Cell Wall Degrading Enzyme Induced Rice Innate Immune Responses Are Suppressed by the Type 3 Secretion System Effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Sinha, Dipanwita ^a   Gupta, Mahesh Kumar ^a   Patel, Hitendra Kumar ^a,b   Ranjan, Ashish ^a   Sonti, Ramesh V ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACID LIPASE; BACTERIAL PROTEIN; UNCLASSIFIED DRUG; XOPQ PROTEIN; XOPX PROTEIN; XOPZ PROTEIN;

APOPTOSIS; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CALLOSE DEPOSITION; CELL DAMAGE; CONTROLLED STUDY; ENZYME REPRESSION; GENE MUTATION; GENE TRANSFER; HOST PATHOGEN INTERACTION; INNATE IMMUNITY; MUTANT; NONHUMAN; PLANT IMMUNITY; PLANT LEAF; RHIZOBIUM; RICE; XANTHOMONAS ORYZAE; XOPN GENE; XOPQ GENE; XOPX GENE; XOPZ GENE;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA PRIMERS; GENE TRANSFER TECHNIQUES; GENES, BACTERIAL; GENETIC VECTORS; GLUCANS; IMMUNITY, INNATE; MUTAGENESIS; ORYZA SATIVA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; VIRULENCE; XANTHOMONAS;

EID: 84884642216     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075867     Document Type: Article

References (54)

1. Nürnberger T, Brunner F, Kemmerling B, Piater L, (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249-266. doi:10.1111/j.0105-2896.2004.0119.x. PubMed: 15199967.
2. Cunha C, Carvalho A, Esposito A, Bistoni F, Romani L, (2012) DAMP signaling in fungal infections and diseases. Front Immunol 3: 286. PubMed: 22973279.
3. Gallucci S, Matzinger P, (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13: 114-119. doi:10.1016/S0952-7915(00)00191-6. PubMed: 11154927.
4. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323-329. doi:10.1038/nature05286. PubMed: 17108957.
5. Göhre V, Robatzek S, (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46: 189-215. doi:10.1146/annurev.phyto.46.120407.110050. PubMed: 18422429.
6. Swords KM, Dahlbeck D, Kearney B, Roy M, Staskawicz BJ, (1996) Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J Bacteriol 178: 4661-4669. PubMed: 8755898.
7. Roden JA, Belt B, Ross JB, Tachibana T, Vargas J, et al. (2004) A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc Natl Acad Sci U S A 101: 16624-16629. doi:10.1073/pnas.0407383101. PubMed: 15545602.
8. Kim JG, Li X, Roden JA, Taylor KW, Aakre CD, et al. (2009) Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell 21: 1305-1323. doi:10.1105/tpc.108.063123. PubMed: 19366901.
9. Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, et al. (2009) The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Mol Plant Microbe Interact 22: 655-664. doi:10.1094/MPMI-22-6-0655. PubMed: 19445590.
10. Schulze S, Kay S, Büttner D, Egler M, Eschen-Lippold L, et al. (2012) Analysis of new type III effectors from Xanthomonas uncovers XopB and XopS as suppressors of plant immunity. New Phytol 195: 894-911. doi:10.1111/j.1469-8137.2012.04210.x. PubMed: 22738163.
11. Metz M, Dahlbeck D, Morales CQ, Al Sady B, Clark ET, et al. (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J 41: 801-814. doi:10.1111/j.1365-313X.2005.02338.x. PubMed: 15743446.
12. Kim JG, Taylor KW, Hotson A, Keegan M, Schmelz EA, et al. (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20: 1915-1929. doi:10.1105/tpc.108.058529. PubMed: 18664616.
13. Song C, Yang B, (2010) Mutagenesis of 18 Type III effectors reveals virulence function of XopZPXO99 in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 23: 893-902. doi:10.1094/MPMI-23-7-0893. PubMed: 20521952.
14. Akimoto-Tomiyama C, Furutani A, Tsuge S, Washington EJ, Nishizawa Y, et al. (2012) XopR, a type III effector secreted by Xanthomonas oryzae pv. oryzae, suppresses microbe-associated molecular pattern-triggered immunity in Arabidopsis thaliana. Mol Plant Microbe Interact 25: 505-514. doi:10.1094/MPMI-06-11-0167. PubMed: 22204644.
15. Kim JG, Park BK, Yoo CH, Jeon E, Oh J, et al. (2003) Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J Bacteriol 185: 3155-3166. PubMed: 12730176.
16. Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB, (2004) Characterization of the Xanthomonas AvrXv4 Effector, a SUMO protease translocated into plant cells. Mol Plant Microbe Interact 17: 633-643. PubMed: 15195946.
17. Wang L, Tang X, He C, (2007) The bifunctional effector AvrXccC of Xanthomonas campestris pv. campestris requires plasma membrane-anchoring for host recognition. Mol Plant Pathol 8: 491-501. PubMed: 20507516.
18. Albersheim P, Jones TM, English PD, (1969) Biochemistry of the cell wall in relation to infective processes. Annu Rev Phytopathol 7: 171-194. doi:10.1146/annurev.py.07.090169.001131. PubMed: 18554147.
19. Darvill AG, Albersheim P, (1984) Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu Rev Plant Physiol A 35: 243-275. doi:10.1146/annurev.pp.35.060184.001331.
20. Ryan CA, Farmer EE, (1991) Oligosaccharide signals in plants: a current assessment. Annu Rev Plant Physiol Plant Mol Biol 42: 651-674. doi:10.1146/annurev.pp.42.060191.003251.
21. Rajeshwari R, Jha G, Sonti RV, (2005) Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on rice. Mol Plant Microbe Interact 18: 830-837. doi:10.1094/MPMI-18-0830. PubMed: 16134895.
22. Jha G, Rajeshwari R, Sonti RV, (2007) Functional interplay between two Xanthomonas oryzae pv. oryzae secretion systems in modulating virulence on rice. Mol Plant Microbe Interact 20: 31-40. doi:10.1094/MPMI-20-0031. PubMed: 17249420.
23. Aparna G, Chatterjee A, Sonti RV, Sankaranarayanan R, (2009) A cell wall-degrading esterase of Xanthomonas oryzae requires a unique substrate recognition module for pathogenesis on rice. Plant Cell. 21: 1860-1873. doi:10.1105/tpc.109.066886. PubMed: 19525415.
24. Furutani A, Takaoka M, Sanada H, Noguchi Y, Oku T, et al. (2009) Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 22: 96-106. doi:10.1094/MPMI-22-1-0096. PubMed: 19061406.
25. Pennell RI, Lamb C, (1997) Programmed cell death in plants. Plant Cell 9: 1157-1168. doi:10.1105/tpc.9.7.1157. PubMed: 12237381.
26. Christensen AH, Quail PH, (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5: 213-218. PubMed: 8673150.
27. Bestwick CS, Bennett MH, Mansfield JW, (1995) Hrp mutant of Pseudomonas syringae pv. phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol 108: 503-516. PubMed: 12228488.
28. 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. PubMed: 19400727.
29. Huffaker A, Pearce G, Ryan CA, (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci U S A 103: 10098-10103. doi:10.1073/pnas.0603727103. PubMed: 16785434.
30. Taylor KW, Kim JG, Su XB, Aakre CD, Roden JA, et al. (2012) Tomato TFT1 is required for PAMP-triggered immunity and mutations that prevent T3S effector XopN from binding to TFT1 attenuate Xanthomonas virulence. PLOS Pathog 8: e1002768. PubMed: 22719257.
31. Cingolani G, Petosa C, Weis K, Müller CW, (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399: 221-229. doi:10.1038/20367. PubMed: 10353244.
32. Cheng Y, Dai X, Zhao Y, (2004) AtCAND1, a HEAT-repeat protein that participates in auxin signaling in Arabidopsis. Plant Physiol 135: 1020-1026. doi:10.1104/pp.104.044495. PubMed: 15181201.
33. Li W, Chiang YH, Coaker G, (2013) The HopQ1 effector's nucleoside hydrolase-like domain is required for bacterial virulence in Arabidopsis and tomato, but not host recognition in tobacco. PLOS ONE 8: e59684. PubMed: 23555744.
34. Giska F, Lichocka M, Piechocki M, Dadlez M, Schmelzer E, (2013) Phosphorylation of HopQ1, a type III effector from Pseudomonas syringae, creates a binding site for host 14-3-3 proteins. Plant Physiol 161: 2049-2061. doi:10.1104/pp.112.209023. PubMed: 23396834.
35. Ryan RP, Vorhölter FJ, Potnis N, Jones JB, Van Sluys MA, (2011) Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 9: 344-355. doi:10.1038/nrmicro2558. PubMed: 21478901.
36. Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics 10: 616. doi:10.1186/1471-2164-10-616. PubMed: 20017926.
37. Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genomics 9: 204. PubMed: 18452608.
38. Lee BM, Park YJ, Park DS, Kang HW, Kim JG, (2005) The genome sequence of Xanthomonas oryzae pv. oryzae KACC10331 the bacterial blight pathogen of rice. Nucleic Acids Res 33: 577-586. doi:10.1093/nar/gki591. PubMed: 15673718.
39. 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 Agric Res Q 39: 275-287.
40. Zhao S, Mo WL, Wu F, Tang W, Tang JL, et al. (2013) Identification of non-TAL effectors in Xanthomonas oryzae pv. oryzae Chinese strain 13751 and analysis of their role in the bacterial virulence. World J Microbiol Biotechnol 29: 733-744. doi:10.1007/s11274-012-1229-5. PubMed: 23296915.
41. 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. PubMed: 10755302.
42. Leach J, White F, Rhoads M, Leung H, (1990) A repetitive DNA sequence differentiates Xanthomonas campestris pv. oryzae from other pathovars of X. campestris. Mol Plant Microbe Interact 3: 238-246.
43. Sambrook J, Fritsch E, Maniatis T, (1989) Molecular cloning: A laboratory manual.
44. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. doi:10.1016/S0022-2836(05)80360-2. PubMed: 2231712.
45. Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, et al. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73. doi:10.1016/0378-1119(94)90324-7. PubMed: 8045426.
46. Windgassen M, Urban A, Jaeger KE, (2000) Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol Lett 193: 201-205. doi:10.1111/j.1574-6968.2000.tb09424.x. PubMed: 11111024.
47. Pandey A, Sonti RV, (2010) Role of the FeoB protein and siderophore in promoting virulence of Xanthomonas oryzae pv. oryzae on Rice. J Bacteriol 192: 3187-3203. doi:10.1128/JB.01558-09. PubMed: 20382771.
48. Innes RW, Hirose MA, Kuempel PL, (1988) Induction of nitrogen-fixing nodules on clover requires only 32 kilobase pairs of DNA from the Rhizobium trifolii symbiosis plasmid. J Bacteriol 170: 3793-3802. PubMed: 3410817.
49. Hauck P, Thilmony R, He SY, (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A 100: 8577-8582. doi:10.1073/pnas.1431173100. PubMed: 12817082.
50. Kauffman HE, Reddy APK, Hsieh SPY, Merca SD, (1973) An improved technique for evaluation of resistance of rice varieties to Xanthomonas oryzae. Plant Dis Rep 57: 537-541.
51. Curtis MD, Grossniklaus U, (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469. PubMed: 14555774.
52. Simon R, Priefer U, Puhler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1: 784-791.
53. Hood EE, Helmer GL, Fraley RT, Chilton MD, (1986) The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J Bacteriol 168: 1291-1301. PubMed: 3782037.
54. Hood EE, Gelvin SB, Melchers LS, Hoekema A, (1993) New Agrobacterium helper plasmids for gene transfer to plants. Transgenic Res 2: 208-218. doi:10.1007/BF01977351.