The Effect of Nitrogen on Disease Development and Gene Expression in Bacterial and Fungal Plant Pathogens

Successful colonisation of plants by pathogens requires efficient utilisation of nutrient resources available in host tissues. Several bacterial and fungal genes are specifically induced during pathogenesis and under nitrogen-limiting conditions in vitro. This suggests that a nitrogen-limiting environment may be one of the cues for disease symptom development during growth of the pathogens in planta. Here we review recent literature on the effect of nitrogen and nitrogen-regulated genes on disease development, caused by phytopathogenic bacteria and fungi. Furthermore, the potential influence of nitrogen-limitation or general nutrient limitation on several in planta-induced bacterial and fungal pathogenicity, virulence and avirulence genes will be discussed.

[1]  B. Carpenter,et al.  NUT1, a major nitrogen regulatory gene inMagnaporthe grisea, is dispensable for pathogenicity , 1996, Molecular and General Genetics MGG.

[2]  G. Marzluf,et al.  nit-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C. Mortensen,et al.  Bioassay of Toxins as a Diagnostic Method for Pseudomonas syringae Pathovars , 1992 .

[4]  B. Staskawicz,et al.  Prokaryotic plant parasites , 1993, Cell.

[5]  J. Hamer,et al.  Regulatory Genes Controlling MPG1 Expression and Pathogenicity in the Rice Blast Fungus Magnaporthe grisea. , 1996, The Plant cell.

[6]  G. Marzluf,et al.  Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi , 1999, Molecular and General Genetics MGG.

[7]  P. Cossart,et al.  Pleiotropic control of Listeria monocytogenes virulence factors by a gene that is autoregulated , 1991, Molecular microbiology.

[8]  G. Reubel,et al.  Identification, cloning and sequence analysisof the equine adenovirus 1 hexon gene , 1997, Archives of Virology.

[9]  D. Huber,et al.  Nitrogen form and plant disease. , 1974, Annual review of phytopathology.

[10]  D. K. Willis,et al.  IN PSEUDOMONAS SYRINGAE , 2004 .

[11]  N. Keen,et al.  Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. , 1995, Molecular plant-microbe interactions : MPMI.

[12]  J. Kan,et al.  Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. , 1991 .

[13]  H. Ochman,et al.  How Salmonella became a pathogen. , 1997, Trends in microbiology.

[14]  A. S. Lynch,et al.  Regulation of Gene Expression in Escherichia coli , 1996, Springer US.

[15]  T. Goosen,et al.  Transcription of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by a GATA-type transcription factor in Aspergillus nidulans , 1999, Molecular and General Genetics MGG.

[16]  N. Crawford,et al.  Nitrate: nutrient and signal for plant growth. , 1995, The Plant cell.

[17]  G. Marzluf,et al.  Molecular cloning and analysis of nre, the major nitrogen regulatory gene of Penicillium chrysogenum , 2004, Current Genetics.

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

[19]  G. Marzluf,et al.  The negative-acting NMR regulatory protein of Neurospora crassa binds to and inhibits the DNA-binding activity of the positive-acting nitrogen regulatory protein NIT2. , 1995, Biochemistry.

[20]  Kate J. Graham,et al.  The structures of syringolides 1 and 2, novel C-glycosidic elicitors from Pseudomonas syringae pv. tomato , 1993 .

[21]  J. Turner,et al.  Tabtoxin-induced symptoms are associated with the accumulation of ammonia formed during photorespiration , 1982 .

[22]  U. Bonas,et al.  Recognition of bacterial avirulence proteins occurs inside the plant cell: a general phenomenon in resistance to bacterial diseases? , 1997, The Plant journal : for cell and molecular biology.

[23]  Gerald R. Fink,et al.  Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: Regulation by starvation and RAS , 1992, Cell.

[24]  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.

[25]  A. Bogdanove,et al.  Erwinia amylovora Secretes DspE, a Pathogenicity Factor and Functional AvrE Homolog, through the Hrp (Type III Secretion) Pathway , 1998, Journal of bacteriology.

[26]  J. Lucas,et al.  Plant pathology and plant pathogens , 1986 .

[27]  R. Reuter,et al.  Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif , 1999, The EMBO journal.

[28]  K. Moore,et al.  Nitrogen starvation of the rice blast fungusMagnaporthe griseamay act as an environmental cue for disease symptom expression , 1997 .

[29]  F. Cánovas,et al.  Cytosolic localization in tomato mesophyll cells of a novel glutamine synthetase induced in response to bacterial infection or phosphinothricin treatment , 1998, Planta.

[30]  W. J. Hooker,et al.  PLANT NUTRITION IN RELATION TO DISEASE DEVELOPMENT. I. CABBAGE YELLOWS , 1945 .

[31]  A. Bailey,et al.  Cloning and characterisation of a gene encoding a cuticle-degrading protease from the insect pathogenic fungus Metarhizium anisopliae. , 1995, Gene.

[32]  M. Gallegly,et al.  PLANT NUTRITION IN RELATION TO DISEASE DEVELOPMENT. V. BACTERIAL WILT OF TOMATO , 1949 .

[33]  F. Chumley,et al.  Molecular genetic analysis of the rice blast fungus, magnaporthe grisea. , 1991, Annual review of phytopathology.

[34]  J. Aguirre,et al.  Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. , 1995, Microbiology.

[35]  R. Leger The role of cuticle-degrading proteases in fungal pathogenesis of insects , 1995 .

[36]  D. Frank,et al.  Molecular cloning and regulatory analysis of the cuticle-degrading-protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. , 1992, European journal of biochemistry.

[37]  G. V. D. Ackerveken,et al.  Nitrogen limitation induces expression of the avirulence gene avr9 in the tomato pathogen Cladosporium fulvum , 1994, Molecular and General Genetics MGG.

[38]  R. Bieleski,et al.  Involvement of phaseolotoxin in halo blight of beans: transport and conversion to functional toxin. , 1977, Plant physiology.

[39]  G. Coruzzi,et al.  THE MOLECULAR-GENETICS OF NITROGEN ASSIMILATION INTO AMINO ACIDS IN HIGHER PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[40]  G. Marzluf,et al.  Nucleotide sequence and analysis of NMR, a negative-acting regulatory gene in the nitrogen circuit of Neurospora crassa , 1990, Molecular and General Genetics MGG.

[41]  R. Oliver,et al.  Isolation and characterisation of five different hydrophobin-encoding cDNAs from the fungal tomato pathogen Cladosporium fulvum , 1999, Molecular and General Genetics MGG.

[42]  R. C. Spangler Cladosporium fulvum , 1924, Botanical Gazette.

[43]  N. Keen,et al.  Characterization of the promoter of avirulence gene D from Pseudomonas syringae pv. tomato , 1993, Journal of bacteriology.

[44]  M. Spector The starvation-stress response (SSR) of Salmonella. , 1998, Advances in microbial physiology.

[45]  R. Durbin,et al.  The role of intercellular fluid and bacterial isolate on the in vivo production of tabtoxin and tabtoxinine- β-lactarn , 1984 .

[46]  M. Hensel,et al.  The role of the Aspergillus fumigatusareA gene in invasive pulmonary aspergillosis , 1998, Molecular and General Genetics MGG.

[47]  G. Cornelis,et al.  The rpoS gene from Yersinia enterocolitica and its influence on expression of virulence factors , 1995, Infection and immunity.

[48]  I. Roberts,et al.  Identification and Characterization of theErwinia amylovora rpoS Gene: RpoS Is Not Involved in Induction of Fireblight Disease Symptoms , 1998, Journal of bacteriology.

[49]  A. Tunlid,et al.  Sequence analysis and regulation of a gene encoding a cuticle-degrading serine protease from the nematophagous fungus Arthrobotrys oligospora. , 1996, Microbiology.

[50]  T. Christensen,et al.  Role of the Regulatory Gene areA ofAspergillus oryzae in Nitrogen Metabolism , 1998, Applied and Environmental Microbiology.

[51]  U. Bonas,et al.  The Xanthomonas Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[52]  A. Andrianopoulos,et al.  Characterization of the Aspergillus nidulans nmrA Gene Involved in Nitrogen Metabolite Repression , 1998, Journal of bacteriology.

[53]  Keen Nt,et al.  Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. , 1995 .

[54]  G. Balestra,et al.  Influence of Nitrogen Fertilization on the Colonization of Olive Phylloplane by Pseudomonas syringae subsp. savastanoi. , 1997 .

[55]  F. Fang,et al.  RpoS is necessary for both the positive and negative regulation of starvation survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium , 1994, Journal of bacteriology.

[56]  A. Bailey,et al.  Isolation of a nitrogen response regulator gene (nrr1) from Metarhizium anisopliae. , 1998, Gene.

[57]  U. Bonas,et al.  Expression of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors , 1991, Journal of bacteriology.

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

[59]  J. Paulin,et al.  DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB‐dependent way , 1997, Molecular microbiology.

[60]  S. Hutcheson,et al.  Influence of Pseudomonas syringae culture conditions on initiation of the hypersensitive response of culture tobacco cells , 1989, Applied and environmental microbiology.

[61]  M. Fěvre,et al.  Isolation and expression of a nitrogen regulatory gene, nmc, of Penicillium roqueforti. , 1999, FEMS microbiology letters.

[62]  J. Dangl The enigmatic avirulence genes of phytopathogenic bacteria. , 1994, Current topics in microbiology and immunology.

[63]  G. Van den Ackerveken,et al.  Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. , 1991, Molecular plant-microbe interactions : MPMI.

[64]  W. Niemczura,et al.  Inhibitors of Ornithine Carbamoyltransferase from Pseudomonas syringae pv. phaseolicola. st]Revised Structure of Phaseolotoxin , 1984 .

[65]  D. Gross,et al.  Pseudomonas syringae Phytotoxins: Mode of Action, Regulation, and Biosynthesis by Peptide and Polyketide Synthetases , 1999, Microbiology and Molecular Biology Reviews.

[66]  N. Dunn-Coleman,et al.  The regulation of nitrate assimilation in Neurospora crassa: The isolation and genetic analysis of nmr-1 mutants , 2004, Molecular and General Genetics MGG.

[67]  B. Völksch,et al.  Toxin production by pathovars of Pseudomonas syringae and their antagonistic activities against epiphytic microorganisms , 1998, Journal of basic microbiology.

[68]  R. Mitchell Isolation and structure of a chlorosis-inducing toxin of Pseudomonas phaseolicola , 1976 .

[69]  J. Visser,et al.  Identification, cloning and sequence of the Aspergillus niger areA wide domain regulatory gene controlling nitrogen utilisation. , 1998, Biochimica et biophysica acta.

[70]  T. Bisseling,et al.  Symbiotic Nitrogen Fixation. , 1995, The Plant cell.

[71]  P. De Wit,et al.  THE TOMATO-CLADOSPORIUM FULVUM INTERACTION: A Versatile Experimental System to Study Plant-Pathogen Interactions. , 1999, Annual review of phytopathology.

[72]  G. Marzluf,et al.  Amino-acid substitutions in the zinc finger of NIT2, the nitrogen regulatory protein of Neurospora crassa, alter promoter element recognition , 1993, Current Genetics.

[73]  M. Coleman,et al.  Starvation-induced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. , 1997, Molecular plant-microbe interactions : MPMI.

[74]  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.

[75]  M. Hensel,et al.  Regulation of fungal extracellular proteases and their role in mammalian pathogenesis , 1995 .

[76]  F. Cánovas,et al.  Differential expression of glutamine synthetase isoforms in tomato detached leaflets infected with Pseudomonas syringae pv. tomato , 1995 .

[77]  C. Scazzocchio,et al.  The intergenic region between the divergently transcribed niiA and niaD genes of Aspergillus nidulans contains multiple NirA binding sites which act bidirectionally , 1995, Molecular and cellular biology.

[78]  N J Talbot,et al.  Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. , 1998, Fungal genetics and biology : FG & B.

[79]  R. Dixon,et al.  Activation, structure, and organization of genes involved in microbial defense in plants. , 1990, Advances in genetics.

[80]  N. Talbot,et al.  Having a blast: exploring the pathogenicity of Magnaporthe grisea. , 1995, Trends in microbiology.

[81]  S. Gold,et al.  Construction of a Tn7-lux system for gene expression studies in gram-negative bacteria. , 1992, Gene.

[82]  M. Stayton,et al.  Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. , 1990 .

[83]  S. Beer,et al.  Expression of Erwinia amylovora hrp genes in response to environmental stimuli , 1992, Journal of bacteriology.

[84]  A. Showalter,et al.  Structure and function of plant cell wall proteins. , 1993, The Plant cell.

[85]  M. Rhen,et al.  Role of rpoS in the regulation of Salmonella plasmid virulence (spv) genes. , 1994, FEMS microbiology letters.

[86]  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.

[87]  R. Curtiss,et al.  Role of sigma factor RpoS in initial stages of Salmonella typhimurium infection , 1997, Infection and immunity.

[88]  J. Wessels,et al.  Hydrophobins: proteins that change the nature of the fungal surface. , 1997, Advances in microbial physiology.

[89]  G. Van den Ackerveken,et al.  Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. , 1992, The Plant journal : for cell and molecular biology.

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

[91]  J. Manners,et al.  Cloning and characterisation of glutamine synthetase from Colletotrichum gloeosporioides and demonstration of elevated expression during pathogenesis on Stylosanthes guianensis , 1997, Current Genetics.

[92]  L. M. Albright,et al.  Prokaryotic signal transduction mediated by sensor and regulator protein pairs. , 1989, Annual review of genetics.

[93]  G. Marzluf,et al.  Genetic regulation of nitrogen metabolism in the fungi , 1997, Microbiology and molecular biology reviews : MMBR.

[94]  R. Edwards,et al.  Nitrogen control in bacteria. , 1995, Microbiological reviews.

[95]  N. Talbot,et al.  Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. , 1993, The Plant cell.

[96]  M. Hensel,et al.  The role of the Aspergillus fumigatus areA gene in invasive pulmonary aspergillosis. , 1998, Molecular & general genetics : MGG.

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

[98]  C. Scazzocchio The fungal GATA factors. , 2000, Current opinion in microbiology.

[99]  P. D. Wit Fungal avirulence genes and plant resistance genes: unravelling the molecular basis of gene-for-gene interactions. , 1995 .

[100]  P. W. Dyson,et al.  AN EFFECT OF NITROGEN ON THE FORMATION OF POTATO TUBERS AND THE INCIDENCE OF COMMON SCAB (STREPTOMYCES SCABIES) , 1966 .