1932

Abstract

This article recounts the experiences that shaped my career as a molecular plant pathologist. It focuses primarily on technical and conceptual developments in molecular phytobacteriology, shares some personal highlights and untold stories that impacted my professional development, and describes the early years of agricultural biotechnology. Writing this article required reflection on events occurring over several decades that were punctuated by a mid-career relocation across the Atlantic. I hope it will still be useful, informative, and enjoyable to read. An extended version of the abstract is provided in the , available online.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080516-035506
2017-08-04
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/phyto/55/1/annurev-phyto-080516-035506.html?itemId=/content/journals/10.1146/annurev-phyto-080516-035506&mimeType=html&fmt=ahah

Literature Cited

  1. Agrios GN. 1.  2005. Plant Pathology Amsterdam: Elsevier Acad. Press922, 5th ed..
  2. Bagdasarian M, Lurz R, Rukert B, Franklin FCH, Bagdasarian MM. 2.  et al. 1981. Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number RSFI010-derived vectors and a host-vector system for gene cloning in Pseudomonas. . Gene 16:237–47 [Google Scholar]
  3. Bagdasarian MM, Timmis KN. 3.  1982. Host-vector systems for gene cloning in Pseudomonas. . Curr. Top. Microbiol. Immunol. 96:47–67 [Google Scholar]
  4. Boch J, Bonas U, Lahaye T. 4.  2014. TAL effectors: pathogen strategies and plant resistance engineering. New Phytol 204:823–32 [Google Scholar]
  5. Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A. 5.  et al. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:681–83 [Google Scholar]
  6. Boller T, Felix G. 6.  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 [Google Scholar]
  7. Bonas U. 7.  1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79–98 [Google Scholar]
  8. Boucher CA, Gough CL, Arlat M. 8.  1992. Molecular genetics of pathogenicity determinants of Pseudomonas solanacearum with special emphasis on hrp genes. Annu. Rev. Phytopathol. 30:443–61 [Google Scholar]
  9. Brown IR, Mansfield JW, Taira S, Roine E, Romantschuk M. 9.  2001. Immunocytochemical localization of HrpA and HrpZ supports a role for a transfer of effector proteins from Pseudomonas syringae pv. tomato across the plant cell wall. Mol. Plant-Microbe Interact. 14:394–404 [Google Scholar]
  10. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML. 10.  et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. PNAS 100:10181–86 [Google Scholar]
  11. Büttner D. 11.  2012. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol. Mol. Biol. Rev. 76:262–310 [Google Scholar]
  12. Büttner D, Bonas U. 12.  2002. Getting across: bacterial type III effector proteins on their way to the plant cell. EMBO J 21:5313–22 [Google Scholar]
  13. Büttner D, Bonas U. 13.  2006. Who comes first? How plant pathogenic bacteria orchestrate type III secretion. Curr. Opin. Microbiol. 9:193–200 [Google Scholar]
  14. Chatterjee AK, Starr MP. 14.  1980. Genetics of Erwinia species. Annu. Rev. Microbiol. 34:645–76 [Google Scholar]
  15. Chilton MD. 15.  2001. Agrobacterium. A Memoir. Plant Physiol 125:9–14 [Google Scholar]
  16. Cho JJ, Panopoulos NJ, Schroth MN. 16.  1975. Genetic transfer of Pseudomonas aeruginosa R factors to plant pathogenic Erwinia species. J. Bacteriol. 122:192–98 [Google Scholar]
  17. Cook DE, Mesarich CH, Thomma BPHJ. 17.  2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 53:541–63 [Google Scholar]
  18. Cornelis GR. 18.  2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811–25 [Google Scholar]
  19. Cornelis GR, Van Gijsegem F. 19.  2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735–74 [Google Scholar]
  20. Crabill E, Karpisek A, Alfano JR. 20.  2012. The Pseudomonas syringae HrpJ protein controls the secretion of type III translocator proteins and has a virulence role inside plant cells. Mol. Microbiol. 85:225–38 [Google Scholar]
  21. Daniels MJ, Dow JM, Osburn AE. 21.  1988. Molecular genetics of pathogenicity in phytopathogenic bacteria. Annu. Rev. Phytopathol. 26:285–312 [Google Scholar]
  22. Davison J. 22.  2002. Genetic tools for pseudomonads, rhizobia, and other gram-negative bacteria. BioTechniques 32:386–401 [Google Scholar]
  23. Day PR. 23.  1974. Genetics of Host-Parasite Interaction San Francisco: W.H. Freeman
  24. Deng X, Liang H, Chen K, He C, Lan L, Tang X. 24.  2014. Molecular mechanisms of two-component system RhpRS regulating type III secretion system in Pseudomonas syringae. . Nucleic Acids Res. 42:11472–86 [Google Scholar]
  25. de Wit PJGM. 25.  2016. Cladosporium fulvum effectors: weapons in the arms race with tomato. Annu. Rev. Phytopathol. 54:1–23 [Google Scholar]
  26. Durbin R ed. 26.  1981. Toxins in Plant Disease New York: Academic
  27. Ellingboe AH. 27.  1976. Genetics of host-parasite interactions. Encyclopedia of Plant Physiology 4 Physiological Plant Pathology R Heitefuss, PH Williams 761–78 New York: Springer [Google Scholar]
  28. Erhardt M, Namba K, Hughes KT. 28.  2010. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb. Perspect. Biol. 2:a000299 [Google Scholar]
  29. Fadouloglou VE, Bastaki MN, Ashcroft AE, Phillips SEV, Panopoulos NJ. 29.  et al. 2009. On the quaternary association of the type III secretion system HrcQB-C protein: experimental evidence differentiates among the various oligomerization models. J. Struct. Biol. 166:214–25 [Google Scholar]
  30. Fadouloglou VE, Tampakaki AP, Glykos NM, Bastaki MN, Hadden JM. 30.  et al. 2004. Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems. PNAS 101:70–75 [Google Scholar]
  31. Fulbright DW, Leary JV. 31.  1978. Linkage analysis of Pseudomonas glycinea. J. Bacteriol. 136:497–500 [Google Scholar]
  32. Galan JE, Wolf-Watz H. 32.  2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567–73 [Google Scholar]
  33. Gazi AD, Bastaki M, Charova SN, Gkougkoulia EA, Kapellios EA. 33.  et al. 2008. Evidence for a coiled-coil interaction mode of disordered proteins from bacterial type III secretion systems. J. Biol. Chem. 283:34062–68 [Google Scholar]
  34. Gazi AD, Charova S, Aivaliotis M, Panopoulos NJ, Kokkinidis M. 34.  2015. HrpG and HrpV proteins from the Type III secretion system of Erwinia amylovora form a stable heterodimer. FEMS Microbiol. Lett. 362:1–8 [Google Scholar]
  35. Gazi AD, Charova SN, Panopoulos NJ, Kokkinidis M. 35.  2009. Coiled-coils in type III secretion systems: structural flexibility, disorder and biological implications. Cell. Microbiol. 11:719–29 [Google Scholar]
  36. Georgopoulos SG, Panopoulos NJ. 36.  1966. The relative mutability of the cnb loci in Hypomyces. . Can. J. Genet. Cytol. 8:347–49 [Google Scholar]
  37. Gianinazzi SC, Martin C, Vallée JC. 37.  1970. Hypersensibilité aux virus, temperature et protéines solubles chez le Nicotiana Xanthi n.c. Apparition de nouvelles macromolécules lors de la répression de la synthèse virale. C. R. Acad. Sci. 270D:2383–86 [Google Scholar]
  38. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B. 38.  et al. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–28 [Google Scholar]
  39. Gough CL, Genin S, Zischek C, Boucher CA. 39.  1992. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant-Microbe Interact. 5:384–89 [Google Scholar]
  40. Grimm C, Aufsatz W, Panopoulos NJ. 40.  1995. The hrpRS locus of Pseudomonas syringae pv. phaseolicola constitutes a complex regulatory unit. Mol. Microbiol. 15:155–65 [Google Scholar]
  41. Grimm CG, Panopoulos NJ. 41.  1989. The predicted protein product of a pathogenicity locus from Pseudomonas syringae pv. phaseolicola is homologous to a highly conserved domain of several prokaryotic regulatory proteins. J. Bacteriol. 171:5031–38 [Google Scholar]
  42. Gross DC, Lichens-Park A, Kole CH. 42.  2014. Genomics of Plant-Associated Bacteria. Berlin/Heidelberg: Springer-Verlag [Google Scholar]
  43. Haapalainen M, van Gestel K, Pirhonen M, Taira S. 43.  2009. Soluble plant cell signals induce the expression of the type III secretion system of Pseudomonas syringae and upregulate the production of pilus protein HrpA. Mol. Plant-Microbe Interact. 22:282–90 [Google Scholar]
  44. Hammond-Kosack KE, Jones JDG. 44.  1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:575–607 [Google Scholar]
  45. He SY. 45.  1998. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36:363–92 [Google Scholar]
  46. Holloway BW. 46.  1979. Plasmids that mobilize bacterial chromosome. Plasmid 2:1–19 [Google Scholar]
  47. Hu W, Yuan J, Jin Q-L, Hart P, He SY. 47.  2001. Immunogold labeling of Hrp pili of Pseudomonas syringae pv. tomato assembled in minimal medium and in planta. Mol. Plant-Microbe Interact. 14:234–41 [Google Scholar]
  48. Huang HC, Schuurink R, Denny TP, Atkinson MM, Baker CJ. 48.  et al. 1988. Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J. Bacteriol. 170:4748–56 [Google Scholar]
  49. Hueck CJ. 49.  1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379–433 [Google Scholar]
  50. Hutcheson SW, Bretz J, Sussan T, Jin S, Pak K. 50.  2001. Enhancer-binding proteins HrpR and HrpS interact to regulate hrp-encoded type III protein secretion in Pseudomonas syringae strains. J. Bacteriol 183:5589–98 [Google Scholar]
  51. Huynh T, Dahlbeck D, Staskawicz BJ. 51.  1989. Bacterial blight of soybeans: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374–77 [Google Scholar]
  52. Jackson RW. 52.  2009. Plant Pathogenic Bacteria: Genomics and Molecular Biology Haverhill, UK: Caister Acad.
  53. Johal GS, Briggs SP. 53.  1992. Reductase activity encoded by the HM7 disease resistance gene in maize. Science 258:985–87 [Google Scholar]
  54. Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ. 54.  1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175:4859–69 [Google Scholar]
  55. Jin Q, Hu W, Brown I, McGhee G, Hart P. 55.  et al. 2001. Visualization of secreted Hrp and Avr proteins along the Hrp pilus during type III secretion in Erwiniaamylovora and Pseudomonas syringae. . Mol. Microbiol. 40:1129–39 [Google Scholar]
  56. Jones JDG, Dangl JL. 56.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  57. Jovanovic M, Lawton E, Schumacher J, Buck M. 57.  2014. Interplay among Pseudomonas syringae HrpR, HrpS and HrpV proteins for regulation of the type III secretion system. FEMS Microbiol. Lett. 356:201–11 [Google Scholar]
  58. Kado CI. 58.  2014. Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens. Front. Microbiol. 5:340 [Google Scholar]
  59. Kado CI, Knight CA. 59.  1966. Location of a local lesion gene in tobacco mosaic virus RNA. PNAS 55:1276–83 [Google Scholar]
  60. Kado CI, Knight CA. 60.  1968. The coat protein gene of tobacco mosaic virus. Location of the gene by mixed infection. J. Mol. Biol. 36:15–23 [Google Scholar]
  61. Klement Z, Farkas GL, Lovrekovich L. 61.  1964. Hypersensitive reaction induced by phytopathogenic bacteria in the tobacco leaf. Phytopathology 54:474–77 [Google Scholar]
  62. Khokhani D, Zhang C, Li Y, Wang Q, Zeng Q. 62.  et al. 2013. Discovery of plant phenolic compounds that act as type III secretion system inhibitors or inducers of the fire blight pathogen. Erwinia amylovora. Appl. Environ. Microbiol. 79:5424–36 [Google Scholar]
  63. Lacy GH, Leary JV. 63.  1979. Genetic systems in phytopathogenic bacteria. Annu. Rev. Phytopathol. 17:181–202 [Google Scholar]
  64. Lee J, Klüsener B, Tsiamis G, Stevens C, Neyt C. 64.  et al. 2001. HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion‐conducting pore in vitro. PNAS 98:289–94 [Google Scholar]
  65. Leong SA, Holden DW. 65.  1989. Molecular genetic approaches to the study of fungal pathogenesis. Annu. Rev. Phytopathol. 27:463–81 [Google Scholar]
  66. Li C-M, Brown I, Mansfield J, Stevens C, Boureau T. 66.  et al. 2002. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J 21:1909–15 [Google Scholar]
  67. Lindgren PB. 67.  1997. The role of hrp genes during plant-bacterial interactions. Annu. Rev. Phytopathol. 35:129–52 [Google Scholar]
  68. Lindgren PB, Frederick R, Govindarajan AG, Panopoulos NJ, Staskawicz BJ, Lindow SE. 68.  1989. An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syringae pv. phaseolicola. EMBO J. 8:1291–301 [Google Scholar]
  69. Lindgren PB, Panopoulos NJ, Staskawicz BJ, Dahlbeck D. 69.  1988. Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae. . Mol. Gen. Genet. 211:499–506 [Google Scholar]
  70. Lindgren PB, Peet RC, Panopoulos NJ. 70.  1986. Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogencity on bean and hypersensitivity on non-host plants. J. Bacteriol. 168:512–22 [Google Scholar]
  71. Lohou D, Lonjon F, Genin S, Vailleau F. 71.  2013. Type III chaperones & Co in bacterial plant pathogens: a set of specialized bodyguards mediating effector delivery. Front. Plant Sci. 4:435 [Google Scholar]
  72. Loper JE, Orser CS, Panopoulos NJ, Schroth MN. 72.  1984. Genetic analysis of fluorescent pigment production in Pseudomonas syringae pv. syringae. J. Gen. Microbiol. 130:1507–15 [Google Scholar]
  73. Losada L, Sussan T, Pak K, Zeyad S, Rozenbaum I, Hutcheson SW. 73.  2004. Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulence functions by a HrpL-dependent promoter-trap assay. Mol. Plant-Microbe Interact. 17:254–62 [Google Scholar]
  74. Mansfield JW. 74.  2009. From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Mol. Plant Pathol. 10:721–34 [Google Scholar]
  75. Mills D. 75.  1985. Transposon mutagenesis and its potential for studying virulence genes in plant pathogens. Annu. Rev. Phytopathol. 23:297–320 [Google Scholar]
  76. Mucyn TS, Yourstone S, Lind AL, Biswas S, Nishimura MT. 76.  et al. 2014. Variable suites of non-effector genes are co-regulated in the type III secretion virulence regulon across the Pseudomonas syringae phylogeny. PLOS Pathog 10:e1003807 [Google Scholar]
  77. Nester E. 77.  2008. Agrobacterium: the natural genetic engineer 100 years later. APSnet Features https://doi.org/10.1094/APSnetFeatures-2008-0608 [Crossref]
  78. Oliver R, Osbourn AE. 78.  1995. Molecular dissection of fungal phytopathogenicity. Microbiology 141:1–9 [Google Scholar]
  79. Orser CS, Staskawicz BJ, Panopoulos NJ, Dahlbeck D, Lindow SE. 79.  1985. Cloning and expression of bacterial ice nucleation genes in Escherichia coli. . J. Bacteriol. 164:359–66 [Google Scholar]
  80. Ortiz-Martín I, Macho AP, Lambersten L, Ramos C, Beuzón CR. 80.  2006. Suicide vectors for antibiotic marker exchange and rapid generation of multiple knockout mutants by allelic exchange in Gram-negative bacteria. J. Microbiol. Methods 67:395–407 [Google Scholar]
  81. Ortiz-Martín I, Thwaites R, Macho AP, Mansfield JW, Beuzón CR. 81.  2010. Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. . Mol. Plant-Microbe Interact. 23:665–81 [Google Scholar]
  82. Ortiz-Martín I, Thwaites R, Mansfield JW, Beuzón CR. 82.  2010. Negative regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact. 23:682–701 [Google Scholar]
  83. Panopoulos NJ, Guimaraes WV, Schroth MN. 83.  1975. Conjugative transfer of R factors from Pseudomonas aeruginosa to plant pathogenic Pseudomonas spp.. Phytopathology 65:380–88 [Google Scholar]
  84. Panopoulos NJ, Peet RC. 84.  1985. The molecular genetics of plant pathogenic bacteria and their plasmids. Annu. Rev. Phytopathol. 23:381–419 [Google Scholar]
  85. Panopoulos NJ, Schroth MN. 85.  1974. Role of flagellar motility in the invasion of bean leaves by Pseudomonas phaseolicola. . Phytopathology 64:1389–97 [Google Scholar]
  86. Panopoulos NJ, Walton JD, Willis DK. 86.  1984. Genetic and biochemical basis of virulence in plant pathogens. Plant Gene Research 1 Plant Pathogens and Defense Mechanisms TH Hohn, DPS Verma 339–74 Berlin/Heidelberg/New York: Springer-Verlag [Google Scholar]
  87. Peet RC, Lindgren PB, Willis DK, Panopoulos NJ. 87.  1986. Identification and cloning of genes involved in phaseolotoxin production by Pseudomonas syringae pv. phaseolicola. J. Bacteriol. 166:1096–105 [Google Scholar]
  88. Portaliou AG, Tsolis KC, Loos MS, Zorzini V, Economou A. 88.  2016. Type III secretion: building and operating a remarkable nanomachine. Trends Biochem. Sci. 41:175–89 [Google Scholar]
  89. Pozidis C, Chalkiadaki A, Gomez-Serrano A, Stahlberg H, Brown I. 89.  et al. 2003. Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. J. Biol. Chem. 278:25816–24 [Google Scholar]
  90. Pring DR, Levings CS. 90.  1978. Heterogeneity of maize cytoplasmic genomes among male-sterile cytoplasms. Genetics 89:121–36 [Google Scholar]
  91. Rahme LG, Mindrinos MN, Panopoulos NJ. 91.  1991. Genetic and transcriptional organization of the hrp cluster of Pseudomonas syringae pv. phaseolicola. . J. Bacteriol 173:575–86 [Google Scholar]
  92. Rahme LG, Mindrinos MN, Panopoulos NJ. 92.  1992. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J. Bacteriol. 174:3499–507 [Google Scholar]
  93. Roine E, Saarinen J, Kalkkinen N, Romantschuk M. 93.  1997. Purified HrpA of Pseudomonas syringae pv. tomato DC3000 reassembles into pili. FEBS Lett. 417:168–72 [Google Scholar]
  94. Roine E, Wei W, Yuan J, Nurmiaho-Lassila E-L, Kalkkinen N. 94.  et al. 1997. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomatoDC3000. PNAS 94:3459–64 [Google Scholar]
  95. Rufian JS, Sanchez-Romero M-A, Lopez-Marquez D, Macho AP, Mansfield JW. 95.  et al. 2016. Pseudomonas syringae differentiates into phenotypically distinct subpopulations during colonization of a plant host. Environ. Microbiol. 18:3593–605 [Google Scholar]
  96. Salmeron JM, Staskawicz BJ. 96.  1993. Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonassyringae pv. tomato. . Mol. Gen. Genet. 239:6–10 [Google Scholar]
  97. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S. 97.  et al. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. . Nature 415:497–502 [Google Scholar]
  98. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A. 98.  2004. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. Mol. Plant-Microbe Interact. 17:254–62 [Google Scholar]
  99. Schreiber KJ, Baudin M, Hassan JA, Lewis JD. 99.  2016. Die another day: molecular mechanisms of effector-triggered immunity elicited by type III secreted effector proteins. Semin. Cell Dev. Biol. 56:124–33 [Google Scholar]
  100. Schuster M, Grimm C. 100.  2000. Molecular domain switching between hrpR and hrpS affects the regulatory function of the hybrid genes in Pseudomonas syringae pv. phaseolicola. Plant Pathol. 4:233–41 [Google Scholar]
  101. Shaefer W. 101.  1994. Molecular mechanisms of fungal pathogenicity on plants. Annu. Rev. Phytopathol. 32:461–77 [Google Scholar]
  102. Simpson AJG, Reinach FC, Arruda P, Abreu FA, Acencio M. 102.  et al. 2000. The genome sequence of plant pathogen Xylella fastidiosa. . Nature 406:151–59 [Google Scholar]
  103. Staskawicz BJ, Dahlbeck D, Keen NT. 103.  1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. PNAS 81:6024–28 [Google Scholar]
  104. Stent GS. 104.  1968. That was the molecular biology that was. Science 160:390–95 [Google Scholar]
  105. Sundin GW, Wang N, Charkowski AO, Castiblanco LF, Jia H, Zhao Y. 105.  2016. Perspectives on the transition from bacterial phytopathogen genomics studies to applications enhancing disease management: from promise to practice. Phytopathology 106:1071–82 [Google Scholar]
  106. Tampakaki A, Fadouloglou V, Gazi A, Panopoulos N, Kokkinidis M. 106.  2004. Conserved features of type III secretion. Cell. Microbiol. 6:805–16 [Google Scholar]
  107. Tampakaki AP, Panopoulos NJ. 107.  2000. Elicitation of hypersensitive cell death by extracellularly targeted HrpZPsph produced in planta. Mol. Plant-Microbe Interact. 13:1366–74 [Google Scholar]
  108. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF. 108.  et al. 2010. Playing the “Harp”: evolution of our understanding of hrp/hrc genes. Annu. Rev. Phytopathol. 48:347–70 [Google Scholar]
  109. Thomas CM, Smith CA. 109.  1987. Incompatibility group P plasmids: genetics, evolution and use in genetic manipulation. Annu. Rev. Microbiol. 41:77–101 [Google Scholar]
  110. Thwaites R, Spanu PD, Panopoulos NJ, Stevens C, Mansfield JW. 110.  2004. Transcriptional regulation of components of the type III secretion system and effectors in Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact. 17:1250–58 [Google Scholar]
  111. Troisfontaines P, Cornelis GR. 111.  2005. Type III secretion: more systems than you think. Physiology 20:326–39 [Google Scholar]
  112. Turner J, Novacky A. 112.  1974. The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 64:885–90 [Google Scholar]
  113. Upadhyaya NM, Mago R, Staskawicz BJ, Ayliffe MA, Ellis JG, Dodds PN. 113.  2014. A bacterial type III secretion assay for delivery of fungal effector proteins into wheat. Mol. Plant-Microbe Interact. 27:255–64 [Google Scholar]
  114. Wu D, Ding W, Zhang Y, Liu X, Yang L. 114.  2015. Oleanolic acid induces the type III secretion system of Ralstonia solanacearum. . Front. Microbiol. 6:1466 [Google Scholar]
  115. van der Hoorn RAL, Kamoun S. 115.  2009. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–201 [Google Scholar]
  116. Vanderplank JE.116.  1978. Genetic and Molecular Basis of Plant Pathogenesis Berlin-Heidelberg: Springer-Verlag
  117. Vanderplank JE. 117.  1984. Disease Resistance in Plants Orlando, FL: Academic
  118. Van Kammen A. 118.  1972. Plant viruses with a divided genome. Annu. Rev. Phytopathol. 101:125–50 [Google Scholar]
  119. van Loon LC, Van Kammen A. 119.  1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. ‘Samsun’ and ‘Samsun NN’. II. Changes in protein constitution after infection with TMV. Virology 40:199–201 [Google Scholar]
  120. Vargas P, Farias GA, Nogales J, Prada H, Carvajal V. 120.  et al. 2013. Plant flavonoids target Pseudomonas syringae pv. tomato DC3000 flagella and type III secretion system. Environ. Microbiol. Rep. 5:841–50 [Google Scholar]
  121. Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S. 121.  et al. 2006. Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol. Plant-Microbe Interact. 19:1193–206 [Google Scholar]
  122. Walton JD. 122.  1996. Host-selective toxins: agents of compatibility. Plant Cell 8:1723–33 [Google Scholar]
  123. Wang B, Barahona M, Buck M. 123.  2014. Engineering modular and tunable genetic amplifiers for scaling transcriptional signals in cascaded gene networks. Nucleic Acids Res 42:9484–92 [Google Scholar]
  124. Wei C-F, Deng W-L, Huang H-C. 124.  2005. A chaperone-like HrpG protein acts as a suppressor of HrpV in regulation of the Pseudomonas syringae pv. syringae type III secretion system. Mol. Microbiol. 57:520–36 [Google Scholar]
  125. Willis DK, Rich JJ, Hrabak EM. 125.  1991. hrp genes of phytopathogenic bacteria. Mol. Plant-Microbe Interact. 4:132–38 [Google Scholar]
  126. Win J, Chaperro-Garcia A, Belhaj K, Saunders DGO, Yoshida K. 126.  et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235–47 [Google Scholar]
  127. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP. 127.  et al. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–23 [Google Scholar]
  128. Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW. 128.  1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol. 176:1025–36 [Google Scholar]
  129. Xiao Y, Hutcheson SW. 129.  1994. A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J. Bacteriol. 176:3089–91 [Google Scholar]
  130. Xiao Y, Lu Y, Heu S, Hutcheson SW. 130.  1992. Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J. Bacteriol. 174:1734–41 [Google Scholar]
  131. Yang S, Peng Q, San Francisco M, Wang Y, Zeng Q, Yang C-H. 131.  2008. Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids. PLOS ONE 3:e2973 [Google Scholar]
  132. Yoder OC, Turgeon BG. 132.  1996. Molecular-genetic evaluation of fungal molecules for roles in pathogenesis to plants. J. Genet. 75:425–40 [Google Scholar]
  133. Zaitlin M. 133.  1999. Elucidation of the genome organization of tobacco mosaic virus. Philos. Trans. R. Soc. Lond. B 354:587–91 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080516-035506
Loading

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error