Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 43, 2013, Pages 17594-17599

  Ve, Thomas ^a   Williams, Simon J ^a   Catanzariti, Ann Maree ^b   Rafiqi, Maryam ^b,c   Rahman, Motiur ^d   Ellis, Jeffrey G ^e   Hardham, Adrienne R ^b   Jones, David A ^b   Anderson, Peter A ^d   Dodds, Peter N ^e   Kobe, Bostjan ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d FLINDERS UNIVERSITY   (Australia)

^e CSIRO   (Australia)

Author keywords

Avirulence protein; Innate immunity; Lipid binding; Plant cell internalization; Plant disease resistance

Indexed keywords

AVRM PROTEIN; DIMER; PHOSPHATIDYLINOSITIDE; PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; HYDROPHOBICITY; INNATE IMMUNITY; INTERNALIZATION; MUTATIONAL ANALYSIS; PLANT CELL; PLANT IMMUNITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; RNA PROCESSING; STATIC ELECTRICITY;

AVIRULENCE PROTEIN; INNATE IMMUNITY; LIPID BINDING; PLANT CELL INTERNALIZATION; PLANT DISEASE RESISTANCE;

AMINO ACID SEQUENCE; BASIDIOMYCOTA; CRYSTALLOGRAPHY, X-RAY; FLAX; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNOBLOTTING; MICROSCOPY, CONFOCAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATIDYLINOSITOLS; PLANT CELLS; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO;

EID: 84886411524     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307614110     Document Type: Article

References (37)

1. Rafiqi M, Ellis JG, Ludowici VA, Hardham AR, Dodds PN (2012) Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr Opin Plant Biol 15(4):477-482.
2. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S (2012) Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol 15(4):483-492.
3. de Jonge R, Bolton MD, Thomma BP (2011) How filamentous pathogens co-opt plants: The ins and outs of fungal effectors. Curr Opin Plant Biol 14(4):400-406.
4. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124(4):803-814.
5. Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323-329.
6. Dodds PN, Rathjen JP (2010) Plant immunity: Towards an integrated view of plantpathogen interactions. Nat Rev Genet 11(8):539-548.
7. Rafiqi M, et al. (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22(6):2017-2032.
8. Khang CH, et al. (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22(4):1388-1403.
9. Whisson SC, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450(7166):115-118.
10. Kemen E, et al. (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant Microbe Interact 18(11):1130-1139.
11. Djamei A, et al. (2011) Metabolic priming by a secreted fungal effector. Nature 478(7369):395-398.
12. Plett JM, et al. (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21(14):1197-1203.
13. Ribot C, et al. (2013) The Magnaporthe oryzae effector AVR1-CO39 is translocated into rice cells independently of a fungal-derived machinery. Plant J 74(1):1-12.
14. Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21(14):1204-1209.
15. Kale SD, et al. (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142(2):284-295.
16. Dou D, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20(7): 1930-1947.
17. Haas BJ, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461(7262):393-398.
18. Schornack S, et al. (2010) Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci USA 107(40):17421-17426.
19. Yaeno T, Shirasu K (2013) The RXLR motif of oomycete effectors is not a sufficient element for binding to phosphatidylinositol monophosphates. Plant Signal Behav 8(4).
20. Yaeno T, et al. (2011) Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci USA 108(35):14682-14687.
21. Wawra S, et al. (2012) Avirulence protein 3a (AVR3a) from the potato pathogen Phytophthora infestans forms homodimers through its predicted translocation region and does not specifically bind phospholipids. J Biol Chem 287(45):38101-38109.
22. Wawra S, et al. (2013) In vitro translocation experiments with RxLR-reporter fusion proteins of Avr1b from Phytophthora sojae and AVR3a from Phytophthora infestans fail to demonstrate specific autonomous uptake in plant and animal cells. Mol Plant Microbe Interact 26(5):528-536.
23. Tyler BM, et al. (2013) Microbe-independent entry of oomycete RxLR effectors and fungal RxLR-like effectors into plant and animal cells is specific and reproducible. Mol Plant Microbe Interact 26(6):611-616.
24. Wang CI, et al. (2007) Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity. Plant Cell 19(9): 2898-2912.
25. Dodds PN, et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103(23):8888-8893.
26. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellis JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18(1):243-256.
27. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16(3):755-768.
28. Catanzariti AM, et al. (2010) The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol Plant Microbe Interact 23(1):49-57.
29. Gan PH, et al. (2010) Lipid binding activities of flax rust AvrM and AvrL567 effectors. Plant Signal Behav 5(10):1272-1275.
30. Win J, et al. (2012) Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog 8(1):e1002400.
31. Burkhard P, Stetefeld J, Strelkov SV (2001) Coiled coils: A highly versatile protein folding motif. Trends Cell Biol 11(2):82-88.
32. Lin J, et al. (2011) Structural basis for site-specific ribose methylation by box C/D RNA protein complexes. Nature 469(7331):559-563.
33. Boutemy LS, et al. (2011) Structures of Phytophthora RXLR effector proteins: A conserved but adaptable fold underpins functional diversity. J Biol Chem 286(41): 35834-35842.
34. Chou S, et al. (2011) Hyaloperonospora arabidopsidis ATR1 effector is a repeat protein with distributed recognition surfaces. Proc Natl Acad Sci USA 108(32): 13323-13328.
35. Rüter C, Buss C, Scharnert J, Heusipp G, Schmidt MA (2010) A newly identified bacterial cell-penetrating peptide that reduces the transcription of pro-inflammatory cytokines. J Cell Sci 123(pt 13):2190-2198.
36. Ve T, et al. (2011) Crystallization and X-ray diffraction analysis of the C-terminal domain of the flax rust effector protein AvrM. Acta Crystallogr Sect F Struct Biol Cryst Commun 67(pt 12):1603-1607.
37. Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60(pt 12 pt 1):2256-2268.