Abstract
Plant-associated Pseudomonas live as saprophytes and parasites on plant surfaces and inside plant tissues. Many plant-associated Pseudomonas promote plant growth by suppressing pathogenic micro-organisms, synthesizing growth-stimulating plant hormones and promoting increased plant disease resistance. Others inhibit plant growth and cause disease symptoms ranging from rot and necrosis through to developmental dystrophies such as galls. It is not easy to draw a clear distinction between pathogenic and plant growth-promoting Pseudomonas. They colonize the same ecological niches and possess similar mechanisms for plant colonization. Pathogenic, saprophytic and plant growth-promoting strains are often found within the same species, and the incidence and severity of Pseudomonas diseases are affected by environmental factors and host-specific interactions. Plants are faced with the challenge of how to recognize and exclude pathogens that pose a genuine threat, while tolerating more benign organisms. This review examines Pseudomonas from a plant perspective, focusing in particular on the question of how plants perceive and are affected by saprophytic and plant growth-promoting Pseudomonas (PGPP), in contrast to their interactions with plant pathogenic Pseudomonas. A better understanding of the molecular basis of plant-PGPP interactions and of the key differences between pathogens and PGPP will enable researchers to make more informed decisions in designing integrated disease-control strategies and in selecting, modifying and using PGPP for plant growth promotion, bioremediation and biocontrol.
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- Abramovitch Robert B., Kim Young-Jin, Chen Shaorong, Dickman Martin B., Martin Gregory B. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 2003 Jan 2;22(1):60–69. doi: 10.1093/emboj/cdg006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Audenaert Kris, Pattery Theresa, Cornelis Pierre, Höfte Monica. Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact. 2002 Nov;15(11):1147–1156. doi: 10.1094/MPMI.2002.15.11.1147. [DOI] [PubMed] [Google Scholar]
- Axtell Michael J., Staskawicz Brian J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell. 2003 Feb 7;112(3):369–377. doi: 10.1016/s0092-8674(03)00036-9. [DOI] [PubMed] [Google Scholar]
- Bauer Wolfgang D., Robinson Jayne B. Disruption of bacterial quorum sensing by other organisms. Curr Opin Biotechnol. 2002 Jun;13(3):234–237. doi: 10.1016/s0958-1669(02)00310-5. [DOI] [PubMed] [Google Scholar]
- Bender C. L., Alarcón-Chaidez F., Gross D. C. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev. 1999 Jun;63(2):266–292. doi: 10.1128/mmbr.63.2.266-292.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bestwick C. S., Brown I. R., Bennett M. H., Mansfield J. W. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell. 1997 Feb;9(2):209–221. doi: 10.1105/tpc.9.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Björklöf K., Nurmiaho-Lassila E. L., Klinger N., Haahtela K., Romantschuk M. Colonization strategies and conjugal gene transfer of inoculated Pseudomonas syringae on the leaf surface. J Appl Microbiol. 2000 Sep;89(3):423–432. doi: 10.1046/j.1365-2672.2000.01130.x. [DOI] [PubMed] [Google Scholar]
- Bloemberg G. V., Lugtenberg B. J. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol. 2001 Aug;4(4):343–350. doi: 10.1016/s1369-5266(00)00183-7. [DOI] [PubMed] [Google Scholar]
- Blumer C., Haas D. Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol. 2000 Mar;173(3):170–177. doi: 10.1007/s002039900127. [DOI] [PubMed] [Google Scholar]
- Braun P. G., Hildebrand P. D., Ells T. C., Kobayashi D. Y. Evidence and characterization of a gene cluster required for the production of viscosin, a lipopeptide biosurfactant, by a strain of Pseudomonas fluorescens. Can J Microbiol. 2001 Apr;47(4):294–301. doi: 10.1139/w01-017. [DOI] [PubMed] [Google Scholar]
- Brown I. R., Mansfield J. W., Taira S., Roine E., Romantschuk M. Immunocytochemical localization of HrpA and HrpZ supports a role for the Hrp pilus in the transfer of effector proteins from Pseudomonas syringae pv. tomato across the host plant cell wall. Mol Plant Microbe Interact. 2001 Mar;14(3):394–404. doi: 10.1094/MPMI.2001.14.3.394. [DOI] [PubMed] [Google Scholar]
- Budde I. P., Ullrich M. S. Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. Mol Plant Microbe Interact. 2000 Sep;13(9):951–961. doi: 10.1094/MPMI.2000.13.9.951. [DOI] [PubMed] [Google Scholar]
- Büttner Daniela, Bonas Ulla. Getting across--bacterial type III effector proteins on their way to the plant cell. EMBO J. 2002 Oct 15;21(20):5313–5322. doi: 10.1093/emboj/cdf536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cao H., Baldini R. L., Rahme L. G. Common mechanisms for pathogens of plants and animals. Annu Rev Phytopathol. 2001;39:259–284. doi: 10.1146/annurev.phyto.39.1.259. [DOI] [PubMed] [Google Scholar]
- Cook D. R. Medicago truncatula--a model in the making! Curr Opin Plant Biol. 1999 Aug;2(4):301–304. doi: 10.1016/s1369-5266(99)80053-3. [DOI] [PubMed] [Google Scholar]
- Dangl J. L., Dietrich R. A., Richberg M. H. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell. 1996 Oct;8(10):1793–1807. doi: 10.1105/tpc.8.10.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Meyer G., Capieau K., Audenaert K., Buchala A., Métraux J. P., Höfte M. Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol Plant Microbe Interact. 1999 May;12(5):450–458. doi: 10.1094/MPMI.1999.12.5.450. [DOI] [PubMed] [Google Scholar]
- Dow Max, Newman Mari-Anne, von Roepenack Edda. THE INDUCTION AND MODULATION OF PLANT DEFENSE RESPONSES BY BACTERIAL LIPOPOLYSACCHARIDES. Annu Rev Phytopathol. 2000;38(NaN):241–261. doi: 10.1146/annurev.phyto.38.1.241. [DOI] [PubMed] [Google Scholar]
- Felix G., Duran J. D., Volko S., Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 1999 May;18(3):265–276. doi: 10.1046/j.1365-313x.1999.00265.x. [DOI] [PubMed] [Google Scholar]
- Ferguson M. W., Maxwell J. A., Vincent T. S., da Silva J., Olson J. C. Comparison of the exoS gene and protein expression in soil and clinical isolates of Pseudomonas aeruginosa. Infect Immun. 2001 Apr;69(4):2198–2210. doi: 10.1128/IAI.69.4.2198-2210.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finkel Toren. Oxidant signals and oxidative stress. Curr Opin Cell Biol. 2003 Apr;15(2):247–254. doi: 10.1016/s0955-0674(03)00002-4. [DOI] [PubMed] [Google Scholar]
- Flores HE, Vivanco JM, Loyola-Vargas VM. 'Radicle' biochemistry: the biology of root-specific metabolism. Trends Plant Sci. 1999 Jun;4(6):220–226. doi: 10.1016/s1360-1385(99)01411-9. [DOI] [PubMed] [Google Scholar]
- Foreman Julia, Demidchik Vadim, Bothwell John H. F., Mylona Panagiota, Miedema Henk, Torres Miguel Angel, Linstead Paul, Costa Silvia, Brownlee Colin, Jones Jonathan D. G. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature. 2003 Mar 27;422(6930):442–446. doi: 10.1038/nature01485. [DOI] [PubMed] [Google Scholar]
- Gage D. J., Margolin W. Hanging by a thread: invasion of legume plants by rhizobia. Curr Opin Microbiol. 2000 Dec;3(6):613–617. doi: 10.1016/s1369-5274(00)00149-1. [DOI] [PubMed] [Google Scholar]
- Gilroy S., Jones D. L. Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 2000 Feb;5(2):56–60. doi: 10.1016/s1360-1385(99)01551-4. [DOI] [PubMed] [Google Scholar]
- Greenberg Jean T., Vinatzer Boris A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol. 2003 Feb;6(1):20–28. doi: 10.1016/s1369-5274(02)00004-8. [DOI] [PubMed] [Google Scholar]
- Gómez-Gómez L., Felix G., Boller T. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 1999 May;18(3):277–284. doi: 10.1046/j.1365-313x.1999.00451.x. [DOI] [PubMed] [Google Scholar]
- Gómez-Gómez Lourdes, Boller Thomas. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 2002 Jun;7(6):251–256. doi: 10.1016/s1360-1385(02)02261-6. [DOI] [PubMed] [Google Scholar]
- Haefele D. M., Lindow S. E. Flagellar Motility Confers Epiphytic Fitness Advantages upon Pseudomonas syringae. Appl Environ Microbiol. 1987 Oct;53(10):2528–2533. doi: 10.1128/aem.53.10.2528-2533.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hawes M. C., Gunawardena U., Miyasaka S., Zhao X. The role of root border cells in plant defense. Trends Plant Sci. 2000 Mar;5(3):128–133. doi: 10.1016/s1360-1385(00)01556-9. [DOI] [PubMed] [Google Scholar]
- He Sheng Yang, Jin Qiaoling. The Hrp pilus: learning from flagella. Curr Opin Microbiol. 2003 Feb;6(1):15–19. doi: 10.1016/s1369-5274(02)00007-3. [DOI] [PubMed] [Google Scholar]
- Holt Ben F., 3rd, Hubert David A., Dangl Jeffery L. Resistance gene signaling in plants--complex similarities to animal innate immunity. Curr Opin Immunol. 2003 Feb;15(1):20–25. doi: 10.1016/s0952-7915(02)00014-6. [DOI] [PubMed] [Google Scholar]
- Jamet Alexandre, Sigaud Samuel, Van de Sype Ghislaine, Puppo Alain, Hérouart Didier. Expression of the bacterial catalase genes during Sinorhizobium meliloti-Medicago sativa symbiosis and their crucial role during the infection process. Mol Plant Microbe Interact. 2003 Mar;16(3):217–225. doi: 10.1094/MPMI.2003.16.3.217. [DOI] [PubMed] [Google Scholar]
- Kang Li, Li Jianxiong, Zhao Tiehan, Xiao Fangming, Tang Xiaoyan, Thilmony Roger, He ShengYang, Zhou Jian-Min. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci U S A. 2003 Mar 7;100(6):3519–3524. doi: 10.1073/pnas.0637377100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kjemtrup S., Nimchuk Z., Dangl J. L. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr Opin Microbiol. 2000 Feb;3(1):73–78. doi: 10.1016/s1369-5274(99)00054-5. [DOI] [PubMed] [Google Scholar]
- Kremer R. J., Souissi T. Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol. 2001 Sep;43(3):182–186. doi: 10.1007/s002840010284. [DOI] [PubMed] [Google Scholar]
- Kunkel Barbara N., Brooks David M. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol. 2002 Aug;5(4):325–331. doi: 10.1016/s1369-5266(02)00275-3. [DOI] [PubMed] [Google Scholar]
- Kus Julianne V., Zaton Kasia, Sarkar Raani, Cameron Robin K. Age-related resistance in Arabidopsis is a developmentally regulated defense response to Pseudomonas syringae. Plant Cell. 2002 Feb;14(2):479–490. doi: 10.1105/tpc.010481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lambrecht M., Okon Y., Vande Broek A., Vanderleyden J. Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol. 2000 Jul;8(7):298–300. doi: 10.1016/s0966-842x(00)01732-7. [DOI] [PubMed] [Google Scholar]
- Lindow Steven E., Brandl Maria T. Microbiology of the phyllosphere. Appl Environ Microbiol. 2003 Apr;69(4):1875–1883. doi: 10.1128/AEM.69.4.1875-1883.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loh John, Pierson Elizabeth A., Pierson Leland S., 3rd, Stacey Gary, Chatterjee Arun. Quorum sensing in plant-associated bacteria. Curr Opin Plant Biol. 2002 Aug;5(4):285–290. doi: 10.1016/s1369-5266(02)00274-1. [DOI] [PubMed] [Google Scholar]
- Lugtenberg B. J., Dekkers L., Bloemberg G. V. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol. 2001;39:461–490. doi: 10.1146/annurev.phyto.39.1.461. [DOI] [PubMed] [Google Scholar]
- Lyczak J. B., Cannon C. L., Pier G. B. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2000 Jul;2(9):1051–1060. doi: 10.1016/s1286-4579(00)01259-4. [DOI] [PubMed] [Google Scholar]
- Ma Qinhong, Zhai Yufeng, Schneider Jane C., Ramseier Tom M., Saier Milton H., Jr Protein secretion systems of Pseudomonas aeruginosa and P fluorescens. Biochim Biophys Acta. 2003 Apr 1;1611(1-2):223–233. doi: 10.1016/s0005-2736(03)00059-2. [DOI] [PubMed] [Google Scholar]
- Mackey David, Belkhadir Youssef, Alonso Jose M., Ecker Joseph R., Dangl Jeffery L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell. 2003 Feb 7;112(3):379–389. doi: 10.1016/s0092-8674(03)00040-0. [DOI] [PubMed] [Google Scholar]
- Magor B. G., Magor K. E. Evolution of effectors and receptors of innate immunity. Dev Comp Immunol. 2001 Oct-Dec;25(8-9):651–682. doi: 10.1016/s0145-305x(01)00029-5. [DOI] [PubMed] [Google Scholar]
- Mahajan-Miklos S., Rahme L. G., Ausubel F. M. Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol Microbiol. 2000 Sep;37(5):981–988. doi: 10.1046/j.1365-2958.2000.02056.x. [DOI] [PubMed] [Google Scholar]
- Mahajan-Miklos S., Tan M. W., Rahme L. G., Ausubel F. M. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell. 1999 Jan 8;96(1):47–56. doi: 10.1016/s0092-8674(00)80958-7. [DOI] [PubMed] [Google Scholar]
- Manefield M., de Nys R., Kumar N., Read R., Givskov M., Steinberg P., Kjelleberg S. Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology. 1999 Feb;145(Pt 2):283–291. doi: 10.1099/13500872-145-2-283. [DOI] [PubMed] [Google Scholar]
- Marie C., Broughton W. J., Deakin W. J. Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol. 2001 Aug;4(4):336–342. doi: 10.1016/s1369-5266(00)00182-5. [DOI] [PubMed] [Google Scholar]
- Mathesius Ulrike, Mulders Susan, Gao Mengsheng, Teplitski Max, Caetano-Anolles Gustavo, Rolfe Barry G., Bauer Wolfgang D. Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A. 2003 Jan 2;100(3):1444–1449. doi: 10.1073/pnas.262672599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matzinger P. An innate sense of danger. Semin Immunol. 1998 Oct;10(5):399–415. doi: 10.1006/smim.1998.0143. [DOI] [PubMed] [Google Scholar]
- Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 1994;12:991–1045. doi: 10.1146/annurev.iy.12.040194.005015. [DOI] [PubMed] [Google Scholar]
- Mittal S., Davis K. R. Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact. 1995 Jan-Feb;8(1):165–171. doi: 10.1094/mpmi-8-0165. [DOI] [PubMed] [Google Scholar]
- Moran P. J., Thompson G. A. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 2001 Feb;125(2):1074–1085. doi: 10.1104/pp.125.2.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson K. E., Weinel C., Paulsen I. T., Dodson R. J., Hilbert H., Martins dos Santos V. A. P., Fouts D. E., Gill S. R., Pop M., Holmes M. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol. 2002 Dec;4(12):799–808. doi: 10.1046/j.1462-2920.2002.00366.x. [DOI] [PubMed] [Google Scholar]
- Newman Mari-Anne, von Roepenack-Lahaye Edda, Parr Adrian, Daniels Michael J., Dow J. Maxwell. Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J. 2002 Feb;29(4):487–495. doi: 10.1046/j.0960-7412.2001.00233.x. [DOI] [PubMed] [Google Scholar]
- Nielsen T. H., Christophersen C., Anthoni U., Sørensen J. Viscosinamide, a new cyclic depsipeptide with surfactant and antifungal properties produced by Pseudomonas fluorescens DR54. J Appl Microbiol. 1999 Jul;87(1):80–90. doi: 10.1046/j.1365-2672.1999.00798.x. [DOI] [PubMed] [Google Scholar]
- Nielsen Tommy Harder, Sørensen Jan. Production of cyclic lipopeptides by Pseudomonas fluorescens strains in bulk soil and in the sugar beet rhizosphere. Appl Environ Microbiol. 2003 Feb;69(2):861–868. doi: 10.1128/AEM.69.2.861-868.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nimchuk Z., Rohmer L., Chang J. H., Dangl J. L. Knowing the dancer from the dance: R-gene products and their interactions with other proteins from host and pathogen. Curr Opin Plant Biol. 2001 Aug;4(4):288–294. doi: 10.1016/s1369-5266(00)00175-8. [DOI] [PubMed] [Google Scholar]
- Nürnberger Thorsten, Brunner Frédéric. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr Opin Plant Biol. 2002 Aug;5(4):318–324. doi: 10.1016/s1369-5266(02)00265-0. [DOI] [PubMed] [Google Scholar]
- Perret X., Staehelin C., Broughton W. J. Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev. 2000 Mar;64(1):180–201. doi: 10.1128/mmbr.64.1.180-201.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Plotnikova J. M., Rahme L. G., Ausubel F. M. Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol. 2000 Dec;124(4):1766–1774. doi: 10.1104/pp.124.4.1766. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Preston G. M., Bertrand N., Rainey P. B. Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol. 2001 Sep;41(5):999–1014. doi: 10.1046/j.1365-2958.2001.02560.x. [DOI] [PubMed] [Google Scholar]
- Preston G. M., Haubold B., Rainey P. B. Bacterial genomics and adaptation to life on plants: implications for the evolution of pathogenicity and symbiosis. Curr Opin Microbiol. 1998 Oct;1(5):589–597. doi: 10.1016/s1369-5274(98)80094-5. [DOI] [PubMed] [Google Scholar]
- Pukatzki Stefan, Kessin Richard H., Mekalanos John J. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc Natl Acad Sci U S A. 2002 Feb 26;99(5):3159–3164. doi: 10.1073/pnas.052704399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rabin Shira D. P., Hauser Alan R. Pseudomonas aeruginosa ExoU, a toxin transported by the type III secretion system, kills Saccharomyces cerevisiae. Infect Immun. 2003 Jul;71(7):4144–4150. doi: 10.1128/IAI.71.7.4144-4150.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rainey P. B. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ Microbiol. 1999 Jun;1(3):243–257. doi: 10.1046/j.1462-2920.1999.00040.x. [DOI] [PubMed] [Google Scholar]
- Ramonell Katrina M., Somerville Shauna. The genomics parade of defense responses: to infinity and beyond. Curr Opin Plant Biol. 2002 Aug;5(4):291–294. doi: 10.1016/s1369-5266(02)00266-2. [DOI] [PubMed] [Google Scholar]
- Roy-Burman A., Savel R. H., Racine S., Swanson B. L., Revadigar N. S., Fujimoto J., Sawa T., Frank D. W., Wiener-Kronish J. P. Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis. 2001 May 17;183(12):1767–1774. doi: 10.1086/320737. [DOI] [PubMed] [Google Scholar]
- Ryu Choong-Min, Farag Mohamed A., Hu Chia-Hui, Reddy Munagala S., Wei Han-Xun, Paré Paul W., Kloepper Joseph W. Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A. 2003 Apr 8;100(8):4927–4932. doi: 10.1073/pnas.0730845100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saliba Alessandra Mattos, Filloux Alain, Ball Geneviève, Silva Anamaria S. V., Assis Maria-Cristina, Plotkowski Maria-Cristina. Type III secretion-mediated killing of endothelial cells by Pseudomonas aeruginosa. Microb Pathog. 2002 Oct;33(4):153–166. [PubMed] [Google Scholar]
- Santos R., Franza T., Laporte M. L., Sauvage C., Touati D., Expert D. Essential role of superoxide dismutase on the pathogenicity of Erwinia chrysanthemi strain 3937. Mol Plant Microbe Interact. 2001 Jun;14(6):758–767. doi: 10.1094/MPMI.2001.14.6.758. [DOI] [PubMed] [Google Scholar]
- Schneider David S. Plant immunity and film Noir: what gumshoe detectives can teach us about plant-pathogen interactions. Cell. 2002 May 31;109(5):537–540. doi: 10.1016/s0092-8674(02)00764-x. [DOI] [PubMed] [Google Scholar]
- Shao Feng, Merritt Peter M., Bao Zhaoqin, Innes Roger W., Dixon Jack E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell. 2002 May 31;109(5):575–588. doi: 10.1016/s0092-8674(02)00766-3. [DOI] [PubMed] [Google Scholar]
- Smith Kevin P., Goodman Robert M. HOST VARIATION FOR INTERACTIONS WITH BENEFICIAL PLANT-ASSOCIATED MICROBES. Annu Rev Phytopathol. 1999;37(NaN):473–491. doi: 10.1146/annurev.phyto.37.1.473. [DOI] [PubMed] [Google Scholar]
- Stuber Katja, Frey Joachim, Burnens André P., Kuhnert Peter. Detection of type III secretion genes as a general indicator of bacterial virulence. Mol Cell Probes. 2003 Feb;17(1):25–32. doi: 10.1016/s0890-8508(02)00108-1. [DOI] [PubMed] [Google Scholar]
- Taguchi Fumiko, Shimizu Rena, Inagaki Yoshishige, Toyoda Kazuhiro, Shiraishi Tomonori, Ichinose Yuki. Post-translational modification of flagellin determines the specificity of HR induction. Plant Cell Physiol. 2003 Mar;44(3):342–349. doi: 10.1093/pcp/pcg042. [DOI] [PubMed] [Google Scholar]
- Thanassi D. G., Hultgren S. J. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol. 2000 Aug;12(4):420–430. doi: 10.1016/s0955-0674(00)00111-3. [DOI] [PubMed] [Google Scholar]
- Thomashow L. S. Biological control of plant root pathogens. Curr Opin Biotechnol. 1996 Jun;7(3):343–347. doi: 10.1016/s0958-1669(96)80042-5. [DOI] [PubMed] [Google Scholar]
- Thrane C, Harder Nielsen T, Neiendam Nielsen M, Sørensen J, Olsson S. Viscosinamide-producing Pseudomonas fluorescens DR54 exerts a biocontrol effect on Pythium ultimum in sugar beet rhizosphere. FEMS Microbiol Ecol. 2000 Aug 1;33(2):139–146. doi: 10.1111/j.1574-6941.2000.tb00736.x. [DOI] [PubMed] [Google Scholar]
- Timmusk S., Wagner E. G. The plant-growth-promoting rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol Plant Microbe Interact. 1999 Nov;12(11):951–959. doi: 10.1094/MPMI.1999.12.11.951. [DOI] [PubMed] [Google Scholar]
- Ton J., Davison S., Van Wees S. C., Van Loon L., Pieterse C. M. The arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiol. 2001 Feb;125(2):652–661. doi: 10.1104/pp.125.2.652. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ton J., Pieterse C. M., Van Loon L. C. Identification of a locus in arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact. 1999 Oct;12(10):911–918. doi: 10.1094/MPMI.1999.12.10.911. [DOI] [PubMed] [Google Scholar]
- Ton Jurriaan, De Vos Martin, Robben Charlotte, Buchala Anthony, Métraux Jean-Pierre, Van Loon L. C., Pieterse Corné M. J. Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J. 2002 Jan;29(1):11–21. doi: 10.1046/j.1365-313x.2002.01190.x. [DOI] [PubMed] [Google Scholar]
- Ton Jurriaan, Van Pelt Johan A., Van Loon L. C., Pieterse Corné M. J. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis. Mol Plant Microbe Interact. 2002 Jan;15(1):27–34. doi: 10.1094/MPMI.2002.15.1.27. [DOI] [PubMed] [Google Scholar]
- Van Wees S. C., Pieterse C. M., Trijssenaar A., Van 't Westende Y. A., Hartog F., Van Loon L. C. Differential induction of systemic resistance in Arabidopsis by biocontrol bacteria. Mol Plant Microbe Interact. 1997 Aug;10(6):716–724. doi: 10.1094/MPMI.1997.10.6.716. [DOI] [PubMed] [Google Scholar]
- Venisse Jean-Stéphane, Barny Marie-Anne, Paulin Jean-Pierre, Brisset Marie-Noëlle. Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS Lett. 2003 Feb 27;537(1-3):198–202. doi: 10.1016/s0014-5793(03)00123-6. [DOI] [PubMed] [Google Scholar]
- Von Bodman Susanne B., Bauer W. Dietz, Coplin David L. Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol. 2003 Apr 29;41:455–482. doi: 10.1146/annurev.phyto.41.052002.095652. [DOI] [PubMed] [Google Scholar]
- Wan Jinrong, Dunning F. Mark, Bent Andrew F. Probing plant-pathogen interactions and downstream defense signaling using DNA microarrays. Funct Integr Genomics. 2002 Oct 17;2(6):259–273. doi: 10.1007/s10142-002-0080-4. [DOI] [PubMed] [Google Scholar]
- Weingart H., Volksch B. Ethylene Production by Pseudomonas syringae Pathovars In Vitro and In Planta. Appl Environ Microbiol. 1997 Jan;63(1):156–161. doi: 10.1128/aem.63.1.156-161.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wisniewski M., Lindow S. E., Ashworth E. N. Observations of Ice Nucleation and Propagation in Plants Using Infrared Video Thermography. Plant Physiol. 1997 Feb;113(2):327–334. doi: 10.1104/pp.113.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wolfgang Matthew C., Lee Vincent T., Gilmore Meghan E., Lory Stephen. Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell. 2003 Feb;4(2):253–263. doi: 10.1016/s1534-5807(03)00019-4. [DOI] [PubMed] [Google Scholar]
- de Torres Marta, Sanchez Pedro, Fernandez-Delmond Isabelle, Grant Murray. Expression profiling of the host response to bacterial infection: the transition from basal to induced defence responses in RPM1-mediated resistance. Plant J. 2003 Feb;33(4):665–676. doi: 10.1046/j.1365-313x.2003.01653.x. [DOI] [PubMed] [Google Scholar]
- ffrench-Constant Richard, Waterfield Nicholas, Daborn Phillip, Joyce Susan, Bennett Helen, Au Candy, Dowling Andrea, Boundy Sam, Reynolds Stuart, Clarke David. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev. 2003 Jan;26(5):433–456. doi: 10.1111/j.1574-6976.2003.tb00625.x. [DOI] [PubMed] [Google Scholar]
- van Loon L. C., Bakker P. A., Pieterse C. M. Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol. 1998;36:453–483. doi: 10.1146/annurev.phyto.36.1.453. [DOI] [PubMed] [Google Scholar]
- van Wees S. C., Luijendijk M., Smoorenburg I., van Loon L. C., Pieterse C. M. Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol Biol. 1999 Nov;41(4):537–549. doi: 10.1023/a:1006319216982. [DOI] [PubMed] [Google Scholar]