Signals Involved in Arabidopsis Resistance toTrichoplusia ni Caterpillars Induced by Virulent and Avirulent Strains of the Phytopathogen Pseudomonas syringae 1

Plants have evolved different but interconnected strategies to defend themselves against herbivorous insects and microbial pathogens. We used an Arabidopsis/Pseudomonas syringaepathosystem to investigate the impact of pathogen-induced defense responses on cabbage looper (Trichoplusia ni) larval feeding. Arabidopsis mutants [npr1,pad4, eds5, andsid2(eds16)] or transgenic plants (nahG) that are more susceptible to microbial pathogens and are compromised in salicylic acid (SA)-dependent defense responses exhibited reduced levels of feeding by T. ni compared with wild-type plants. Consistent with these results, Arabidopsis mutants that are more resistant to microbial pathogens and have elevated levels of SA (cpr1 and cpr6) exhibited enhanced levels of T. ni feeding. These experiments suggested an inverse relationship between an active SA defense pathway and insect feeding. In contrast to these results, there was increased resistance toT. ni in wild-type Arabidopsis ecotype Columbia plants that were infected with P. syringae pv.maculicola strain ES4326 (Psm ES4326) expressing the avirulence genes avrRpt2 oravrB, which elicit a hypersensitive response, high levels of SA accumulation, and systemic acquired resistance to bacterial infection. Similar results were obtained with other ecotypes, including Landsberg erecta, Cape Verdi Islands, and Shakdara. When infected with PsmES4326(avrRpt2) or PsmES4326(avrB), nahG transgenic andnpr1 mutant plants (which are more susceptible to virulent and avirulent P. syringae strains) failed to show the increased insect resistance exhibited by wild-type plants. It was surprising that wild-type plants, as well as nahGand npr1 plants, infected with Psm ES4326 not expressing avrRpt2 or avrB, which elicits disease, became more susceptible to T. ni. Our results suggest two potentially novel systemic signaling pathways: a systemic response elicited by HR that leads to enhanced T. ni resistance and overrides the SA-mediated increase in T. ni susceptibility, and a SA-independent systemic response induced by virulent pathogens that leads to enhanced susceptibility to T. ni.

[1]  M. Newman,et al.  Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4 , 2001, The EMBO journal.

[2]  J. Glazebrook,et al.  Genes controlling expression of defense responses in Arabidopsis--2001 status. , 2001, Current opinion in plant biology.

[3]  E. Stahl,et al.  Evolutionary Dynamics of Plant R-Genes , 2001, Science.

[4]  F. Ausubel,et al.  The TASTY locus on chromosome 1 of Arabidopsis affects feeding of the insect herbivore Trichoplusia ni. , 2001, Plant physiology.

[5]  M. Axtell,et al.  Mutational analysis of the Arabidopsis RPS2 disease resistance gene and the corresponding pseudomonas syringae avrRpt2 avirulence gene. , 2001, Molecular plant-microbe interactions : MPMI.

[6]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[7]  F. Ausubel,et al.  Mutational Analysis of the Arabidopsis Nucleotide Binding Site–Leucine-Rich Repeat Resistance Gene RPS2 , 2000, Plant Cell.

[8]  T. Eulgem,et al.  The transcriptome of Arabidopsis thaliana during systemic acquired resistance , 2000, Nature Genetics.

[9]  J. J. Grant,et al.  Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. , 2000, The Plant journal : for cell and molecular biology.

[10]  T. Mitchell-Olds,et al.  Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. , 2000, Plant physiology.

[11]  F. Ausubel,et al.  Roles of Salicylic Acid, Jasmonic Acid, and Ethylene in cpr-Induced Resistance in Arabidopsis , 2000, Plant Cell.

[12]  S. Somerville,et al.  Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. C. Heath Hypersensitive response-related death , 2000, Plant Molecular Biology.

[14]  F. Ausubel,et al.  Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. , 2000, The Plant journal : for cell and molecular biology.

[15]  E. Lam,et al.  Nitric oxide and salicylic acid signaling in plant defense. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[16]  P. Hatcher,et al.  On integrating molecular and ecological studies of plant resistance: variety of mechanisms and breadth of antagonists , 2000 .

[17]  C. Pieterse,et al.  Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Luthe,et al.  A Unique 33-kD Cysteine Proteinase Accumulates in Response to Larval Feeding in Maize Genotypes Resistant to Fall Armyworm and Other Lepidoptera , 2000, Plant Cell.

[19]  R. Karban,et al.  Jasmonic Acid Induced Resistance in Grapevines to a Root and Leaf Feeder , 2000, Journal of economic entomology.

[20]  F. Katagiri,et al.  Eukaryotic Fatty Acylation Drives Plasma Membrane Targeting and Enhances Function of Several Type III Effector Proteins from Pseudomonas syringae , 2000, Cell.

[21]  P. Reymond,et al.  Differential Gene Expression in Response to Mechanical Wounding and Insect Feeding in Arabidopsis , 2000, Plant Cell.

[22]  F. Katagiri,et al.  A resistance gene product of the nucleotide binding site -- leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. , 2000, The Plant journal : for cell and molecular biology.

[23]  J. Taylor,et al.  Coping with multiple enemies: an integration of molecular and ecological perspectives. , 2000, Trends in plant science.

[24]  J. Dangl,et al.  Signal transduction in the plant immune response. , 2000, Trends in biochemical sciences.

[25]  C. Pieterse,et al.  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 , 1999, Plant Molecular Biology.

[26]  D. Guttman,et al.  The Gain-of-Function Arabidopsis acd6 Mutant Reveals Novel Regulation and Function of the Salicylic Acid Signaling Pathway in Controlling Cell Death, Defenses, and Cell Growth , 1999, Plant Cell.

[27]  E. Stahl,et al.  Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis , 1999, Nature.

[28]  Jean-Pierre Métraux,et al.  Salicylic Acid Induction–Deficient Mutants of Arabidopsis Express PR-2 and PR-5 and Accumulate High Levels of Camalexin after Pathogen Inoculation , 1999, Plant Cell.

[29]  J. Glazebrook Genes controlling expression of defense responses in Arabidopsis. , 1999, Current opinion in plant biology.

[30]  R. Bostock,et al.  Trade-Offs in Plant Defense Against Pathogens and Herbivores: A Field Demonstration of Chemical Elicitors of Induced Resistance , 1999, Journal of Chemical Ecology.

[31]  C. Preston,et al.  Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants , 1999, Planta.

[32]  J. Ecker,et al.  EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. , 1999, Science.

[33]  K. Maleck,et al.  Defense on multiple fronts: how do plants cope with diverse enemies? , 1999, Trends in plant science.

[34]  R. Dixon,et al.  Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory , 1999, Current Biology.

[35]  Jonathan D. G. Jones,et al.  EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  R. Bostock,et al.  Signal interactions in pathogen and insect attack: Systemic plant-mediated interactions between pathogens and herbivores of the tomato, Lycopersicon esculentum , 1999 .

[37]  C. Pieterse,et al.  Salicylic acid-independent plant defence pathways. , 1999, Trends in plant science.

[38]  J. Dangl,et al.  The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Rebecca L. Brown,et al.  The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid , 1998, Plant Molecular Biology.

[40]  B. Thomma,et al.  Concomitant Activation of Jasmonate and Ethylene Response Pathways Is Required for Induction of a Plant Defensin Gene in Arabidopsis , 1998, Plant Cell.

[41]  J. Tumlinson,et al.  Concerted biosynthesis of an insect elicitor of plant volatiles. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  F. Ausubel,et al.  Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. , 1998, The Plant journal : for cell and molecular biology.

[43]  C. Wasternack,et al.  Wounding and chemicals induce expression of the Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via the octadecanoid pathway , 1998, FEBS letters.

[44]  C. Pieterse,et al.  A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis , 1998, Plant Cell.

[45]  J. Parker,et al.  Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Xinnian Dong,et al.  SA, JA, ethylene, and disease resistance in plants. , 1998, Current opinion in plant biology.

[47]  I. Baldwin Jasmonate-induced responses are costly but benefit plants under attack in native populations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  D F Klessig,et al.  PAD4 Functions Upstream from Salicylic Acid to Control Defense Responses in Arabidopsis , 1998, Plant Cell.

[49]  I. Mitsuhara,et al.  Antagonistic Effect of Salicylic Acid and Jasmonic Acid on the Expression of Pathogenesis-Related (PR) Protein Genes in Wounded Mature Tobacco Leaves , 1998 .

[50]  D. Klessig,et al.  Uncoupling PR Gene Expression from NPR1 and Bacterial Resistance: Characterization of the Dominant Arabidopsis cpr6-1 Mutant , 1998, Plant Cell.

[51]  R. Dixon,et al.  Evidence for Chewing Insect-Specific Molecular Events Distinct from a General Wound Response in Leaves , 1997, Plant physiology.

[52]  F. Ausubel,et al.  Use of Arabidopsis for genetic dissection of plant defense responses. , 1997, Annual review of genetics.

[53]  D F Klessig,et al.  The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. , 1997, The Plant cell.

[54]  R. Creelman,et al.  Jasmonate is essential for insect defense in Arabidopsis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  F. Ausubel,et al.  Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. , 1997, The Plant cell.

[56]  J. Ryals,et al.  The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. , 1997, The Plant cell.

[57]  Jane Glazebrook,et al.  The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats , 1997, Cell.

[58]  H. Leyser,et al.  Ethylene as a Signal Mediating the Wound Response of Tomato Plants , 1996, Science.

[59]  Franky R. G. Terras,et al.  Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. , 1996, The Plant cell.

[60]  J. Parker,et al.  Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. , 1996, The Plant cell.

[61]  G. Howe,et al.  An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. , 1996, The Plant cell.

[62]  F. Ausubel,et al.  Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. , 1996, Genetics.

[63]  J. Renwick,et al.  Effects of ultraviolet-B exposure of Arabidopsis thaliana on herbivory by two crucifer-feeding insects (Lepidoptera) , 1996 .

[64]  J. Ryals,et al.  Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. , 1995, Molecular plant-microbe interactions : MPMI.

[65]  J. Dangl,et al.  Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance , 1995, Science.

[66]  E. Weiler,et al.  Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid , 1995, Plant physiology.

[67]  J. Ryals,et al.  Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance , 1995 .

[68]  J. Ryals,et al.  Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[69]  D. Klessig,et al.  A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. , 1994, The Plant cell.

[70]  E. Ward,et al.  A Central Role of Salicylic Acid in Plant Disease Resistance , 1994, Science.

[71]  Xinnian Dong,et al.  Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance. , 1994, The Plant cell.

[72]  F. Ausubel,et al.  Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[73]  E. Ward,et al.  Salicylic Acid Is Not the Translocated Signal Responsible for Inducing Systemic Acquired Resistance but Is Required in Signal Transduction. , 1994, The Plant cell.

[74]  J. Dangl,et al.  Arabidopsis mutants simulating disease resistance response , 1994, Cell.

[75]  F. Ausubel,et al.  Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions , 1994, Cell.

[76]  A. Bent,et al.  Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean. , 1993, The Plant journal : for cell and molecular biology.

[77]  F. Ausubel,et al.  Arabidopsis mutants compromised for the control of cellular damage during pathogenesis and aging. , 1993, The Plant journal : for cell and molecular biology.

[78]  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.

[79]  A. Bent,et al.  RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. , 1993, The Plant cell.

[80]  L. Willmitzer,et al.  Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis , 1993, Planta.

[81]  F. Ausubel,et al.  Arabidopsis mutations at the RPS2 locus result in loss of resistance to Pseudomonas syringae strains expressing the avirulence gene avrRpt2. , 1993, Molecular plant-microbe interactions : MPMI.

[82]  N. Shaw,et al.  Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. , 1993, Molecular plant-microbe interactions : MPMI.

[83]  I. Somssich,et al.  Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 disease resistance locus. , 1992, The EMBO journal.

[84]  J. Dangl,et al.  Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. , 1991, The Plant journal : for cell and molecular biology.

[85]  E. Ward,et al.  Differential Regulation of beta-1,3-Glucanase Messenger RNAs in Response to Pathogen Infection. , 1991, Plant physiology.

[86]  F. Ausubel,et al.  Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. , 1991, The Plant cell.

[87]  B. Staskawicz,et al.  Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. , 1991, The Plant cell.

[88]  D. Bowles,et al.  The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids , 1988 .

[89]  Bruce A. McPheron,et al.  Interactions Among Three Trophic Levels: Influence of Plants on Interactions Between Insect Herbivores and Natural Enemies , 1980 .

[90]  K. F. Harris,et al.  Vectors of Plant Pathogens , 1980 .

[91]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[92]  H. Shorey,et al.  The Biology of Trichoplusia ni (Lepidoptera: Noctuidae). I. Life History and Behavior , 1962 .

[93]  A. Ross,et al.  Localized acquired resistance to plant virus infection in hypersensitive hosts. , 1961, Virology.

[94]  King Eo,et al.  Two simple media for the demonstration of pyocyanin and fluorescin. , 1954 .

[95]  K. S. Chester The Problem of Acquired Physiological Immunity in Plants , 1933, The Quarterly Review of Biology.

[96]  D. Klessig,et al.  The cpr 5 Mutant of Arabidopsis Expresses Both NPRl-Dependent and NPRl-1 ndependent Resistance , 2002 .

[97]  P. Pare Concerted biosynthesis of an elicitor of plant volatiles , 1998 .

[98]  D. Klessig,et al.  Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. , 1997, Molecular plant-microbe interactions : MPMI.

[99]  R. Dixon,et al.  Early events in the activation of plant defense responses , 1994 .

[100]  Leslie Friedrich,et al.  Biological induction of systemic acquired resistance in Arabidopsis , 1993 .

[101]  P. Ahl-Goy,et al.  Differential Regulation of,-1,3-Glucanase Messenger RNAsinResponse toPathogen Infection , 1991 .

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

[103]  E. King,et al.  Two simple media for the demonstration of pyocyanin and fluorescin. , 1954, The Journal of laboratory and clinical medicine.