Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat

New Phytologist

Volumn 206, Issue 2, 2015, Pages 606-613

  Schoonbeek, Henk jan ^a   Wang, Hsi Hua ^a   Stefanato, Francesca L ^a,b   Craze, Melanie ^b   Bowden, Sarah ^b   Wallington, Emma ^b   Zipfel, Cyril ^a   Ridout, Christopher J ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b NATIONAL INSTITUTE OF AGRICULTURAL BOTANY   (United Kingdom)

Author keywords

Bacterial halo blight; Dicotyledon to monocotyledon gene transfer; Durable disease resistance; Immune receptor signalling; Pathogen recognition; Pathogen associated molecular pattern (PAMP) microbe associate molecular pattern (MAMP) triggered immunity; Transgenic wheat

Indexed keywords

BACTERIAL DISEASE; BIOASSAY; DICOTYLEDON; DISEASE RESISTANCE; GENE EXPRESSION; GENETIC ALGORITHM; IMMUNE RESPONSE; SIGNALING; TRANSGENIC PLANT;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); DICOTYLEDONEAE; LILIOPSIDA; PSEUDOMONAS SYRINGAE PV. ORYZAE; SOLANACEAE; TRITICUM AESTIVUM;

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; CALLOSE; EFR PROTEIN, ARABIDOPSIS; ELONGATION FACTOR TU; GLUCAN; PATTERN RECOGNITION RECEPTOR;

ARABIDOPSIS; BIOASSAY; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; ORYZA; PHYSIOLOGY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; WHEAT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL ASSAY; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; GLUCANS; ORYZA; PEPTIDE ELONGATION FACTOR TU; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION; TRITICUM;

EID: 84925256357     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13356     Document Type: Article

References (62)

1. Afroz A, Chaudhry Z, Rashid U, Ali GM, Nazir F, Iqbal J, Khan MR. 2011. Enhanced resistance against bacterial wilt in transgenic tomato (Lycopersicon esculentum) lines expressing the Xa21 gene. Plant Cell Tissue and Organ Culture 104: 227-237.
2. Bahar O, Pruitt R, Luu DD, Schwessinger B, Daudi A, Liu F, Ruan R, Fontaine-Bodin L, Koebnik R, Ronald P. 2014. The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles. PeerJ 2: e242.
3. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60: 379-406.
4. Boyd LA, Ridout C, O'Sullivan DM, Leach JE, Leung H. 2013. Plant-pathogen interactions: disease resistance in modern agriculture. Trends in Genetics 29: 233-240.
5. Cantu D, Yang B, Ruan R, Li K, Menzo V, Fu D, Chern M, Ronald P, Dubcovsky J. 2013. Comparative analysis of protein-protein interactions in the defense response of rice and wheat. BMC Genomics 14: 166.
6. Chen XW, Zuo SM, Schwessinger B, Chern M, Canlas PE, Ruan DL, Zhou XG, Wang J, Daudi A, Petzold CJ et al. 2014. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and xa3 immune receptors. Molecular Plant 7: 874-892.
7. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, Felix G, Boller T. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500.
8. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC et al. 2003. SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973-977.
9. Dangl JL, Horvath DM, Staskawicz BJ. 2013. Pivoting the plant immune system from dissection to deployment. Science 341: 746-751.
10. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 11: 539-548.
11. Felix G, Duran JD, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant Journal 18: 265-276.
12. Furukawa T, Inagaki H, Takai R, Hirai H, Che FS. 2014. Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Molecular Plant-Microbe Interactions 27: 113-124.
13. Gomez-Gomez L, Boller T. 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Molecular Cell 5: 1003-1011.
14. Hamel LP, Beaudoin N. 2010. Chitooligosaccharide sensing and downstream signaling: contrasted outcomes in pathogenic and beneficial plant-microbe interactions. Planta 232: 787-806.
15. Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M, Desaki Y, Arima S, Squeglia F, Ruggiero A, Tokuyasu K et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proceedings of the National Academy of Sciences, USA 111: E404-E413.
16. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences, USA 104: 12217-12222.
17. Holton N, Nekrasov V, Ronald PC, Zipfel C. 2015. The phylogenetically-related pattern recognition receptors EFR and XA21 recruit similar immune signaling components in monocots and dicots. PLoS Pathogens 11: e1004602.
18. Hood EE, Gelvin SB, Melchers LS, Hoekema A. 1993. New Agrobacterium helper plasmids for gene-transfer to plants. Transgenic Research 2: 208-218.
19. Hwang MSH, Morgan RL, Sarkar SF, Wang PW, Guttman DS. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Applied and Environmental Microbiology 71: 5182-5191.
20. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proceedings of the National Academy of Sciences, USA 103: 11086-11091.
21. Kawano Y, Shimamoto K. 2013. Early signaling network in rice PRR-mediated and R-mediated immunity. Current Opinion in Plant Biology 16: 496-504.
22. Keller B, Feuillet C, Messmer M 2000. Genetics of disease resistance. In: Slusarenko AJ, Fraser RSS, Loon LC, eds. Mechanisms of resistance to plant diseases. Dordrecht, the Netherlands: Springer, 101-160.
23. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. Journal of Laboratory and Clinical Medicine 44: 301-307.
24. Kirsch C, Logemann E, Lippok B, Schmelzer E, Hahlbrock K. 2001. A highly specific pathogen-responsive promoter element from the immediate-early activated CMPG1 gene in Petroselinum crispum. Plant Journal 26: 217-227.
25. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. 2010. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant Journal 64: 343-354.
26. Klimyuk VI, Carroll BJ, Thomas CM, Jones JDG. 1993. Alkali treatment for rapid preparation of plant-material for reliable pcr analysis. Plant Journal 3: 493-494.
27. Kouzai Y, Mochizuki S, Nakajima K, Desaki Y, Hayafune M, Miyazaki H, Yokotani N, Ozawa K, Minami E, Kaku H et al. 2014a. Targeted gene disruption of OsCERK1 reveals its indispen sable role in chitin perception and involvement in the peptidoglycan response and immunity in rice. Molecular Plant-Microbe Interactions 27: 975-982.
28. Kouzai Y, Nakajima K, Hayafune M, Ozawa K, Kaku H, Shibuya N, Minami E, Nishizawa Y. 2014b. CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Molecular Biology 84: 519-528.
29. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. 2004. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496-3507.
30. Kuwata H. 1985. Pseudomonas syringae pathovar oryzae new pathovar causal agent of bacterial halo blight of rice. Annals of the Phytopathological Society of Japan 51: 212-218.
31. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BPHJ, Staskawicz B et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28: 365-369.
32. Lee W-S, Rudd JJ, Hammond-Kosack KE, Kanyuka K. 2014. Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat. Molecular Plant-Microbe Interactions 27: 236-243.
33. Lloyd SR, Schoonbeek H-j, Trick M, Zipfel C, Ridout CJ. 2014. Methods to study PAMP-triggered immunity in Brassica Species. Molecular Plant-Microbe Interactions 27: 286-295.
34. Lu F, Wang H, Wang S, Jiang W, Shan C, Li B, Yang J, Zhang S, Sun W. 2014. Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR. Journal of Integrative Plant Biology. doi: 10.1111/jipb.12306.
35. Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell 54: 263-272.
36. Mendes BMJ, Cardoso SC, Boscariol-Camargo RL, Cruz RB, Mourao FAA, Bergamin A. 2010. Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathology 59: 68-75.
37. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BPHJ et al. 2012. Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24: 322-335.
38. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proceedings of the National Academy of Sciences, USA 104: 19613-19618.
39. Risacher T, Craze M, Bowden S, Paul W, Barsby T. 2009. Highly efficient Agrobacterium-mediated transformation of wheat via in planta inoculation. In: Jones HD, Shewry PR, eds. Methods in molecular biology. New York, NY, USA: Humana Press, 115-124.
40. Robatzek S, Bittel P, Chinchilla D, Kochner P, Felix G, Shiu SH, Boller T. 2007. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Molecular Biology 64: 539-547.
41. Roux F, Voisin D, Badet T, Balague C, Barlet X, Huard-Chauveau C, Roby D, Raffaele S. 2014. Resistance to phytopathogens e tutti quanti: placing plant quantitative disease resistance on the map. Molecular Plant Pathology 15: 427-432.
42. Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A, Holton N, Malinovsky FG, Tor M, de Vries S, Zipfel C. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23: 2440-2455.
43. Rudd JJ, Keon J, Hammond-Kosack KE. 2008. The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiology 147: 802-815.
44. Rudolph K, von Kietzell J. 1997. Wheat diseases caused by Pseudomonas syringae pathovars. In: Duveiller E, Fucikovsky L, Rudolph K, eds. The bacterial diseases of wheat: concepts and methods of disease management. Mexico City, Mexico: CIMMYT, 49-58.
45. Schwessinger B, Bahar O, Nicolas T, Nekrasov V, Ruan R, Canlas P, Daudi A, Petzold C, Singan V, Kuo R et al. 2014. Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. BioRxiv. doi:10.1101/006155.
46. Schwessinger B, Ronald PC. 2012. Plant innate immunity: perception of conserved microbial signatures. Annual Review of Plant Biology 63: 451-482.
47. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H et al. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant Journal 64: 204-214.
48. Shinya T, Motoyama N, Ikeda A, Wada M, Kamiya K, Hayafune M, Kaku H, Shibuya N. 2012. Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant and Cell Physiology 53: 1696-1706.
49. Singla B, Khurana JP, Khurana P. 2008. Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum. Plant Cell Reports 27: 833-843.
50. Song W-Y, Wang G-L, Chen L-L, Kim H-S, Pi L-Y, Holsten T, Gardner J, Wang B, Zhai W-X, Zhu L-H et al. 1995. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804-1806.
51. Takai R, Isogai A, Takayama S, Che FS. 2008. Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Molecular Plant-Microbe Interactions 21: 1635-1642.
52. Tan SJ, Wang D, Ding J, Tian DC, Zhang XH, Yang SH. 2011. Adaptive evolution of Xa21 homologs in Gramineae. Genetica 139: 1465-1475.
53. Tanaka S, Ichikawa A, Yamada K, Tsuji G, Nishiuchi T, Mori M, Koga H, Nishizawa Y, O'Connell R, Kubo Y. 2010. HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biology 10: 288.
54. Trda L, Fernandez O, Boutrot F, Heloir MC, Kelloniemi J, Daire X, Adrian M, Clement C, Zipfel C, Dorey S et al. 2014. The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytologist 201: 1371-1384.
55. Tripathi JN, Lorenzen J, Bahar O, Ronald P, Tripathi L. 2014. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnology Journal 12: 663-673.
56. Trujillo M, Ichimura K, Casais C, Shirasu K. 2008. Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Current Biology 18: 1396-1401.
57. Tufan HA, McGrann GRD, Magusin A, Morel J-B, Miché L, Boyd LA. 2009. Wheat blast: histopathology and transcriptome reprogramming in response to adapted and nonadapted Magnaporthe isolates. New Phytologist 184: 473-484.
58. Valdés-López O, Thibivilliers S, Qiu J, Wenzhong XuW, Nguyen THN, Libault M, Le BH, Goldberg RB, Hill CB, Hartman GL et al. 2011. Identification of quantitative trait loci controlling gene expression during the innate immunity response of soybean. Plant Physiology 157: 1975-1986.
59. Wan JR, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481.
60. Wu Y, Zhou J-M. 2013. Receptor-like kinases in plant innate immunity. Journal of Integrative Plant Biology 55: 1271-1286.
61. Zipfel C. 2014. Plant pattern-recognition receptors. Trends in Immunology 35: 345-351.
62. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.