Xanthomonas campestris cell-cell signalling molecule DSF (diffusible signal factor) elicits innate immunity in plants and is suppressed by the exopolysaccharide xanthan

Journal of Experimental Botany

Volumn 66, Issue 21, 2015, Pages 6697-6714

  Kakkar, Akanksha ^a,b   Nizampatnam, Narasimha Rao ^a   Kondreddy, Anil ^a   Pradhan, Binod Bihari ^a   Chatterjee, Subhadeep ^a  

^a CENTRE FOR DNA FINGERPRINTING AND DIAGNOSTICS   (India)

^b MANIPAL UNIVERSITY   (India)

Author keywords

Defence suppressor; Elicitor; Extracellular polysaccharide; Innate immunity; Nicotiana benthamiana; Quorum sensing; Rice; Virulence; Xanthomonas campestris pv. campestris; Xanthomonas oryzae pv. oryzae

Indexed keywords

BACTERIAL POLYSACCHARIDE; XANTHAN;

GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PLANT DISEASE; PLANT IMMUNITY; SIGNAL TRANSDUCTION; TOBACCO; XANTHOMONAS CAMPESTRIS;

PLANT DISEASES; PLANT IMMUNITY; POLYSACCHARIDES, BACTERIAL; SIGNAL TRANSDUCTION; TOBACCO; XANTHOMONAS CAMPESTRIS;

EID: 84948434101     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv377     Document Type: Article

References (68)

1. Adam L, Somerville SC. 1996. Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. The Plant Journal 9, 341-356.
2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402.
3. 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. The Plant Cell 21, 1860-1873.
4. Aslam SN, Newman MA, Erbs G, et al. 2008. Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Current Biology 18, 1078-1083.
5. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJG, Slater H, Dow JM, Williams P, Daniels MJ. 1997. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Molecular Microbiology 24, 555-566.
6. Beaulieu ED, Ionescu M, Chatterjee S, Yokota K, Trauner D, Lindow S. 2013. Characterization of a diffusible signaling factor from Xylella fastidiosa. MBio 4, e00539-12.
7. Bestwick, CS, Bennett MH, Mansfield JW. 1995. Hrp mutant of Pseudomonas syringae pv. phaseolicola induces cell wall alteration but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiology 108, 503-516.
8. Bi H, Christensen QH, Feng Y, Wang H, Cronan JE. 2012. The Burkholderia cenocepacia BDSF quorum sensing fatty acid is synthesized by a bifunctional crotonase homologue having both dehydratase and thioesterase activities. Molecular Microbiology 83, 840-855.
9. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379-406.
10. Boon C, Deng Y, Wang LH, He Y, Xu JL, Fan Y, Pan SQ, Zhang LH. 2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME Journal 2, 27-36.
11. Bostock RM. 2005 Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annual Review of Phytopathology 43, 545-580.
12. Bostock RM, Kuc JA, Laine RA. 1981. Eicosapentaenoic and arachidonic acids from Phytophthora infestans elicit fungitoxic sesquiterpenes in the potato. Science 212, 67-69.
13. Bostock RM, Yamamoto H, Choi D, Ricker KE, Ward BL. 1992. Rapid stimulation of 5-lipoxygenase activity in potato by the fungal elicitor arachidonic acid. Plant Physiology 100, 1448-1456.
14. Büttner D, Bonas U. 2010. Regulation and secretion of Xanthomonas virulence factors. FEMS Reviews 34, 107-133.
15. Chatterjee S, Sonti RV. 2002. rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. Molecular Plant-Microbe Interactions 15, 463-471.
16. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803-814.
17. Darvill AG, Albersheim P. 1984. Phytoalexins and their elicitors-a defense against microbial infection in plants. Annual Review of Plant Physiology and Plant Molecular Biology 35, 243-275.
18. DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY. 2004. A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proceedings of the National Academy of Sciences, USA 101, 9927-9932.
19. Deng Y, Wu, J, Tao F, Zhang LH. 2011. Listening to a new language: DSF-based quorum sensing in gram-negative bacteria. Chemical Reviews 111, 160-173.
20. 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. Journal of Biological Chemistry 278, 6201-6208.
21. Felix G, Duran JD, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. The Plant Journal 18, 265-276.
22. Fuqua C, Parsek MR, Greenberg EP. 2001. Regulation of gene expression by cell-cell communication: acyl-homoserine lactone quorum sensing. Annual Review of Genetics 35, 4439-4468.
23. Fuqua WC, Winans SC, Greenberg EP. 1994. Quorum sensing in bacteria: the LuxR LuxI family of cell density-responsive transcriptional regulators. Journal of Bacteriology 176, 269-275.
24. Gudesblat GE, Torres PS, Vojnov AA. 2009. Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-tocell signal-regulated virulence factor. Plant Physiology 149, 1017-1027.
25. Hann DR, Rathjen JP. 2007. Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. The Plant Journal 49, 607-618.
26. Hauck P, Thilmony R, He SY. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proceedings of the National Academy of Sciences, USA 100, 8577-8582.
27. He Y-W, Wu J, Cha JS, Zhang LH. 2010. Rice bacterial blight pathogen Xanthomonas oryzae pv. oryzae produces multiple DSF-family signals in regulation of virulence factor production. BMC Microbiology 10, 187.
28. Jaffe MJ, Leopold AC. 1984. Callose deposition during gravitropism of Zea mays and Pisum sativum and its inhibition by 2-deoxy-D-glucose. Planta 161, 20-26.
29. Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer A, Alfano JR. 2004. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. The Plant Journal 37, 554-565.
30. Jha G, Rajeshwari R, Sonti RV. 2007. Functional interplay between two Xanthomonas oryzae pv. oryzae secretion systems in modulating virulence on rice. Molecular Plant-Microbe Interactions 20, 31-40.
31. Kachroo P, Kachroo A, Lapchyk L, Hildebrand D, Klessig DF. 2003. Restoration of defective cross talk in ssi2 mutants: role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Molecular Plant-Microbe Interactions 16, 1022-1029.
32. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig, DF. 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proceedings of the National Academy of Sciences, USA 98, 9448-9453.
33. 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.
34. Knight VI, Wang H, Lincoln J.-E., Lulai, EC, Gilchrist DG, Bostock RM. 2001. Hydroperoxides of fatty acids induce programmed cell death in tomato protoplasts. Physiological and Molecular Plant Pathology 59, 277-286.
35. Koch E, Slusarenko A. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. The Plant Cell 2, 437-445.
36. 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. The Plant Cell 16, 3496-3507.
37. Larsen RA, Wilson MM, Guss AM, Metcalf WW. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Archives of Microbiology 178, 193-201.
38. Loper JE, Lindow SE. 1987 Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77, 1449-1454.
39. Mansfield J, Genin S, Magori S, et al. 2012 Top 10 plant pathogenic bacteria in molecular plant pathology. Molecular Plant Patholology 13, 614-629.
40. Newman KL, Almeida RPP, Purcell, AH, Lindow SE. 2004. Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. Proceedings of the National Academy of Sciences, USA 101, 1737-1742.
41. Newman KL, Chatterjee S, Ho KA, Lindow SE. 2008. Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. Molecular Plant-Microbe Interactions 21, 326-334.
42. Newman M-A, Lahaye ER, Parr A, Daniels MJ, Dow JM. 2002. Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. The Plant Journal 29, 487-495.
43. Ng W-L, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Annual Review of Genetics 43, 197-222.
44. Nguyen HP, Chakravarthy S, Velásquez AC, McLane HL, Zeng L, Nakayashiki H, Park DH, Collmer A, Martin GB. 2010. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Molecular Plant-Microbe Interactions 23, 991-999.
45. Niňo-Liu DO, Ronald PC, Bogdanove AJ. 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology 7, 303-324.
46. Nurnberger T, Brunner F, Kemmerling B, Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunology Reviews 198, 249-266.
47. Pennell RI, Lamb C. 1997. Programmed cell death in plants. The Plant Cell 9, 1157-1168.
48. Pradhan BB, Chatterjee S. 2014. Reversible non-genetic phenotypic heterogeneity in bacterial quorum sensing. Molecular Microbiology 92, 557-569.
49. Quiñones B, Pujol CJ, Lindow SE. 2004. Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae. Molecular Plant-Microbe Interactions 17, 521-531.
50. Rai R, Pradhan BB, Ranjan M, Chatterjee S. 2012. Atypical regulation of virulence associated functions by a diffusible signal factor in Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions 25, 789-801.
51. Rigano LA, Payette C, Brouillard G, et al. 2007. Bacterial cyclic beta-(1, 2)-glucan acts in systemic suppression of plant immune responses. The Plant Cell 19, 2077-2089.
52. Ryan RP, Dow JM. 2011. Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends in Microbiology 19, 145-152.
53. Savchenko T, Walley JW, Chehab EW, Xiao Y, Kaspi R, Pye MF, Mohamed ME, Lazarus CM, Bostock RM, Dehesh K. 2010. Arachidonic acid: an evolutionarily conserved signaling molecule modulates plant stress signaling networks. The Plant Cell 22, 3193-205.
54. Schafer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A. 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 glutumicum. Gene 145, 69-73.
55. Schenk ST, Hernández-Reyes C, Samans B, et al. 2014. N-Acylhomoserine lactone primes plants for cell wall reinforcement and induces resistance to bacterial pathogens via the salicylic acid/oxylipin pathway. The Plant Cell 26, 2708-2723.
56. Shepherd RW, Lindow SE. 2009. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Applied and Environmental Microbiology 75, 45-53.
57. Siciliano F, Torres P, Sendin L, Bermejo C, Filippone P, Vellice G, Ramallo J, Castagnaro A, Vojnov A, Marano MR. 2006. Analysis of the molecular basis of Xanthomonasaxonopodis pv. citripathogenesis in Citrus limon. Electronic Journal of Biotechnology 9, 199.
58. Silipo A, Molinaro A, Sturiale L, Dow JM, Erbs G, Lanzetta R, Newman MA, Parrilli M. 2005. The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. Journal of Biological Chemistry 280, 33660-33668.
59. Stone JM, Heard JE, Asai T, Ausubel, FM. 2000. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. The Plant Cell 12, 1811-1822.
60. 2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. The Plant Journal 11, 1187-1194.
61. Thowthampitak J, Shaffer BT, Prathuangwong S, Loper JE. 2008. Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean. Phytopathology 98, 1252-1260.
62. Tsuchiya K, Mew TW, Wakimoto S. 1982. Bacteriological and pathological characteristics of wild types and induced mutants of Xanthomonas campestris pv. oryzae. Phytopathology 72, 43-46.
63. Upchurch RG. 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters 30, 967-977.
64. Vinatzer BA, Teitzel GM, Lee MW, Jelenska J, Hotton S, Fairfax K, Jenrette J, Greenberg JT. 2006. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Molecular Microbiology 62, 26-44.
65. Wang LH, He Y, Gao Y, et al. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Molecular Microbiology 51, 903-912.
66. Windgassen M, Urban A, Jaeger KE. 2000. Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiology Letters 193, 201-205.
67. Wu H, Song Z, Hentzer M, et al. 2000. Detection of N-acylhomoserine lactones in lung tissues of mice infected with Pseudomonas aeruginosa. Microbiology 146, 2481-2493.
68. Yun MH, Torres PS, El Oirdi M, Rigano LA, Gonzalez-Lamothe R, Marano MR, Castagnaro AP, Dankert MA, Bouarab K, Vojnov AA. 2006. Xanthan induces plant susceptibility by suppressing callose deposition. Plant Physiology 141, 178-187.