Plant Stomata Function in Innate Immunity against Bacterial Invasion

Microbial entry into host tissue is a critical first step in causing infection in animals and plants. In plants, it has been assumed that microscopic surface openings, such as stomata, serve as passive ports of bacterial entry during infection. Surprisingly, we found that stomatal closure is part of a plant innate immune response to restrict bacterial invasion. Stomatal guard cells of Arabidopsis perceive bacterial surface molecules, which requires the FLS2 receptor, production of nitric oxide, and the guard-cell-specific OST1 kinase. To circumvent this innate immune response, plant pathogenic bacteria have evolved specific virulence factors to effectively cause stomatal reopening as an important pathogenesis strategy. We provide evidence that supports a model in which stomata, as part of an integral innate immune system, act as a barrier against bacterial infection.

[1]  D. Xie,et al.  COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. , 1998, Science.

[2]  Alain Vavasseur,et al.  Arabidopsis OST1 Protein Kinase Mediates the Regulation of Stomatal Aperture by Abscisic Acid and Acts Upstream of Reactive Oxygen Species Production Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.007906. , 2002, The Plant Cell Online.

[3]  B. Kunkel,et al.  The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. , 2005, Molecular plant pathology.

[4]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[5]  S. S. Hirano,et al.  Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte , 2000, Microbiology and Molecular Biology Reviews.

[6]  A. Hetherington,et al.  The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement , 2005, Nature.

[7]  P. Low,et al.  Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. , 1999, Plant physiology.

[8]  A. Collmer,et al.  Regulatory interactions between the Hrp type III protein secretion system and coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000. , 2000, Microbiology.

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

[10]  Sarah M Assmann,et al.  Guard cells: a dynamic signaling model. , 2004, Current opinion in plant biology.

[11]  S. Lindow,et al.  Microbiology of the Phyllosphere , 2003, Applied and Environmental Microbiology.

[12]  F. Katagiri,et al.  The Arabidopsis Thaliana-Pseudomonas Syringae Interaction , 2002, The arabidopsis book.

[13]  S. He,et al.  Suppression of host defense in compatible plant-Pseudomonas syringae interactions. , 2005, Current opinion in plant biology.

[14]  S. Akira,et al.  Toll-like receptors. , 2003, Annual review of immunology.

[15]  J. Dangl,et al.  Common and Contrasting Themes of Plant and Animal Diseases , 2001, Science.

[16]  J. D. Jones,et al.  K+ channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. , 1999, The Plant journal : for cell and molecular biology.

[17]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[18]  V. Morris,et al.  Characterization of a DNA region required for production of the phytotoxin coronatine by Pseudomonas syringae pv. tomato , 1991 .

[19]  H. Sambrook Molecular cloning : a laboratory manual. Cold Spring Harbor, NY , 1989 .

[20]  L. Beuchat Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. , 2002, Microbes and infection.

[21]  Alan Collmer,et al.  Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. , 2002, Trends in microbiology.

[22]  A. P. Kloek,et al.  Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. , 2001, The Plant journal : for cell and molecular biology.

[23]  S. Spiegel,et al.  Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins , 2003, Nature.

[24]  F. Ausubel Are innate immune signaling pathways in plants and animals conserved? , 2005, Nature Immunology.

[25]  T. Boller,et al.  FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. , 2000, Molecular cell.

[26]  J. Schroeder,et al.  GUARD CELL SIGNAL TRANSDUCTION. , 2003, Annual review of plant physiology and plant molecular biology.

[27]  S. Lindow,et al.  Plant Species and Plant Incubation Conditions Influence Variability in Epiphytic Bacterial Population Size , 2000, Microbial Ecology.

[28]  K. Davis,et al.  Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. , 1995, Molecular plant-microbe interactions : MPMI.

[29]  Eric D Mintz,et al.  Concurrent outbreaks of Shigella sonnei and enterotoxigenic Escherichia coli infections associated with parsley: implications for surveillance and control of foodborne illness. , 2003, Journal of food protection.

[30]  A. P. Kloek,et al.  Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. , 2004, Molecular plant-microbe interactions : MPMI.

[31]  T. Boller,et al.  Flagellin perception: a paradigm for innate immunity. , 2002, Trends in plant science.

[32]  S. Chisholm,et al.  Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response , 2022 .

[33]  E Bingen,et al.  [Escherichia coli O157:H7, an emerging pathogen]. , 1999, Presse medicale.

[34]  Alain Vavasseur,et al.  Cytoplasmic Alkalization Precedes Reactive Oxygen Species Production during Methyl Jasmonate- and Abscisic Acid-Induced Stomatal Closure1 , 2004, Plant Physiology.

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

[36]  A. Collmer,et al.  EFFECTOR PROTEINS : Double Agents in Bacterial Disease and Plant Defense , 2004 .

[37]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[38]  F. Ausubel,et al.  corrigendum: Isochorismate synthase is required to synthesize salicylic acid for plant defence , 2002, Nature.

[39]  G. Howe,et al.  Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. , 2003, The Plant journal : for cell and molecular biology.

[40]  M. B. Mudgett New insights to the function of phytopathogenic bacterial type III effectors in plants. , 2005, Annual review of plant biology.

[41]  Jeff H. Chang,et al.  A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[43]  B. Vinatzer,et al.  Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. , 2003, Current opinion in microbiology.

[44]  Paul R. Ebert,et al.  Antagonistic Interaction between Abscisic Acid and Jasmonate-Ethylene Signaling Pathways Modulates Defense Gene Expression and Disease Resistance in Arabidopsis , 2004, The Plant Cell Online.

[45]  F. Ausubel,et al.  Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[47]  S. Jacobsen,et al.  Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. , 1996, The Plant journal : for cell and molecular biology.

[48]  G. Martin,et al.  Strategies used by bacterial pathogens to suppress plant defenses. , 2004, Current opinion in plant biology.

[49]  S. He,et al.  Powerful screens for bacterial virulence proteins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[50]  S. He,et al.  A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Jonathan D. G. Jones,et al.  Bacterial disease resistance in Arabidopsis through flagellin perception , 2004, Nature.

[52]  S. Park,et al.  Escherichia coli O157:H7 As An Emerging Foodborne Pathogen: A Literature Review , 2001, Critical reviews in food science and nutrition.

[53]  S. He,et al.  A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Frederick M. Ausubel,et al.  Isochorismate synthase is required to synthesize salicylic acid for plant defence , 2001, Nature.

[55]  T. Hartung,et al.  Innate immunity in Arabidopsis thaliana: lipopolysaccharides activate nitric oxide synthase (NOS) and induce defense genes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Sheng Yang He,et al.  Type III protein secretion mechanism in mammalian and plant pathogens. , 2004, Biochimica et biophysica acta.

[57]  M. G. Kim,et al.  Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis , 2005, Cell.