A Career on Both Sides of the Atlantic: Memoirs of a Molecular Plant Pathologist.

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 Supplemental Materials , available online.

[1]  J. Casadesús,et al.  Pseudomonas syringae Differentiates into Phenotypically Distinct Subpopulations During Colonization of a Plant Host. , 2016, Environmental microbiology.

[2]  P. D. Wit Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato , 2016 .

[3]  Maël Baudin,et al.  Die another day: Molecular mechanisms of effector-triggered immunity elicited by type III secreted effector proteins. , 2016, Seminars in cell & developmental biology.

[4]  Youfu Zhao,et al.  Perspectives on the Transition From Bacterial Phytopathogen Genomics Studies to Applications Enhancing Disease Management: From Promise to Practice. , 2016, Phytopathology.

[5]  A. Economou,et al.  Type III Secretion: Building and Operating a Remarkable Nanomachine. , 2016, Trends in biochemical sciences.

[6]  W. Ding,et al.  Oleanolic Acid Induces the Type III Secretion System of Ralstonia solanacearum , 2015, Front. Microbiol..

[7]  B. Thomma,et al.  Understanding plant immunity as a surveillance system to detect invasion. , 2015, Annual review of phytopathology.

[8]  U. Bonas,et al.  TAL effectors--pathogen strategies and plant resistance engineering. , 2014, The New phytologist.

[9]  Chuan He,et al.  Molecular mechanisms of two-component system RhpRS regulating type III secretion system in Pseudomonas syringae , 2014, Nucleic acids research.

[10]  C. Kado Historical account on gaining insights on the mechanism of crown gall tumorigenesis induced by Agrobacterium tumefaciens , 2014, Front. Microbiol..

[11]  Mauricio Barahona,et al.  Engineering modular and tunable genetic amplifiers for scaling transcriptional signals in cascaded gene networks , 2014, Nucleic acids research.

[12]  J. Schumacher,et al.  Interplay among Pseudomonas syringae HrpR, HrpS and HrpV proteins for regulation of the type III secretion system , 2014, FEMS microbiology letters.

[13]  P. Dodds,et al.  A bacterial type III secretion assay for delivery of fungal effector proteins into wheat. , 2014, Molecular plant-microbe interactions : MPMI.

[14]  David A. Baltrus,et al.  Variable Suites of Non-effector Genes Are Co-regulated in the Type III Secretion Virulence Regulon across the Pseudomonas syringae Phylogeny , 2014, PLoS pathogens.

[15]  Marta Martín,et al.  Plant flavonoids target Pseudomonas syringae pv. tomato DC3000 flagella and type III secretion system. , 2013, Environmental microbiology reports.

[16]  S. Genin,et al.  Type III chaperones & Co in bacterial plant pathogens: a set of specialized bodyguards mediating effector delivery , 2013, Front. Plant Sci..

[17]  Ching-Hong Yang,et al.  Discovery of Plant Phenolic Compounds That Act as Type III Secretion System Inhibitors or Inducers of the Fire Blight Pathogen, Erwinia amylovora , 2013, Applied and Environmental Microbiology.

[18]  E. Crabill,et al.  The Pseudomonas syringae HrpJ protein controls the secretion of type III translocator proteins and has a virulence role inside plant cells , 2012, Molecular microbiology.

[19]  D. Büttner Protein Export According to Schedule: Architecture, Assembly, and Regulation of Type III Secretion Systems from Plant- and Animal-Pathogenic Bacteria , 2012, Microbiology and Molecular Reviews.

[20]  Keiichi Namba,et al.  Bacterial nanomachines: the flagellum and type III injectisome. , 2010, Cold Spring Harbor perspectives in biology.

[21]  M. Kokkinidis,et al.  Playing the "Harp": evolution of our understanding of hrp/hrc genes. , 2010, Annual review of phytopathology.

[22]  J. Mansfield,et al.  Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. , 2010, Molecular plant-microbe interactions : MPMI.

[23]  J. Mansfield 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. , 2009, Molecular plant pathology.

[24]  S. Phillips,et al.  On the quaternary association of the type III secretion system HrcQB-C protein: experimental evidence differentiates among the various oligomerization models. , 2009, Journal of structural biology.

[25]  M. Kokkinidis,et al.  Coiled‐coils in type III secretion systems: structural flexibility, disorder and biological implications , 2009, Cellular microbiology.

[26]  T. Boller,et al.  A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. , 2009, Annual review of plant biology.

[27]  M. Pirhonen,et al.  Soluble plant cell signals induce the expression of the type III secretion system of Pseudomonas syringae and upregulate the production of pilus protein HrpA. , 2009, Molecular plant-microbe interactions : MPMI.

[28]  Michael Kokkinidis,et al.  Evidence for a Coiled-coil Interaction Mode of Disordered Proteins from Bacterial Type III Secretion Systems* , 2008, Journal of Biological Chemistry.

[29]  Ching-Hong Yang,et al.  Type III Secretion System Genes of Dickeya dadantii 3937 Are Induced by Plant Phenolic Acids , 2008, PloS one.

[30]  S. Kamoun,et al.  From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors , 2008, The Plant Cell Online.

[31]  Carmen R Beuzón,et al.  Suicide vectors for antibiotic marker exchange and rapid generation of multiple knockout mutants by allelic exchange in Gram-negative bacteria. , 2006, Journal of microbiological methods.

[32]  Jonathan D. G. Jones,et al.  The plant immune system , 2006, Nature.

[33]  Monica Vencato,et al.  Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. , 2006, Molecular plant-microbe interactions : MPMI.

[34]  G. Cornelis,et al.  The type III secretion injectisome , 2006, Nature Reviews Microbiology.

[35]  Hans Wolf-Watz,et al.  Protein delivery into eukaryotic cells by type III secretion machines , 2006, Nature.

[36]  U. Bonas,et al.  Who comes first? How plant pathogenic bacteria orchestrate type III secretion. , 2006, Current opinion in microbiology.

[37]  Paul Troisfontaines,et al.  Type III secretion: more systems than you think. , 2005, Physiology.

[38]  Chia-Fong Wei,et al.  A chaperone‐like HrpG protein acts as a suppressor of HrpV in regulation of the Pseudomonas syringae pv. syringae type III secretion system , 2005, Molecular microbiology.

[39]  C. Stevens,et al.  Transcriptional regulation of components of the type III secretion system and effectors in Pseudomonas syringae pv. phaseolicola. , 2004, Molecular plant-microbe interactions : MPMI.

[40]  M. Kokkinidis,et al.  Conserved features of type III secretion , 2004, Cellular microbiology.

[41]  S. Hutcheson,et al.  Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulence functions by a HrpL-dependent promoter-trap assay. , 2004, Molecular plant-microbe interactions : MPMI.

[42]  Alan Collmer,et al.  Pseudomonas syringae Type III Secretion System Targeting Signals and Novel Effectors Studied with a Cya Translocation Reporter , 2004, Journal of bacteriology.

[43]  S. Phillips,et al.  Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Jia Liu,et al.  The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  H. Stahlberg,et al.  Type III Protein Translocase , 2003, Journal of Biological Chemistry.

[46]  U. Bonas,et al.  Getting across—bacterial type III effector proteins on their way to the plant cell , 2002, The EMBO journal.

[47]  C. Stevens,et al.  The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ , 2002, The EMBO journal.

[48]  J. Davison Genetic tools for pseudomonads, rhizobia, and other gram-negative bacteria. , 2002, BioTechniques.

[49]  J. Weissenbach,et al.  Genome sequence of the plant pathogen Ralstonia solanacearum , 2002, Nature.

[50]  B. Goldman,et al.  Genome Sequence of the Plant Pathogen and Biotechnology Agent Agrobacterium tumefaciens C58 , 2001, Science.

[51]  J A Eisen,et al.  The Genome of the Natural Genetic Engineer Agrobacterium tumefaciens C58 , 2001, Science.

[52]  S. Hutcheson,et al.  Enhancer-Binding Proteins HrpR and HrpS Interact To Regulate hrp-Encoded Type III Protein Secretion inPseudomonas syringae Strains , 2001, Journal of bacteriology.

[53]  S. He,et al.  Visualization of secreted Hrp and Avr proteins along the Hrp pilus during type III secretion in Erwinia amylovora and Pseudomonas syringae , 2001, Molecular microbiology.

[54]  M. Romantschuk,et al.  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. , 2001, Molecular plant-microbe interactions : MPMI.

[55]  P. Hart,et al.  Immunogold labeling of Hrp pili of Pseudomonas syringae pv. tomato assembled in minimal medium and in planta. , 2001, Molecular plant-microbe interactions : MPMI.

[56]  C. Stevens,et al.  HrpZ(Psph) from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[57]  N. Panopoulos,et al.  Elicitation of hypersensitive cell death by extracellularly targeted HrpZPsph produced in planta. , 2000, Molecular plant-microbe interactions : MPMI.

[58]  D. A. Palmieri,et al.  The genome sequence of the plant pathogen Xylella fastidiosa , 2000, Nature.

[59]  M. Zaitlin Elucidation of the genome organization of tobacco mosaic virus. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[60]  C. Hueck,et al.  Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants , 1998, Microbiology and Molecular Biology Reviews.

[61]  M. Romantschuk,et al.  Purified HrpA of Pseudomonas syringae pv. tomato DC3000 reassembles into pili , 1997, FEBS letters.

[62]  Jonathan D. G. Jones,et al.  PLANT DISEASE RESISTANCE GENES. , 1997, Annual review of plant physiology and plant molecular biology.

[63]  A. Møller,et al.  Genetics of host-parasite interactions. , 1997, Trends in ecology & evolution.

[64]  S. He,et al.  Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[65]  B. Turgeon,et al.  Molecular-genetic evaluation of fungal molecules for roles in pathogenesis to plants , 1996, Journal of Genetics.

[66]  J. Walton,et al.  Host-selective toxins: agents of compatibility. , 1996, The Plant cell.

[67]  A. Bogdanove,et al.  Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria , 1996, Molecular microbiology.

[68]  W. Aufsatz,et al.  The hrpRS locus of Pseudomonas syringae pv. phaseolicola constitutes a complex regulatory unit , 1995, Molecular microbiology.

[69]  S. Hutcheson,et al.  A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae , 1994, Journal of bacteriology.

[70]  S. Heu,et al.  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 , 1994, Journal of bacteriology.

[71]  A. Bent,et al.  Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes , 1993, Journal of bacteriology.

[72]  B. Staskawicz,et al.  Molecular characterization and hrp dependence of the avirulence gene avrPro from Pseudomonas syringae pv. tomato , 1993, Molecular and General Genetics MGG.

[73]  S. Briggs,et al.  Reductase activity encoded by the HM1 disease resistance gene in maize. , 1992, Science.

[74]  C. Boucher,et al.  hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. , 1992, Molecular plant-microbe interactions : MPMI.

[75]  M. Mindrinos,et al.  Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola , 1992, Journal of bacteriology.

[76]  S. Heu,et al.  Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster , 1992, Journal of bacteriology.

[77]  M. Mindrinos,et al.  Genetic and transcriptional organization of the hrp cluster of Pseudomonas syringae pv. phaseolicola , 1991, Journal of bacteriology.

[78]  B. Staskawicz,et al.  Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. , 1989, Science.

[79]  N. Panopoulos,et al.  The predicted protein product of a pathogenicity locus from Pseudomonas syringae pv. phaseolicola is homologous to a highly conserved domain of several procaryotic regulatory proteins , 1989, Journal of bacteriology.

[80]  S. Lindow,et al.  An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syringae pv. phaseolicola. , 1989, The EMBO journal.

[81]  C. Baker,et al.  Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants , 1988, Journal of bacteriology.

[82]  B. Staskawicz,et al.  Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae , 1988, Molecular and General Genetics MGG.

[83]  Gene Cluster of Pseudomonas syringae pv. “phaseolicola” Controls Pathogenicity of Bean Plants and Hypersensitivity on Nonhost Plants , 1987 .

[84]  N. Panopoulos,et al.  Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants , 1986, Journal of bacteriology.

[85]  D. K. Willis,et al.  Identification and cloning of genes involved in phaseolotoxin production by Pseudomonas syringae pv. "phaseolicola" , 1986, Journal of bacteriology.

[86]  S. Lindow,et al.  Cloning and expression of bacterial ice nucleation genes in Escherichia coli , 1985, Journal of bacteriology.

[87]  B. Staskawicz,et al.  Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[88]  M. Schroth,et al.  Genetic Analysis of Fluorescent Pigment Production in Pseudomonas syringae pv. syringae , 1984 .

[89]  K. Timmis,et al.  Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. , 1981, Gene.

[90]  J. V. Leary,et al.  Genetic Systems in Phytopathogenic Bacteria , 1979 .

[91]  D. Fulbright,et al.  Linkage analysis of Pseudomonas glycinea , 1978, Journal of bacteriology.

[92]  D. Pring,et al.  Heterogeneity of Maize Cytoplasmic Genomes among Male-Sterile Cytoplasms. , 1978, Genetics.

[93]  M. Schroth,et al.  Genetic transfer of Pseudomonas aeruginosa R factors to plant pathogenic Erwinia species , 1975, Journal of bacteriology.

[94]  A. van Kammen,et al.  Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Samsun" and "Samsun NN". II. Changes in protein constitution after infection with tobacco mosaic virus. , 1970, Virology.

[95]  C. A. Knight,et al.  The coat protein gene of tobacco mosaic virus. I. Location of the gene by mixed infection. , 1968, Journal of molecular biology.

[96]  G. Stent That was the molecular biology that was. , 1968, Science.

[97]  N. Panopoulos,et al.  The relative mutability of the cnb loci in Hypomyces. , 1966, Canadian journal of genetics and cytology. Journal canadien de genetique et de cytologie.

[98]  C. A. Knight,et al.  Location of a local lesion gene in tobacco mosaic virus RNA. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Ph. Gitta L. Coaker,et al.  Plant Pathology , 1957, Nature.

[100]  O Appel,et al.  Disease Resistance in Plants , 1915, Nature.

[101]  P. D. de Wit Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato. , 2016, Annual review of phytopathology.

[102]  M. Kokkinidis,et al.  HrpG and HrpV proteins from the Type III secretion system of Erwinia amylovora form a stable heterodimer. , 2015, FEMS microbiology letters.

[103]  Chittaranjan Kole,et al.  Genomics of Plant-Associated Bacteria , 2014, Springer Berlin Heidelberg.

[104]  C. Zipfel,et al.  Effector biology of plant-associated organisms: concepts and perspectives. , 2012, Cold Spring Harbor symposia on quantitative biology.

[105]  J. Mansfield,et al.  Negative regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. , 2010, Molecular plant-microbe interactions : MPMI.

[106]  R. Jackson Plant pathogenic bacteria : genomics and molecular biology , 2009 .

[107]  E. Nester Agrobacterium: The Natural Genetic Engineer 100 Years Later , 2008 .

[108]  H. Stahlberg,et al.  Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. , 2003, The Journal of biological chemistry.

[109]  M. Chilton Agrobacterium. A memoir. , 2001, Plant physiology.

[110]  G. Cornelis,et al.  Assembly and function of type III secretory systems. , 2000, Annual review of microbiology.

[111]  S. He,et al.  Type III protein secretion systems in plant and animal pathogenic bacteria. , 1998, Annual review of phytopathology.

[112]  P. Lindgren The role of hrp genes during plant-bacterial interactions. , 1997, Annual review of phytopathology.

[113]  A. Osbourn,et al.  Molecular dissection of fungal phytopathogenicity. , 1995, Microbiology.

[114]  U. Bonas hrp genes of phytopathogenic bacteria. , 1994, Current topics in microbiology and immunology.

[115]  W. Schafer MOLECULAR MECHANISMS OF FUNGAL PATHOGENICITY TO PLANTS , 1994 .

[116]  C. Boucher,et al.  Molecular Genetics of Pathogenicity Determinants of Pseudomonas Solanacearum with Special Emphasis on HRP Genes , 1992 .

[117]  D. K. Willis,et al.  Current ReviewhrpGenes of Phytopathogenic Bacteria , 1991 .

[118]  D. Holden,et al.  Molecular Genetic Approaches to the Study of Fungal Pathogenesis , 1989 .

[119]  A. Osbourn,et al.  Molecular Genetics of Pathogenicity in Phytopathogenic Bacteria , 1988 .

[120]  Christopher M Thomas,et al.  Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. , 1987, Annual review of microbiology.

[121]  D. Singh,et al.  Genetics of Host-Parasite Interaction , 1986 .

[122]  D. Mills Transposon Mutagenesis and its Potential for Studying Virulence Genes in Plant Pathogens , 1985 .

[123]  N. Panopoulos,et al.  The Molecular Genetics of Plant Pathogenic Bacteria and their Plasmids , 1985 .

[124]  D. K. Willis,et al.  Genetic and Biochemical Basis of Virulence in Plant Pathogens , 1984 .

[125]  K. Timmis,et al.  Host: vector systems for gene cloning in Pseudomonas. , 1982, Current topics in microbiology and immunology.

[126]  R. Durbin Chapter 14 – Applications , 1981 .

[127]  R. Durbin Toxins in plant disease. , 1981 .

[128]  M. Starr,et al.  Genetics of Erwinia species. , 1980, Annual review of microbiology.

[129]  B. Holloway Plasmids that mobilize bacterial chromosome. , 1979, Plasmid.

[130]  J. Vanderplank Genetic and molecular basis of plant pathogenesis. , 1978 .

[131]  N. Panopoulos Sulfate Uptake and Translocation in Curly Top Infected Tomatoes , 1975 .

[132]  J. Turner The Quantitative Relation Between Plant and Bacterial Cells Involved in the Hypersensitive Reaction , 1974 .

[133]  N. Panopoulos Role of Flagellar Motility in the Invasion of Bean Leaves by Pseudomonas phaseolicola , 1974 .

[134]  A. van Kammen Plant viruses with a divided genome. , 1972, Annual review of phytopathology.