Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and the effector AVR1

New Phytologist

Volumn 207, Issue 3, 2015, Pages 735-747

  Du, Yu ^a   Berg, Jeroen ^a   Govers, Francine ^a   Bouwmeester, Klaas ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Effector triggered immunity (ETI); Nucleocytoplasmic partitioning; Nucleotide binding leucine rich repeat (NLR); Phytophthora infestans; RXLR effector

Indexed keywords

CELL ORGANELLE; DISEASE RESISTANCE; FUNGAL DISEASE; GENE EXPRESSION; HOST-PATHOGEN INTERACTION; IMMUNE SYSTEM; MICROSCOPY; MOLECULAR ANALYSIS; PHYSIOLOGICAL RESPONSE; POTATO; PROTEIN; VIRULENCE;

NICOTIANA BENTHAMIANA; PHYTOPHTHORA INFESTANS;

GREEN FLUORESCENT PROTEIN; NUCLEAR EXPORT SIGNAL; VIRULENCE FACTOR;

CELL DEATH; CELL NUCLEUS; DISEASE RESISTANCE; FLUORESCENCE; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; NUCLEAR EXPORT SIGNAL; PHYTOPHTHORA INFESTANS; PLANT DISEASE; PROTEIN TRANSPORT; TOBACCO;

CELL DEATH; CELL NUCLEUS; DISEASE RESISTANCE; FLUORESCENCE; GREEN FLUORESCENT PROTEINS; NUCLEAR EXPORT SIGNALS; PHYTOPHTHORA INFESTANS; PLANT DISEASES; PROTEIN TRANSPORT; TOBACCO; VIRULENCE FACTORS;

EID: 84936173198     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13355     Document Type: Article

References (63)

1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences, USA 95: 10306-10311.
2. Anderson RG, Casady MS, Fee RA, Vaughan MM, Deb D, Fedkenheuer K, Huffaker A, Schmelz EA, Tyler BM, McDowell JM. 2012. Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants. Plant Journal 72: 882-893.
3. Ando S, Obinata A, Takahashi H. 2014. WRKY70 interacting with RCY1 disease resistance protein is required for resistance to Cucumber mosaic virus in Arabidopsis thaliana. Physiological and Molecular Plant Pathology 85: 8-14.
4. Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P. 2002. The RAR1 interactor SGT1, an essential component of R Gene-triggered disease resistance. Science 295: 2073-2076.
5. Bai SW, Liu J, Chang C, Zhang L, Maekawa T, Wang QY, Xiao WK, Liu YL, Chai JJ, Takken FLW et al. 2012. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathogens 8: e1002752.
6. Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C. 2002. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant Journal 30: 361-371.
7. Belkhadir Y, Subramaniam R, Dangl JL. 2004. Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Current Opinion in Plant Biology 7: 391-399.
8. Bernoux M, Timmers T, Jauneau A, Briere C, de Wit PJGM, Marco Y, Deslandes L. 2008. RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell 20: 2252-2264.
9. Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Tian ZD, Engelhardt S, Vetukuri RR, Harrower B et al. 2010. Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences, USA 107: 9909-9914.
10. Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, Canut H, Govers F. 2011. The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathogens 7: e1001327.
11. Bouwmeester K, Han M, Blanco-Portales R, Song W, Weide R, Guo LY, van der Vossen EAG, Govers F. 2014. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnology Journal 12: 10-16.
12. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biology 5: 501-514.
13. Caillaud MC, Piquerez SJM, Fabro G, Steinbrenner J, Ishaque N, Beynon J, Jones JDG. 2012a. Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant Journal 69: 252-265.
14. Caillaud MC, Wirthmueller L, Fabro G, Piquerez SJ, Asai S, Ishaque N, Jones JD. 2012b. Mechanisms of nuclear suppression of host immunity by effectors from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). Cold Spring Harbor Symposia on Quantitative Biology 77: 285-293.
15. Caplan J, Padmanabhan M, Dinesh-Kumar SP. 2008. Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host & Microbe 3: 126-135.
16. Carrasco A, Chauvin JE, Trognitz B, Pawlak A, Rubio-Covarruvias O, Zimnoch-Guzowska E. 2009. Marker-assisted breeding for disease resistance in potato. Potato Research 52: 245-248.
17. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ. 1997. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963-1965.
18. Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C, Heupink A, van de Vondervoort PJI, Jacobsen E, Visser RGF, van der Vossen EAG et al. 2009. Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Molecular Plant-Microbe Interactions 22: 1535-1545.
19. Chang C, Yu DS, Jiao J, Jing SJ, Schulze-Lefert P, Shen QH. 2013. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell 25: 1158-1173.
20. Cheng YT, Germain H, Wiermer M, Bi DL, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang YL et al. 2009. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21: 2503-2516.
21. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
22. Elmore JM, Lin ZJD, Coaker G. 2011. Plant NB-LRR signaling: upstreams and downstreams. Current Opinion in Plant Biology 14: 365-371.
23. Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PRJ. 2012. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24: 5142-5158.
24. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE. 2005. Arabidopsis senescence-associated gene 101 stabilizes and signals within an enhanced disease susceptibility 1 complex in plant innate immunity. Plant Cell 17: 2601-2613.
25. Gao ZY, Chung EH, Eitas TK, Dang JL. 2011. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proceedings of the National Academy of Sciences, USA 108: 8915-8915.
26. Haasen D, Kohler C, Neuhaus G, Merkle T. 1999. Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant Journal 20: 695-705.
27. Hardham AR, Cahill DM. 2010. The role of oomycete effectors in plant-pathogen interactions. Functional Plant Biology 37: 919-925.
28. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334: 1401-1404.
29. van der Hoorn RAL, Laurent F, Roth R, de Wit PJGM. 2000. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Molecular Plant-Microbe Interactions 13: 439-446.
30. Hoser R, Zurczak M, Lichocka M, Zuzga S, Dadlez M, Samuel MA, Ellis BE, Stuttmann J, Parker JE, Hennig J et al. 2013. Nucleocytoplasmic partitioning of tobacco N receptor is modulated by SGT1. New Phytologist 200: 158-171.
31. Inoue H, Hayashi N, Matsushita A, Liu XQ, Nakayama A, Sugano S, Jiang CJ, Takatsuji H. 2013. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proceedings of the National Academy of Sciences, USA 110: 9577-9582.
32. Jo KR, Kim CJ, Kim SJ, Kim TY, Bergervoet M, Jongsma MA, Visser RGF, Jacobsen E, Vossen JH. 2014. Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnology 14: 50.
33. Jones JDG, Witek K, Verweij W, Jupe F, Cooke D, Dorling S, Tomlinson L, Smoker M, Perkins S, Foster S. 2014. Elevating crop disease resistance with cloned genes. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 20130087.
34. Kamoun S, van West P, Vleeshouwers VGAA, de Groot KE, Govers F. 1998. Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10: 1413-1425.
35. Lee LY, Fang MJ, Kuang LY, Gelvin SB. 2008. Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods 4: 24.
36. van der Lee T, Testa A, Robold A, van't Klooster J, Govers F. 2004. High-density genetic linkage maps of Phytophthora infestans reveal trisomic progeny and chromosomal rearrangements. Genetics 167: 1643-1661.
37. Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJC, Takken FLW. 2012. Dual regulatory roles of the extended N terminus for activation of the tomato Mi-1.2 resistance protein. Molecular Plant-Microbe Interactions 25: 1045-1057.
38. Ma L, Cornelissen BJ, Takken FLW. 2013. A nuclear localization for Avr2 from Fusarium oxysporum is required to activate the tomato resistance protein I-2. Frontiers in Plant Science 4: 94.
39. Marfori M, Mynott A, Ellis JJ, Mehdi AM, Saunders NFW, Curmi PM, Forwood JK, Boden M, Kobe B. 2011. Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research 1813: 1562-1577.
40. Matsushita T, Mochizuki N, Nagatani A. 2003. Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424: 571-574.
41. McLellan H, Boevink PC, Armstrong MR, Pritchard L, Gomez S, Morales J, Whisson SC, Beynon JL, Birch PRJ. 2013. An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathogens 9: e1003670.
42. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW. 2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 1683-1683.
43. Nguyen Ba AN, Pogoutse A, Provart N, Moses A. 2009. NLStradamus: a simple hidden markov model for nuclear localization signal prediction. BMC Bioinformatics 10: 202.
44. Padmanabhan MS, Dinesh-Kumar SP. 2014. The conformational and subcellular compartmental dance of plant NLRs during viral recognition and defense signaling. Current Opinion in Microbiology 20: 55-61.
45. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathogens 9: e1003235.
46. Saunders DGO, Breen S, Win J, Schornack S, Hein I, Bozkurt TO, Champouret N, Vleeshouwers VGAA, Birch PRJ, Gilroy EM 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.
47. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P. 2007. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
48. Shen QH, Schulze-Lefert P. 2007. Rumble in the nuclear jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO Journal 26: 4293-4301.
49. Shirasu K. 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annual Review of Plant Biology 60: 139-164.
50. Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling WIL, Joosten MHAJ, Pomp R, van Schaik C, Dees R, Borst JW et al. 2010. Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell 22: 4195-4215.
51. Takken FLW, Tameling WIL. 2009. To nibble at plant resistance proteins. Science 324: 744-746.
52. Tameling WIL, Baulcombe DC. 2007. Physical association of the NB-LRR resistance protein Rx with a ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19: 1682-1694.
53. Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW, Haring MA, Cornelissen BJC. 2002. The tomato R gene products I-2 and Mi-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14: 2929-2939.
54. Tameling WIL, Nooijen C, Ludwig N, Boter M, Slootweg E, Goverse A, Shirasu K, Joosten MHAJ. 2010. RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22: 4176-4194.
55. Tameling WIL, Takken FLW. 2008. Resistance proteins: scouts of the plant innate immune system. European Journal of Plant Pathology 121: 243-255.
56. Torto TA, Li SA, Styer A, Huitema E, Testa A, Gow NAR, van West P, Kamoun S. 2003. EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Research 13: 1675-1685.
57. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokossou A, Kessel G et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annual Review of Phytopathology 49: 507-531.
58. Vleeshouwers VGAA, van Dooijeweert W, Keizer LCP, Sijpkes L, Govers F, Colon LT. 1999. A laboratory assay for Phytophthora infestans resistance in various Solanum species reflects the field situation. European Journal of Plant Pathology 105: 241-250.
59. Wang Q, Han C, Ferreira AO, Yu X, Ye W, Tripathy S, Kale SD, Gu B, Sheng Y, Sui Y et al. 2011. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 6: 2064-2086.
60. Wen W, Meinkoth JL, Tsien RY, Taylor SS. 1995. Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463-473.
61. Wiermer M, Feys BJ, Parker JE. 2005. Plant immunity: the EDS1 regulatory node. Current Opinion in Plant Biology 8: 383-389.
62. Wirthmueller L, Zhang Y, Jones JDG, Parker JE. 2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Current Biology 17: 2023-2029.
63. Yu XL, Tang JL, Wang QQ, Ye WW, Tao K, Duan SY, Lu CC, Yang XY, Dong SM, Zheng XB et al. 2012. The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytologist 196: 247-260.