The effects of extracellular adenosine 5′‐triphosphate on the tobacco proteome

Extracellular adenosine 5′‐triphosphate (eATP) is emerging as an important plant signalling compound capable of mobilising intracellular second messengers such as Ca2+, nitric oxide, and reactive oxygen species. However, the downstream molecular targets and the spectrum of physiological processes that eATP regulates are largely unknown. We used exogenous ATP and a non‐hydrolysable analogue as probes to identify the molecular and physiological effects of eATP‐mediated signalling in tobacco. 2‐DE coupled with MS/MS analysis revealed differential protein expression in response to perturbation of eATP signalling. These proteins are in several functional classes that included photosynthesis, mitochondrial ATP synthesis, and defence against oxidative stress, but the biggest response was in the pathogen defence‐related proteins. Consistent with this, impairment of eATP signalling induced resistance against the bacterial pathogen Erwinia carotovora subsp. carotovora. In addition, disease resistance activated by a fungal pathogen elicitor (xylanase from Trichoderma viride) was concomitant with eATP depletion. These results reveal several previously unknown putative molecular targets of eATP signalling, which pinpoint eATP as an important hub at which regulatory signals of some major primary metabolic pathways and defence responses are integrated.

[1]  K. Lindsey,et al.  Extracellular ATP is a regulator of pathogen defence in plants. , 2009, The Plant journal : for cell and molecular biology.

[2]  J. Davies,et al.  Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+ channels. , 2009, The Plant journal : for cell and molecular biology.

[3]  Shu-jing Wu,et al.  Extracellular ATP-induced NO production and its dependence on membrane Ca2+ flux in Salvia miltiorrhiza hairy roots , 2008, Journal of experimental botany.

[4]  A. Fernie,et al.  The Potato-Specific Apyrase Is Apoplastically Localized and Has Influence on Gene Expression, Growth, and Development1[W][OA] , 2008, Plant Physiology.

[5]  K. Lilley,et al.  Identification by 2‐D DIGE of apoplastic proteins regulated by oligogalacturonides in Arabidopsis thaliana , 2008, Proteomics.

[6]  L. Dolan,et al.  Local Positive Feedback Regulation Determines Cell Shape in Root Hair Cells , 2008, Science.

[7]  C. Casalongué,et al.  Extracellular ATP Induces Nitric Oxide Production in Tomato Cell Suspensions1 , 2007, Plant Physiology.

[8]  D. Arnold,et al.  Apyrases (Nucleoside Triphosphate-Diphosphohydrolases) Play a Key Role in Growth Control in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[9]  G. Stacey,et al.  Extracellular ATP in Plants. Visualization, Localization, and Analysis of Physiological Significance in Growth and Signaling1[W] , 2006, Plant Physiology.

[10]  B. Khakh,et al.  P2X receptors as cell-surface ATP sensors in health and disease , 2006, Nature.

[11]  K. Lindsey,et al.  Proteomic analysis of differentially expressed proteins in fungal elicitor-treated Arabidopsis cell cultures. , 2006, Journal of experimental botany.

[12]  Stephen C. Stout,et al.  Extracellular ATP Induces the Accumulation of Superoxide via NADPH Oxidases in Arabidopsis1 , 2006, Plant Physiology.

[13]  E. Bayer,et al.  Arabidopsis cell wall proteome defined using multidimensional protein identification technology , 2006, Proteomics.

[14]  T. Boller,et al.  The Arabidopsis Receptor Kinase FLS2 Binds flg22 and Determines the Specificity of Flagellin Perception[W] , 2005, The Plant Cell Online.

[15]  K. Lindsey,et al.  Extracellular ATP Functions as an Endogenous External Metabolite Regulating Plant Cell Viability , 2005, The Plant Cell Online.

[16]  J. Nasrallah.  Recognition and rejection of self in plant self-incompatibility: comparisons to animal histocompatibility. , 2005, Trends in immunology.

[17]  E. Jamet,et al.  Proteomic analysis of secreted proteins from Arabidopsis thaliana seedlings: improved recovery following removal of phenolic compounds. , 2005, Phytochemistry.

[18]  J. Davies,et al.  Is ATP a signalling agent in plants , 2005 .

[19]  Elizabeth Hénaff,et al.  Evidence of a Novel Cell Signaling Role for Extracellular Adenosine Triphosphates and Diphosphates in Arabidopsis , 2004, The Plant Cell Online.

[20]  Amal K. Dutta,et al.  Role of ATP‐conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions , 2004, The Journal of physiology.

[21]  R. Dixon,et al.  Proteomics of Medicago sativa cell walls. , 2004, Phytochemistry.

[22]  A. Avni,et al.  The Receptor for the Fungal Elicitor Ethylene-Inducing Xylanase Is a Member of a Resistance-Like Gene Family in Tomato , 2004, The Plant Cell Online.

[23]  David A Jones,et al.  Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. , 2004, Current opinion in immunology.

[24]  J. Davies,et al.  Is ATP a Signaling Agent in Plants?1 , 2003, Plant Physiology.

[25]  Jonathan D. G. Jones,et al.  Reactive oxygen species produced by NADPH oxidase regulate plant cell growth , 2003, Nature.

[26]  G. Muday,et al.  Extracellular ATP Inhibits Root Gravitropism at Concentrations That Inhibit Polar Auxin Transport1 , 2003, Plant Physiology.

[27]  T. Leff.  AMP-activated protein kinase regulates gene expression by direct phosphorylation of nuclear proteins. , 2001, Biochemical Society transactions.

[28]  Ian K Toth,et al.  Soft rot erwiniae: from genes to genomes. , 2003, Molecular plant pathology.

[29]  M. Olczak,et al.  Plant purple acid phosphatases - genes, structures and biological function. , 2003, Acta biochimica Polonica.

[30]  K. Raghothama,et al.  Purification and characterization of two secreted purple acid phosphatase isozymes from phosphate-starved tomato (Lycopersicon esculentum) cell cultures. , 2002, European journal of biochemistry.

[31]  Amal K. Dutta,et al.  Regulation of an ATP‐conductive large‐conductance anion channel and swelling‐induced ATP release by arachidonic acid , 2002, The Journal of physiology.

[32]  T. Altmann,et al.  The Subtilisin-Like Serine Protease SDD1 Mediates Cell-to-Cell Signaling during Arabidopsis Stomatal Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001016. , 2002, The Plant Cell Online.

[33]  S. Chivasa,et al.  Proteomic analysis of the Arabidopsis thaliana cell wall , 2002, Electrophoresis.

[34]  Y. Matsubayashi,et al.  An LRR Receptor Kinase Involved in Perception of a Peptide Plant Hormone, Phytosulfokine , 2002, Science.

[35]  D. Davies,et al.  The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. , 2002, Journal of experimental botany.

[36]  T. Nagata,et al.  The possible involvement of a phosphate-induced transcription factor encoded by phi-2 gene from tobacco in ABA-signaling pathways. , 2002, Plant & cell physiology.

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

[38]  Collin Thomas,et al.  A Role for Ectophosphatase in Xenobiotic Resistance , 2000, Plant Cell.

[39]  M. Sitkovsky,et al.  Ecto-protein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? , 1999, Trends in pharmacological sciences.

[40]  Singh,et al.  Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? , 1999, Trends in plant science.

[41]  H. Uchimiya,et al.  Induction of Hypersensitive Cell Death by a Fungal Protein in Cultures of Tobacco Cells , 1998 .

[42]  M. Carlson,et al.  The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? , 1998, Annual review of biochemistry.

[43]  B. Scharschmidt,et al.  Hepatocellular ATP-binding Cassette Protein Expression Enhances ATP Release and Autocrine Regulation of Cell Volume* , 1997, The Journal of Biological Chemistry.

[44]  A. Avni,et al.  High-affinity binding site for ethylene-inducing xylanase elicitor on Nicotiana tabacum membranes , 1997 .

[45]  J. Carr,et al.  Salicylic Acid Interferes with Tobacco Mosaic Virus Replication via a Novel Salicylhydroxamic Acid-Sensitive Mechanism. , 1997, The Plant cell.

[46]  A. Wojtczak,et al.  Apyrases (ATP diphosphohydrolases, EC 3.6.1.5): function and relationship to ATPases. , 1996, Biochimica et biophysica acta.

[47]  R. Arceci,et al.  The multidrug resistance (mdr1) gene product functions as an ATP channel. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[48]  R. Fluhr,et al.  Xylanase, a novel elicitor of pathogenesis-related proteins in tobacco, uses a non-ethylene pathway for induction. , 1990, Plant physiology.

[49]  J. L. Gordon.  Extracellular ATP: effects, sources and fate. , 1986, The Biochemical journal.

[50]  J. Marchalonis,et al.  Cell recognition in plants: Determinants of the stigma surface and their pollen interactions. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. Ross.  Systemic acquired resistance induced by localized virus infections in plants. , 1961, Virology.