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To be or not to be: howPseudomonas solanacearum decides whether or not to express virulence genes

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Abstract

Pseudomonas solanacearum is a soil-borne phytopathogen that causes a lethal wilting disease of many plants, due in part to production of the unusual exopolysaccharide EPS I and numerous extracellular proteins (EXPs). Levels of EPS I and many EXPs are differentially controlled by a complex sensory array whose size, organization, and other properties set it apart from others found in prokaryotes. This network not only controls reversible switching between two morphotypes, each probably specialized for survival in different ecological niches (plant vs. soil), but also fine tunes transcription of virulence genes in response to multiple environmental signals. The interacting and cascading nature of the network is reminiscent of a primitive neural network, apparently designed to guide virulence gene expression during the dynamic interaction of the pathogen with its environment. This minireview focuses on the unique aspects of the network and its regulated targets.

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Abbreviations

AHSL:

acyl homoserine lactone

EPS:

extracellular polysaccharide

EXP:

extracellular protein

HR:

hypersensitive response

PAME:

palmitic acid methyl ester

References

  • Alex LA and Simon MI (1994) Protein histidine kinases and signal-transduction in prokaryotes and eukaryotes. Trends Genet 10: 133–139

    PubMed  Google Scholar 

  • Allen CA, Huang Y and Sequeira L (1991) Cloning of genes affecting polygalacturonase production inP. solanacearum. Mol Plant-Microbe Interact 4: 147–154

    Google Scholar 

  • Allen CA and Gay J (1995) Structure of a polygalacturonase regulatory operon inPseudomonas solanacearum. Phytopathol 85: 1159 (abstract)

    Google Scholar 

  • Arlat M, van Gijsegem F, Huet JC, Pernollet J and Boucher CA (1994) PopA 1, a protein which induces a hypersensitivity-like response in specific Petunia genotypes is secreted via the Hrp pathway ofPseudomonas solanacearum. EMBO J 13: 543–553

    PubMed  Google Scholar 

  • Boucher CA, Gough C and Arlat MF (1992) Molecular genetics of pathogenicity determinants ofPseudomonas solanacearum with special emphasis onhrp genes. Annu Rev Phytopathol 30: 443–461

    Google Scholar 

  • Bugert P and Geider K (1995) Molecular analysis of theams operon required for exopolysaccharide synthesis ofErwinia amylovora. Mol Micro 15: 917–933

    Google Scholar 

  • Brumbley SM, Carney BF and Denny TP (1993) Phenotype conversion inPseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional activator. J Bacteriol 175: 5477–5487

    PubMed  Google Scholar 

  • Brumbley SM and Denny TP (1990) Cloning ofphcA from wild-typePseudomonas solanacearum, a gene that when mutated alters expression of multiple traits that contribute to virulence. J Bacteriol 172: 5677–5685

    PubMed  Google Scholar 

  • Buddenhagen I and Kelman A (1964) Biological and physiological aspects of bacterial wilt caused byPseudomonas solanacearum. Annu Rev Phytopathol 2: 203–230

    Google Scholar 

  • Clough SJ, Schell MA and Denny TP (1994) Evidence for involvement of a volatile extracellular factor inPseudomonas solanacearum virulence gene expression. Mol Plant-Microbe Interact 7: 621–630

    Google Scholar 

  • Clough SJ, Schell MA and Denny TP (1995) Involvement of a two-component system and 3-hydroxypalmitic acid methyl ester in the regulation of virulence inPseudomonas solanacearum. Phytopathol 85: 1159 (abstract)

    Google Scholar 

  • Cook DE, Barlow E and Sequeira L (1989) Genetic diversity ofPseudomonas solanacearum: detection of restriction length polymorphisms with DNA probes that specify virulence and hypersensitive response. Mol Plant-Microbe Interact 2: 113–121

    Google Scholar 

  • Cook DE and Sequeira L (1994) Strain differentiation ofPseudomonas solanacearum by molecular genetic methods. In: Hayward AC and Hartman GL (eds) Bacterial Wilt: The Disease and Its Causative AgentPseudomonas solanacearum (pp. 77–93) CAB International Oxon, UK

    Google Scholar 

  • Cui Y, Chatterjee A, Liu Y, Dumenyo CK and Chatterjee AK (1995) Identification of a global repressor genersmA ofErwinia carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in softrottingErwinia. J Bacteriol 177: 5108–5115

    PubMed  Google Scholar 

  • Denny TP and Baek SR (1991) Genetic evidence that extracellular polysaccharide is a virulence factor ofPseudomonas solanacearum. Mol Plant-Microbe Interact 4: 198–206

    Google Scholar 

  • Denny TP, Carney BF and and Schell MA (1990) Inactivation of multiple virulence genes reduces the ability ofPseudomonas solanacearum to cause wilt symptoms. Mol Plant-Microbe Interact 3: 293–300

    Google Scholar 

  • Denny TP (1995) Involvement of bacterial polysaccharides in plant pathogenesis. Annu Rev Plant Pathol 33: 173–197

    Google Scholar 

  • Denny TP, Ganova-Raeva L, Huang J and Schell MA (1996) Characterization oftek, the gene encoding the major extracellular protein ofPseudomonas solanacearum. Mol Plant Microbe Interact: In press

  • Downard J and Toal D (1995) Branched-chain fatty acids: the case for a novel form of cell-cell signalling duringMyxococcus xanthus development. Mol Micro 16: 171–175

    Google Scholar 

  • Flavier A and Denny TP (1994) Purification and characterization of a volatile endogenousfactor that restores expression of virulence-associated genes inPseudomonas solanacearum. Phytopathlogy 84: 1134 (abstract)

    Google Scholar 

  • Frosch M, Muller D, Bousset K and Muller A (1992) Conserved outer membrane protein ofNeisseria meningitidis involved in capsule expression. Infect Immun 60: 798–803

    PubMed  Google Scholar 

  • Fuqua WC, Winans SC and Greenberg EP (1995) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269–275

    Google Scholar 

  • Gaffney TD, Lam ST, Ligon J, Gates K, Frazelle A, Dimaio J, Hill S, Torkewicz N, et al. (1994) Global regulation of expression of antifungal factors by aPseudomonas fluorescens biologicalcontrol strain. Mol Plant-Microbe Interact 7: 455–463

    PubMed  Google Scholar 

  • Genin S, Gough CL, Zischek C and Boucher CA (1992) Evidence that thehrpB gene encodes a positive regulator of pathogenicity genes fromPseudomonas solanacearum. Mol Micro 6: 3065–3076

    Google Scholar 

  • Gillis M, Van TV, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T and Fernandez MP (1995) Polyphasic taxonomy in the genusBurkholderia leading to an emended description of the genus and proposition ofBurkholderia vietnamiensis sp. nov. for N2-fixing isolates from rice in Vietnam. Int J Sys Bacteriol 45: 274–289

    Google Scholar 

  • Glucksmann MA, Reuber TL and Walker GC (1993) Genes needed for the modification, polymerization, export, and processing of succinoglycan byRhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175: 7045–7055

    PubMed  Google Scholar 

  • Hayward AC (1991) Biology and epidemiology of bacterial wilt caused byPseudomonas solanacearum. Annu Rev Phytopathol 29: 65–87

    Google Scholar 

  • Hayward AC (1994) Hosts ofPseudomonas solanacearum. In: Hayward AC and Hartman GL (eds) Bacterial Wilt: The Disease and Its Causative AgentPseudomonas solanacearum (pp. 9–24) CAB International Oxon, UK

    Google Scholar 

  • Hellingwerf K, Postma PW, Tommassen J and Westerhoff HV (1995) Signal transduction in bacteria: phospho-neural network(s) inEscherichia coli? FEMS Micro Rev 16: 309–321

    Google Scholar 

  • Hoch JA and Silhavy TJ (eds) (1995) Two-Component Signal Transduction. ASM Press, Herndon, VA

    Google Scholar 

  • Huang H and Sequeira L (1990) Identification of a locus that regulates multiple functions inPseudomonas solanacearum. J Bacteriol 172: 4728–4731

    PubMed  Google Scholar 

  • Huang J, Denny TP and Schell MA (1993) VsrB, a regulator of virulence genes inPseudomonas solanacearum, is homologous to sensors of the two-component regulatory family J Bacteriol 175: 6169–6178

    PubMed  Google Scholar 

  • Huang J, Carney BF, Denny TP, Weissinger AK and Schell MA (1995) A complex network regulateseps and other virulence genes ofPseudomonas solanacearum. J Bacteriol 177: 1259–1267

    PubMed  Google Scholar 

  • Huang J and Schell MA (1995) Characterization of theeps gene cluster ofPseudomonas solanacearum and its transcriptional regulation via a single promoter. Mol Microbiol 16: 977–989

    PubMed  Google Scholar 

  • Ishige K, Nagasawa S, Tokishita S and Mizuno T (1994) A novel device of bacterial signal transducers. EMBO J 13: 5195–5202

    PubMed  Google Scholar 

  • Kang Y, Huang J, Mao G, He L-Y and Schell MA (1994) Dramatically reduced virulence of mutants ofPseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol Plant-Microbe Interact 7: 370–377

    Google Scholar 

  • Kao CC, Barlow, E and Sequeira L (1992) Extracellular polysaccharide is required for wild-type virulence ofPseudomonas solanacearum. J Bacteriol 174: 1068–1071

    PubMed  Google Scholar 

  • Kao CC, Gosti F, Huang Y and Sequeira L (1994) Characterization of a negative regulator of exopolysaccharide production by the plant pathogenic bacteriumPseudomonas solanacearum. Mol Plant-Microbe Interact 7: 121–130

    PubMed  Google Scholar 

  • Kelman A and Sequeira L (1965) Root-to-root spread ofPseudomonas solanacearum. Phytopathology 55: 304–309

    Google Scholar 

  • Leigh J and Coplin D (1992) Exopolysaccharides in plant-bacterial interactions. Annu Rev Micro 46: 307–346

    Google Scholar 

  • Li X, Dorsch M, Deloit T, Sly L, Stackebrandt E and Hayward AC (1994) Phylogenetic studies of the rRNA group II pseudomonads based on 16s rRNA gene sequences. J Appl Bact 74: 324–329

    Google Scholar 

  • McWilliams R, Chapman M, Kowlaczuk M, Hershberger D, Sun J-H and Kao CC (1995) Complementation analyses ofPseudomonas solanacearum extracellular polysaccharide mutants and identification of genes responsive to EpsR. Mol Plant-Microbe Interact 8: 837–844

    PubMed  Google Scholar 

  • Orgambide G, Montrozier H, Servin P, Roussel J, Trigalet-Demery D and Trigalet A (1991) High heterogeneity of the exopolysaccharides ofPseudomonas solanacearum strain GMI1000 and the complete structure of the major polysaccharide. J Biol Chem 266: 8312–8321

    PubMed  Google Scholar 

  • Parkinson JS and Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26: 71–112

    PubMed  Google Scholar 

  • Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG and Ausubel FM (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899–1902

    PubMed  Google Scholar 

  • Rich JJ, Kinscherf TG, Kitten T and Willis DK (1994) Genetic evidence thatgacA encodes the cognate response regulator for thelemA sensor inPseudomonas syringae. J Bacteriol 176: 7468–7475

    PubMed  Google Scholar 

  • Schell MA (1987) Purification and characterization of an excreted endoglucanase fromPseudomonas solanacearum. Appl Environ Microbiol 53: 2237–2241

    Google Scholar 

  • Schell MA, Roberts DP, and Denny TP (1988) Analysis of thePseudomonas solanacearum polygalacturonase encoded bypglA and it involvement in phytopathogenicity. J Bacteriol 170: 4501–4508

    PubMed  Google Scholar 

  • Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47: 597–626

    PubMed  Google Scholar 

  • Schell MA, Denny TP, Clough SJ and Huang J (1993a) Further characterization of genes encoding extracellular polysaccharide ofPseudomonas solanacearum and their regulation. In: Nester EW and Verma DPS (eds) Advances in Molecular Genetics of Plant-Microbe Interactions (pp. 231–239) Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Schell MA, Denny TP and Huang J (1993b) VsrA, a second two-component system regulating virulence genes ofPseudomonas solanacearum. Mol Microbiol 11: 489–500

    Google Scholar 

  • Schell MA, Denny TP and Huang J (1994) Extracellular virulence factors ofPseudomonas solanacearum: Role in disease and regulation of expression. In: Kado CI and Crosa JH (eds) Molecular Mechanisms of Bacterial Virulence (pp. 311–324) Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Schmit J (1978) Microscopic study of early stages of infection byPseudomonas solanacearum EFS on “in vitro” grown tomato seedlings. In: Anonymous (ed) Proceedings of the Fourth International Conference on Plant Pathogenic Bacteria (pp. 841–857) Anger, France

  • Seal SE, Jackson LA, Young JPW and Daniels MJ (1993) Differentiation ofPseudomonas solanacearum, Pseudomonas syzygii, Pseudomonas pickettii and the blood disease bacterium by partial 16s rRNA sequencing: construction of oligonucleotide primers for sensitive detection by polymerase chain reaction. J Gen Micro 139: 1587–1584

    Google Scholar 

  • Van Gijsegem F, Gough C, Zischek C, Niqueux E, Arlat M, Genin S, Barberis P, Castello P and Boucher C (1995) Thehrp locus ofPseudomonas solanacearum which controls the production of a type III secretion system encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol Micro 15: 1095–1114

    Google Scholar 

  • Vasse J, Pascal F and Trigalet A (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots byPseudomonas solanacearum. Mol Plant-Microbe Interact 8: 241–251

    Google Scholar 

  • Von Bodman SB and Farrand S (1995) Capsular polysaccharide biosynthesis and pathogenicity inErwinia stewartii require induction by an N-acyl homoserine lactone autoinducer. J Bacteriol 1177: 5000–5008

    Google Scholar 

  • Wallis FM and Truter SJ (1978) Histopathology of tomato plants infected withPseudomonas solanacearum, with emphasis on ultrastructure. Physiol Pl Path 13: 307–317

    Google Scholar 

  • Willis DK, Rich JJ, Kinscherf TG and Kitten T (1994) Genetic regulation in plant pathogenic pseudomonads. In: Setlow JK (ed) Genetic Engineering, vol 16 (pp. 167–193) Plenum Press, NY

    Google Scholar 

  • Xiao Y, Heu S, Yi J, Lu Y and Hutcheson SW (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression ofPseudomonas syringae pvsyringae Pss61hrp andhrmA genes. J Bacteriol 176: 1025–1036

    PubMed  Google Scholar 

  • Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hahimoto Y, Ezaki T and Arakawa T (1992) Proposal ofBurkholderia gen. nov. and transfer of seven species of the genusPseudomonas group II to the new genus with the type speciesBurkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol 36: 1251–1275

    PubMed  Google Scholar 

  • Yabuuchi E, Kosako Y, Yano I, Hotta H and Nishiuchi Y (1995) Transfer of twoBurkholderia and anAlcaligenes species toRalstonia gen. nov.: proposal ofRalstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb, nov.,Ralstonia solanacearum (Smith 1896) comb. nov. andRalstonia eutropha (Davis 1969) comb. nov. Microbiol Immunol 39: 897–904

    PubMed  Google Scholar 

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  1. Departments of Microbiology and Plant Pathology, University of Georgia, Biological Sciences Bldg., 30602, Athens, GA, USA

    Mark A. Schell

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Schell, M.A. To be or not to be: howPseudomonas solanacearum decides whether or not to express virulence genes. Eur J Plant Pathol 102, 459–469 (1996). https://doi.org/10.1007/BF01877140

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