Details
PMID: 18390593 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b.

The Plant cell ·Vol. 20 ·No. 4 ·2008-04-00 ·Pages 1118-33

Dou D, Kale SD, Wang X, Chen Y, Wang Q, Wang X, Jiang RH, Arredondo FD, Anderson RG, Thakur PB, McDowell JM, Wang Y, Tyler BM

Abstract

The sequenced genomes of oomycete plant pathogens contain large superfamilies of effector proteins containing the protein translocation motif RXLR-dEER. However, the contributions of these effectors to pathogenicity remain poorly understood. Here, we show that the Phytophthora sojae effector protein Avr1b can contribute positively to virulence and can suppress programmed cell death (PCD) triggered by the mouse BAX protein in yeast, soybean (Glycine max), and Nicotiana benthamiana cells. We identify three conserved motifs (K, W, and Y) in the C terminus of the Avr1b protein and show that mutations in the conserved residues of the W and Y motifs reduce or abolish the ability of Avr1b to suppress PCD and also abolish the avirulence interaction of Avr1b with the Rps1b resistance gene in soybean. W and Y motifs are present in at least half of the identified oomycete RXLR-dEER effector candidates, and we show that three of these candidates also suppress PCD in soybean. Together, these results indicate that the W and Y motifs are critical for the interaction of Avr1b with host plant target proteins and support the hypothesis that these motifs are critical for the functions of the very large number of predicted oomycete effectors that contain them.

MeSH Terms
Algal Proteins/chemistry,physiology Amino Acid Sequence Animals Cell Death/physiology Mice Molecular Sequence Data Phytophthora/pathogenicity Sequence Homology, Amino Acid Virulence/physiology
Chemicals
Algal Proteins
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Dou Daolong
Virginia Bioinformatics Institute, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061, USA.
Kale Shiv D
Wang Xinle
Chen Yubo
Wang Qunqing
Wang Xia
Jiang Rays H Y
Arredondo Felipe D
Anderson Ryan G
Thakur Poulami B
McDowell John M
Wang Yuanchao
Tyler Brett M
References (66)
66 references, click to expand
  1. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance.
    EMBO J. 2000 Aug 1;19(15):4004-14 PMID: 10921881
  2. Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes.
    Plant Cell. 2007 Aug;19(8):2349-69 PMID: 17675403
  3. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines.
    Plant Cell. 2005 Jun;17(6):1839-50 PMID: 15894715
  4. A host-targeting signal in virulence proteins reveals a secretome in malarial infection.
    Science. 2004 Dec 10;306(5703):1934-7 PMID: 15591203
  5. Structural biology. Controlling the caspases.
    Science. 2001 Nov 16;294(5546):1477-8 PMID: 11711663
  6. Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity.
    Curr Opin Plant Biol. 2004 Aug;7(4):384-90 PMID: 15231260
  7. The malarial host-targeting signal is conserved in the Irish potato famine pathogen.
    PLoS Pathog. 2006 May;2(5):e50 PMID: 16733545
  8. The plant immune system.
    Nature. 2006 Nov 16;444(7117):323-9 PMID: 17108957
  9. RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members.
    Proc Natl Acad Sci U S A. 2008 Mar 25;105(12):4874-9 PMID: 18344324
  10. Apoptosis in yeast.
    Curr Opin Microbiol. 2004 Dec;7(6):655-60 PMID: 15556039
  11. A bacterial effector acts as a plant transcription factor and induces a cell size regulator.
    Science. 2007 Oct 26;318(5850):648-51 PMID: 17962565
  12. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew.
    Science. 2004 Dec 10;306(5703):1957-60 PMID: 15591208
  13. The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana.
    Plant J. 2006 Oct;48(2):165-76 PMID: 16965554
  14. A novel plant glutathione S-transferase/peroxidase suppresses Bax lethality in yeast.
    J Biol Chem. 2000 Sep 22;275(38):29207-16 PMID: 10859306
  15. Deletion of a disease resistance nucleotide-binding-site leucine-rich- repeat-like sequence is associated with the loss of the Phytophthora resistance gene Rps4 in soybean.
    Genetics. 2004 Dec;168(4):2157-67 PMID: 15611183
  16. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato.
    Plant J. 2003 Dec;36(6):867-82 PMID: 14675451
  17. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  18. Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes.
    Plant Mol Biol. 2004 Sep;56(1):15-27 PMID: 15604726
  19. Phytophthora sojae: root rot pathogen of soybean and model oomycete.
    Mol Plant Pathol. 2007 Jan;8(1):1-8 PMID: 20507474
  20. Type III secretion system effector proteins: double agents in bacterial disease and plant defense.
    Annu Rev Phytopathol. 2004;42:385-414 PMID: 15283671
  21. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy.
    Plant J. 2002 Nov;32(3):361-73 PMID: 12410814
  22. The bacterial injection kit: type III secretion systems.
    Ann Med. 2005;37(4):234-49 PMID: 16019722
  23. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast.
    Plant J. 2004 Feb;37(4):554-65 PMID: 14756767
  24. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes.
    Plant J. 2002 May;30(3):361-71 PMID: 12000683
  25. Oxygen stress: a regulator of apoptosis in yeast.
    J Cell Biol. 1999 May 17;145(4):757-67 PMID: 10330404
  26. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria.
    Curr Opin Microbiol. 2004 Feb;7(1):11-8 PMID: 15036134
  27. Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators.
    Bioessays. 2003 Jan;25(1):47-57 PMID: 12508282
  28. 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
  29. Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions.
    Cell Microbiol. 2007 Jun;9(6):1385-96 PMID: 17451411
  30. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis.
    Science. 2006 Sep 1;313(5791):1261-6 PMID: 16946064
  31. New insights to the function of phytopathogenic bacterial type III effectors in plants.
    Annu Rev Plant Biol. 2005;56:509-31 PMID: 15862106
  32. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase.
    Science. 2006 Jan 13;311(5758):222-6 PMID: 16373536
  33. A bacterial virulence protein suppresses host innate immunity to cause plant disease.
    Science. 2006 Jul 14;313(5784):220-3 PMID: 16840699
  34. 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
  35. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats.
    Cell. 1994 Sep 23;78(6):1089-99 PMID: 7923358
  36. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm.
    Proc Natl Acad Sci U S A. 2005 May 24;102(21):7766-71 PMID: 15894622
  37. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2851-6 PMID: 16477026
  38. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato.
    Plant J. 2005 Oct;44(2):208-22 PMID: 16212601
  39. Innate immunity in plants and animals: striking similarities and obvious differences.
    Immunol Rev. 2004 Apr;198:249-66 PMID: 15199967
  40. The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis.
    Plant J. 2006 Jan;45(2):166-79 PMID: 16367962
  41. An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses.
    Nat Immunol. 2007 Jan;8(1):47-56 PMID: 17159983
  42. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight.
    Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9128-33 PMID: 12872003
  43. Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato.
    Plant J. 2005 Apr;42(2):251-61 PMID: 15807786
  44. Trafficking arms: oomycete effectors enter host plant cells.
    Trends Microbiol. 2006 Jan;14(1):8-11 PMID: 16356717
  45. Two classes of highly similar coiled coil-nucleotide binding-leucine rich repeat genes isolated from the Rps1-k locus encode Phytophthora resistance in soybean.
    Mol Plant Microbe Interact. 2005 Oct;18(10):1035-45 PMID: 16255242
  46. The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death.
    Plant Physiol. 2007 Sep;145(1):135-46 PMID: 17631528
  47. Technical Focus:a guide to Agrobacterium binary Ti vectors.
    Trends Plant Sci. 2000 Oct;5(10):446-51 PMID: 11044722
  48. A translocation signal for delivery of oomycete effector proteins into host plant cells.
    Nature. 2007 Nov 1;450(7166):115-8 PMID: 17914356
  49. Transformation of the oomycete pathogen, Phytophthora infestans.
    Mol Plant Microbe Interact. 1991 Nov-Dec;4(6):602-7 PMID: 1804404
  50. Signal and nutrient exchange at biotrophic plant-fungus interfaces.
    Curr Opin Plant Biol. 2001 Aug;4(4):322-7 PMID: 11418342
  51. Host-microbe interactions: shaping the evolution of the plant immune response.
    Cell. 2006 Feb 24;124(4):803-14 PMID: 16497589
  52. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition.
    Curr Opin Microbiol. 2000 Feb;3(1):73-8 PMID: 10679421
  53. Groovy times: filamentous pathogen effectors revealed.
    Curr Opin Plant Biol. 2007 Aug;10(4):358-65 PMID: 17611143
  54. Bax-induced cell death in tobacco is similar to the hypersensitive response.
    Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7956-61 PMID: 10393929
  55. Baculoviruses and apoptosis: a diversity of genes and responses.
    Curr Drug Targets. 2007 Oct;8(10):1069-74 PMID: 17979666
  56. The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b.
    Mol Plant Microbe Interact. 2004 Apr;17(4):394-403 PMID: 15077672
  57. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  58. Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica).
    Mol Plant Pathol. 2003 May 1;4(3):159-70 PMID: 20569375
  59. Evolution of the protists and protistan parasites from the perspective of molecular systematics.
    Int J Parasitol. 1998 Jan;28(1):11-20 PMID: 9504331
  60. Arabidopsis Bax inhibitor-1 functions as an attenuator of biotic and abiotic types of cell death.
    Plant J. 2006 Mar;45(6):884-94 PMID: 16507080
  61. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death.
    EMBO J. 2003 Jan 2;22(1):60-9 PMID: 12505984
  62. Targeting malaria virulence and remodeling proteins to the host erythrocyte.
    Science. 2004 Dec 10;306(5703):1930-3 PMID: 15591202
  63. Toward improvements of oomycete transformation protocols.
    J Eukaryot Microbiol. 2008 Mar-Apr;55(2):103-9 PMID: 18318863
  64. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  65. Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities.
    Plant J. 2007 Sep;51(5):803-18 PMID: 17587302
  66. Phytophthora sojae avirulence genes Avr4 and Avr6 are located in a 24kb, recombination-rich region of genomic DNA.
    Fungal Genet Biol. 2004 Jan;41(1):62-74 PMID: 14643260
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2008-04-00
Epub
2008-00-04
Pages
1118-33
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2390733
Subset
IM
Databases
GENBANK
ABS50087, EF681129, EU282485, EU282486, EU282487, EU282488, EU282489, EU282490
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]