An RxLR Effector from Phytophthora infestans Prevents Re-localisation of Two Plant NAC Transcription Factors from the Endoplasmic Reticulum to the Nucleus

PLoS Pathogens

Volumn 9, Issue 10, 2013, Pages

  McLellan, Hazel ^a   Boevink, Petra C ^a   Armstrong, Miles R ^a   Pritchard, Leighton ^a,b   Gomez, Sonia ^a,c   Morales, Juan ^c   Whisson, Stephen C ^a   Beynon, Jim L ^d   Birch, Paul R J ^a  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b Information and Computational Sciences Group   (United Kingdom)

^c UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^d UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NAC TRANSCRIPTION FACTOR; NTP1 TRANSCRIPTION FACTOR; NTP2 TRANSCRIPTION FACTOR; PEPTIDES AND PROTEINS; RXLR EFFECTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE COURSE; ENDOPLASMIC RETICULUM; FLUOROMETRY; GENE EXPRESSION; GENE SILENCING; IMMUNOBLOTTING; NICOTIANA BENTHAMIANA; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYTOPHTHORA INFESTANS; PLANT DISEASE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; CELL NUCLEUS; ENDOPLASMIC RETICULUM; GENE SILENCING; PHYTOPHTHORA INFESTANS; PLANT DISEASES; PLANT PROTEINS; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84887264085     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003670     Document Type: Article

References (62)

1. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G, (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465-476.
2. Zipfel C, (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20: 10-16.
3. Boller T, Felix G, (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
4. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM, (2009) Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response. Science 323: 95-101.
5. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329.
6. Block A, Alfano JR, (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Current Opinion in Microbiology 14: 39-46.
7. Birch PRJ, Rehmany AP, Pritchard L, Kamoun S, Beynon JL, (2006) Trafficking arms: oomycete effectors enter host plant cells, Trends in Microbiology. 14: 8-11.
8. Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, et al. (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Current Opinion in Plant Biology 11: 373-379.
9. van der Biezen EA, Jones JDG, (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454-456.
10. Dangl JL, Jones JDG, (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
11. Nimchuk Z, Eulgem T, Holt III BF, Dangl JL, (2003) Recognition and response in the plant immune system. Annu Rev Genet 37: 579-609.
12. Hein I, Gilroy EM, Armstrong MR, Birch PRJ, (2009) The zig-zag-zig in oomycete-plant interactions. Molecular Plant Pathology 10: 1364-370.
13. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839-1850.
14. Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature. 450: 115-118.
15. Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930-1947.
16. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393-398.
17. Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, et al. (2010) Signatures of Adaptation to Obligate Biotrophy in the Hyaloperonospora arabidopsidis Genome. Science 330(6010): 1549-1551.
18. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261-1266.
19. Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, et al. (2009) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21: 2928-2947.
20. Wang Q, Han C, Ferreira AO, Yu X, Yu W, et al. (2011) Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 23: 2064-2086.
21. Fabro G, Steinbrenner J, Coates M, Ishaque N, Baxter L, et al. (2011) Multiple candidate effectors from the oomycete pathogen Hyaloperonospora arabidopsidis suppress host plant immunity. PLoS Pathog 7: e1002348.
22. Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601-607.
23. Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J, et al. (2011) Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network. Science 333: 596-600.
24. Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, et al. (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1 Proc Natl Acad Sci (USA). 107: 9909-9914.
25. Gilroy EM, Taylor RM, Hein I, Boevink PC, Sadanandom A, et al. (2011) CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytologist 190: 1469-8137.
26. Saunders DGO, Breen S, Win J, Schornack S, Hein I, et al. (2012) Host Protein BSL1 Associates with Phytophthora infestans RXLR Effector AVR2 and the Solanum demissum Immune Receptor R2 to Mediate Disease Resistance Plant Cell. 24: 3420-3434.
27. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, et al. (2011) Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface Proc Natl Acad Sci (USA). 108: 20832-20837.
28. Dong S, Yin W, Kong G, Yang X, Qutob D, et al. (2011) Phytophthora sojae Avirulence Effector Avr3b is a Secreted NADH and ADP-ribose Pyrophosphorylase that Modulates Plant Immunity. PLoS Pathog 7: e1002353 doi:10.1371/journal.ppat.1002353.
29. Senchou V, Weide R, Carrasco A, Bouyssou H, Pont-Lezica R, et al. (2004) High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cell Mol Life Sci 61: 502-509.
30. Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, et al. (2011) The Lectin Receptor Kinase LecRK-I.9 Is a Novel Phytophthora Resistance Component and a Potential Host Target for a RXLR Effector. PLoS Pathog 7: e1001327 doi:10.1371/journal.ppat.1001327.
31. Caillaud M-C, Piquerez SJM, Fabro G, Steinbrenner J, Ishaque N, et al. (2012) Subcellular localisation of the Hpa RXLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced susceptibility. The Plant J 69: 252-265.
32. Deslandes L, Rivas S, (2011) The plant cell nucleus: a true arena for the fight between plants and pathogens. Plant Signal Behaviour 6: 42-48.
33. Rivas S, (2012) Nuclear dynamics during plant innate immunity. Plant Physiol 158: 87-94.
34. Lu Y-J, Schornack S, Spallek T, Geldner N, Chory J, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cellular Microbiology 14: 1462-5822.
35. Kim S-Y, Kim S-G, Kim Y-S, Seo PJ, Bae M, et al. (2007) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucl Acids Res 35: 203-213.
36. Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, et al. (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102: 577-586.
37. Kim Y-S, Kim S-G, Park J-E, Park H-Y, Lim M-H, et al. (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18: 3132-44.
38. Seo PJ, Kim S-G, Park CM, (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13: 550-556.
39. Bombarely A, Rosli HG, Vrebalov J, Moffett P, Mueller L, et al. (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact doi: 10.1094/mpmi-06-12-0148-ta.
40. Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP, (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30: 415-429.
41. Avrova AO, Boevink PC, Young V, Grenville-Briggs LJ, van West P, et al. (2008) A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cell Microbiol 10: 2271-2284.
42. Nguyen HP, Chakravarthy S, Velásquez AC, McLane HL, Zeng L, et al. (2010) Methods to Study PAMP-Triggered Immunity Using Tomato and Nicotiana benthamiana. Molecular Plant-Microbe Interactions 23: 991-999.
43. Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H, (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 Transcription Factor by MAPK Functions in the Defense Response. Plant Cell 23: 1153-1170.
44. Puranik S, Sahu PP, Srivastava PS, Prasad M, (2012) NAC proteins: regulation and role in stress tolerance. Trends in Plant Science 17: 369-381.
45. Lee S, Seo PJ, Lee H-J, Park C-M, (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. The Plant J 70: 831-844.
46. Kim S-G, Lee A-K, Yoon H-K, Park C-M, (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. The Plant J 55: 77-88.
47. Seo PJ, Kim MJ, Park J-Y, Jeon J, Lee Y-H, et al. (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. The Plant J 61: 661-671.
48. Nguyen HM, Schippers JHM, Gõni-Ramos O, Christoph MP, Dortay H, et al. (2013) An upstream regulator of the 26S proteasome modulates organ size in Arabidopsis thaliana. The Plant J 74: 25-36.
49. Yoon H-K, Kim S-G, Kim S-Y, Park C-M, (2008) Regulation of leaf senescence by NTL9-mediated osmotic stress signalling in Arabidopsis. Mol Cells 25: 438-445.
50. Olsen AN, Ernst HA, Leggio LL, Shriver K, (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10: 79-87.
51. Ren T, Qu F, Morris TJ, (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. The Plant Cell 12: 1917-1925.
52. Ren T, Qu F, Morris TJ, (2005) The nuclear localisation of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip Crinkle Virus. Virology 331: 316-324.
53. Karimi M, Inze D, Depicker A, (2002) Gateway vectors for Agrobacterium mediated plant transformation. Trends in plant Science 7: 193-195.
54. Curtis MD, Grossniklaus U, (2003) A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta. Plant Physiol 133: 462-469.
55. Gilroy EM, Hein I, van der Hoorn R, Boevink PC, Venter E, et al. (2007) Involvement of cathepsin B in the plant disease resistance hypersensitive response. The Plant Journal 52: 1-13.
56. Chomczynski P, Sacchi N, (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical biochemistry 162: 156-159.
57. Lacomme C, Hrubikova K, (2003) Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats. The Plant J. 34: 543-553.
58. Eddy SR, (2011) Accelerated Profile HMM Searches. PLoS Comput Biol 7(10): e1002195 doi:10.1371/journal.pcbi.1002195.
59. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T, (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
60. Darriba D, Taboada GL, Doallo R, Posada D, (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8): 772.
61. Stamatakis A, (2006) RAxML-VI-HPC: Maximum Likelihood-based Phylogenetic Analyses with Thousands of Taxa and Mixed Models. Bioinformatics 22(21): 2688-2690.
62. Moller S, Croning MDR, Apweiler R, (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17(7): 646-653.