Enhancement of innate immune system in monocot rice by transferring the dicotyledonous elongation factor Tu receptor EFR

Journal of Integrative Plant Biology

Volumn 57, Issue 7, 2015, Pages 641-652

  Lu, Fen ^a   Wang, Huiqin ^a   Wang, Shanzhi ^a   Jiang, Wendi ^a   Shan, Changlin ^b   Li, Bin ^b   Yang, Jun ^a,c   Zhang, Shiyong ^c   Sun, Wenxian ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c SHANDONG PEANUT RESEARCH INSTITUTE   (China)

Author keywords

Bacterial disease resistance; Elongation factor Tu receptor; Interspecific gene transfer; Pattern recognition receptor; Rice

Indexed keywords

ARABIDOPSIS PROTEIN; EFR PROTEIN, ARABIDOPSIS; ELONGATION FACTOR TU; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PATTERN RECOGNITION RECEPTOR; PEPTIDE; REACTIVE OXYGEN METABOLITE;

AMINO ACID SEQUENCE; CHEMISTRY; DISEASE RESISTANCE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; ORYZA; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; TRANSGENIC PLANT; XANTHOMONAS;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; DISEASE RESISTANCE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, PLANT; IMMUNITY, INNATE; MAGNAPORTHE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; ORYZA; PEPTIDE ELONGATION FACTOR TU; PEPTIDES; PLANT DISEASES; PLANT IMMUNITY; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; RECEPTORS, PATTERN RECOGNITION; RNA, MESSENGER; XANTHOMONAS;

EID: 84934439523     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12306     Document Type: Article

References (65)

1. Abbruscato P, Nepusz T, Mizzi L, Del Corvo M, Morandini P, Fumasoni I, Michel C, Paccanaro A, Guiderdoni E, Schaffrath U, Morel JB, Piffanelli P, Faivre-Rampant O (2012) OsWRKY22, a monocot WRKY gene, plays a role in the resistance response to blast. Mol Plant Pathol 13: 828-841
2. Bent AF, Mackey D (2007) Elicitors, effectors, and R genes: The new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 45: 399-436
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. Cao A, Xing L, Wang X, Yang X, Wang W, Sun Y, Qian C, Ni J, Chen Y, Liu D, Wang X, Chen P (2011) Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc Natl Acad Sci USA 108: 7727-7732
5. Cao Y, Ding X, Cai M, Zhao J, Lin Y, Li X, Xu C, Wang S (2007) The expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Genetics 177: 523-533
6. Chen X, Ronald PC (2011) Innate immunity in rice. Trends Plant Sci 16: 451-459
7. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol Plant-Microbe Interact 18: 511-520
8. Chern M, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27: 101-113
9. Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341: 746-751
10. Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush GS, Muthukrishnan S, Datta SK (1999) Over-expression of the cloned rice thaumatin-like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theor Appl Genet 98: 1138-1145
11. Ding B, del Rosario Bellizzi M, Ning Y, Meyers BC, Wang G (2012) HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 24: 3783-3794
12. Felix G, Boller T (2003) Molecular sensing of bacteria in plants: The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278: 6201-6208
13. Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GC, Joosten MH, Thomma BP (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol 156: 2255-2265
14. Furukawa T, Inagaki H, Takai R, Hirai H, Che F (2014) Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Mol Plant-Microbe Interact 27: 113-124
15. Gómez-Gómez L, Boller T (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003-1011
16. Holsters M, De Waele D, Depicker A, Messens E, Van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet 163: 181-187
17. Jwa N, Agrawal GK, Tamogami S, Yonekura M, Han O, Iwahashi H, Rakwal R (2006) Role of defense/stress-related marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms. Plant Physiol Biochem 44: 261-273
18. Kauffman HE, Reddy APK, Hsieh SPY (1973) An improved technique for evaluation of resistance of rice varieties to Xanthomonas oryzae. Plant Dis 57: 537-541
19. Kim J, Kim JG, Kang Y, Jang JY, Jog GJ, Lim JY, Kim S, Suga H, Nagamatsu T, Hwang I (2004) Quorum sensing and the LysR-type transcriptional activator ToxR regulate toxoflavin biosynthesis and transport in Burkholderia glumae. Mol Microbiol 54: 921-934
20. 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
21. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, Van Esse HP, Smoker M, Rallapalli G, Thomma BP, Staskawicz B, Jones JDG, Zipfel C (2010) Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat Biotechnol 28: 365-369
22. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48: 251-275
23. Li B, Liu B, Yu R, Tao Z, Wang Y, Xie G, Li H, Sun G (2011) Bacterial brown stripe of rice in soil-less culture system caused by Acidovorax avenae subsp. avenae in China. J Gen Plant Pathol 77: 64-67
24. Linthorst HJ, Van Loon LC (1991) Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123-150
25. Liu B, Li J, Ao Y, Qu J, Li Z, Su J, Zhang Y, Liu J, Feng D, Qi K, He Y, Wang J, Wang H (2012) Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24: 3406-3419
26. Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164: 969-979
27. 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. Proc Natl Acad Sci USA 104: 19613-19618
28. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321-4326
29. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41
30. Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, Lacombe S, Rougon A, Bittel P, Kiss Papp M, Chinchilla D, van Esse HP, Jorda L, Schwessinger B, Nicaise V, Thomma B, Molina A, Jones JDG, Zipfel C (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J 28: 3428-3438
31. Nimchuk Z, Eulgem T, Holt Iii BF, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37: 579-609
32. Niño Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: Model pathogens of a model crop. Mol Plant Pathol 7: 303-324
33. Ochiai H, Inoue Y, Takeya M, Sasaki A, Kaku H (2005) Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jpn Agr Res 39: 275
34. Ozawa K (2009) Establishment of a high efficiency Agrobacterium-mediated transformation system of rice (Oryza sativa L.). Plant Sci 176: 522-527
35. Ozawa K, Komamine A (1989) Establishment of a system of high-frequency embryogenesis from long-term cell suspension cultures of rice (Oryza sativa L.). Theor Appl Genet 77: 205-211
36. Peng Y, Shishiyama J (1988) Temporal sequence of cytological events in rice leaves infected with Pyricularia oryzae. Can J Bot 66: 730-735
37. Pérez FJ, Rubio S (2006) An improved chemiluminescence method for hydrogen peroxide determination in plant tissues. Plant Growth Regul 48: 89-95
38. Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate and jasmonate-dependent signaling. Mol Plant-Microbe Interact 20: 492-499
39. Ray SK, Rajeshwari R, Sonti RV (2000) Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol Plant-Microbe Interact 13: 394-401
40. Robatzek S, Bittel P, Chinchilla D, Köchner P, Felix G, Shiu S, Boller T (2007) Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol Biol 64: 539-547
41. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7: e1002046
42. Schwessinger B, Zipfel C (2008) News from the frontline: Recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389-395
43. Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64: 204-214
44. 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 Cell Physiol 53: 1696-1706
45. Skamnioti P, Gurr SJ (2009) Against the grain: Safeguarding rice from rice blast disease. Trends Biotechnol 27: 141-150
46. Song W, Wang G, Chen L, Kim H, Pi L, Holsten T, Gardner J, Wang B, Zhai W, Zhu L, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804-1806
47. Stuiver MH, Custers JH (2001) Engineering disease resistance in plants. Nature 411: 865-868
48. Sun W, Cao Y, Labby KJ, Bittel P, Boller T, Bent AF (2012) Probing the Arabidopsis flagellin receptor: FLS2-FLS2 association and the contributions of specific domains to signaling function. Plant Cell 24: 1096-1113
49. Sun X, Wang G (2011) Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS ONE 6: e16079
50. Takai R, Isogai A, Takayama S, Che F (2008) Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol Plant-Microbe Interact 21: 1635-1642
51. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77
52. Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378
53. Trdá L, Fernandez O, Boutrot F, Héloir MC, Kelloniemi J, Daire X, Adrian M, Clément C, Zipfel C, Dorey S, Poinssot B (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201: 1371-1384
54. 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 Biotechnol J 12: 663-673
55. Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55: 85-97
56. Wan J, Zhang X, Neece D, Ramonell KM, Clough S, Kim S, 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
57. Willems A, Goor M, Thielemans S, Gillis M, Kersters K, De Ley J (1992) Transfer of several phytopathogenic Pseudomonas species to Acidovorax as Acidovorax avenae subsp. avenae subsp. nov., comb. nov., Acidovorax avenae subsp. citrulli, Acidovorax avenae subsp. cattleyae, and Acidovorax konjaci. Int J Syst Bacteriol 42: 107-119
58. Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. J Integr Plant Biol 55: 1271-1286
59. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou J (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18: 74-80
60. Xiao S, Brown S, Patrick E, Brearley C, Turner JG (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15: 33-45
61. Zhang Y, Wei C, Jiang W, Wang L, Li C, Wang Y, Dow JM, Sun W (2013) The HD-GYP domain protein RpfG of Xanthomonas oryzae pv. oryzicola regulates synthesis of extracellular polysaccharides that contribute to biofilm formation and virulence on rice. PLoS ONE 8: e59428
62. Zhou Y, Xu M, Zhao M, Xie X, Zhu L, Fu B, Li Z (2010) Genome-wide gene responses in a transgenic rice line carrying the maize resistance gene Rxo1 to the rice bacterial streak pathogen, Xanthomonas oryzae pv. oryzicola. BMC Genomics 11: 78
63. Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35: 345-351
64. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760
65. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767