A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling.

Systemic signaling pathways enable multicellular organisms to prepare all of their tissues and cells to an upcoming challenge that may initially only be sensed by a few local cells. They are activated in plants in response to different stimuli including mechanical injury, pathogen infection, and abiotic stresses. Key to the mobilization of systemic signals in higher plants are cell-to-cell communication events that have thus far been mostly unstudied. The recent identification of systemically propagating calcium (Ca(2+)) and reactive oxygen species (ROS) waves in plants has unraveled a new and exciting cell-to-cell communication pathway that, together with electric signals, could provide a working model demonstrating how plant cells transmit long-distance signals via cell-to-cell communication mechanisms. Here, we summarize recent findings on the ROS and Ca(2+) waves and outline a possible model for their integration.

[1]  J. Fromm,et al.  Electrical signals and their physiological significance in plants. , 2007, Plant, cell & environment.

[2]  A. Dodd,et al.  The language of calcium signaling. , 2010, Annual review of plant biology.

[3]  A. Hills,et al.  A Minimal Cysteine Motif Required to Activate the SKOR K+ Channel of Arabidopsis by the Reactive Oxygen Species H2O2* , 2010, The Journal of Biological Chemistry.

[4]  Stéphanie M. Swarbreck,et al.  Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. , 2014, The Plant journal : for cell and molecular biology.

[5]  E. Spalding,et al.  Calcium Entry Mediated by GLR3.3, an Arabidopsis Glutamate Receptor with a Broad Agonist Profile1[W][OA] , 2006, Plant Physiology.

[6]  J. Davies,et al.  Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. , 2007, The Plant journal : for cell and molecular biology.

[7]  N. Suzuki,et al.  Respiratory burst oxidases: the engines of ROS signaling. , 2011, Current opinion in plant biology.

[8]  E. Spalding,et al.  Ca2+ Conduction by an Amino Acid-Gated Ion Channel Related to Glutamate Receptors1[W] , 2012, Plant Physiology.

[9]  Takeharu Nagai,et al.  Spontaneous network activity visualized by ultrasensitive Ca2+ indicators, yellow Cameleon-Nano , 2010, Nature Methods.

[10]  A. Campbell,et al.  Calcium imaging shows differential sensitivity to cooling and communication in luminous transgenic plants. , 1996, Cell calcium.

[11]  Colin Brownlee,et al.  Spatiotemporal patterning of reactive oxygen production and Ca(2+) wave propagation in fucus rhizoid cells. , 2002, The Plant cell.

[12]  Stanisław Karpiński,et al.  Evidence for Light Wavelength-Specific Photoelectrophysiological Signaling and Memory of Excess Light Episodes in Arabidopsis[W][OA] , 2010, Plant Cell.

[13]  K. Vandepoele,et al.  ROS signaling: the new wave? , 2011, Trends in plant science.

[14]  W. Schulze,et al.  Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation , 2013, Proceedings of the National Academy of Sciences.

[15]  Ryo Ikeda,et al.  Merkel Cells Transduce and Encode Tactile Stimuli to Drive Aβ-Afferent Impulses , 2014, Cell.

[16]  S. Karpiński,et al.  Light acclimation, retrograde signalling, cell death and immune defences in plants. , 2013, Plant, cell & environment.

[17]  S. Spoel,et al.  How do plants achieve immunity? Defence without specialized immune cells , 2012, Nature Reviews Immunology.

[18]  H. Kaya,et al.  Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. , 2012, Biochimica et biophysica acta.

[19]  J. Feijó,et al.  Glutamate Receptor–Like Genes Form Ca2+ Channels in Pollen Tubes and Are Regulated by Pistil d-Serine , 2011, Science.

[20]  M. Zimmerman,et al.  Mitochondria in Cardiovascular Physiology and Disease Mitochondrial-localized NADPH oxidase 4 is a source of superoxide in angiotensin II-stimulated neurons , 2013 .

[21]  R. Hedrich,et al.  TPC1-SV channels gain shape. , 2011, Molecular plant.

[22]  Todd E. Woerner,et al.  Coupling Diurnal Cytosolic Ca2+ Oscillations to the CAS-IP3 Pathway in Arabidopsis , 2007, Science.

[23]  Simon Gilroy,et al.  Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants , 2014, Proceedings of the National Academy of Sciences.

[24]  M. Tester,et al.  Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells , 2003, Journal of Cell Science.

[25]  N. Suzuki,et al.  Temporal-Spatial Interaction between Reactive Oxygen Species and Abscisic Acid Regulates Rapid Systemic Acclimation in Plants[W][OPEN] , 2013, Plant Cell.

[26]  J. Shah,et al.  Long-distance communication and signal amplification in systemic acquired resistance , 2013, Front. Plant Sci..

[27]  J. Downie,et al.  Analysis of calcium spiking using a cameleon calcium sensor reveals that nodulation gene expression is regulated by calcium spike number and the developmental status of the cell. , 2006, The Plant journal : for cell and molecular biology.

[28]  S. Roy,et al.  Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling , 2012, Proceedings of the National Academy of Sciences.

[29]  J. Dangl,et al.  The Plant NADPH Oxidase RBOHD Mediates Rapid Systemic Signaling in Response to Diverse Stimuli , 2009, Science Signaling.

[30]  H. Yoshioka,et al.  Regulation of Rice NADPH Oxidase by Binding of Rac GTPase to Its N-Terminal Extension[W][OA] , 2007, The Plant Cell Online.

[31]  E. Farmer,et al.  GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling , 2013, Nature.

[32]  P. De Koninck,et al.  Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. , 1998, Science.

[33]  G. Stacey,et al.  Identification of a Plant Receptor for Extracellular ATP , 2014, Science.

[34]  S. Shabala,et al.  SV channels dominate the vacuolar Ca2+ release during intracellular signaling , 2009, FEBS letters.

[35]  J. Ward,et al.  Calcium-Activated K+ Channels and Calcium-Induced Calcium Release by Slow Vacuolar Ion Channels in Guard Cell Vacuoles Implicated in the Control of Stomatal Closure. , 1994, The Plant cell.

[36]  R. Mittler,et al.  Reactive oxygen gene network of plants. , 2004, Trends in plant science.

[37]  Kenji Hashimoto,et al.  The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. , 2013, Molecular plant.

[38]  M. Fricker,et al.  Sieve Element Ca2+ Channels as Relay Stations between Remote Stimuli and Sieve Tube Occlusion in Vicia faba[W] , 2009, The Plant Cell Online.

[39]  J. Schroeder,et al.  Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. , 2010, Annual review of plant biology.

[40]  S. Rudaz,et al.  Velocity Estimates for Signal Propagation Leading to Systemic Jasmonic Acid Accumulation in Wounded Arabidopsis* , 2009, The Journal of Biological Chemistry.

[41]  D. Gutterman,et al.  ROS-induced ROS release in vascular biology: redox-redox signaling. , 2011, American journal of physiology. Heart and circulatory physiology.

[42]  Zhen-Ming Pei,et al.  Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells , 2000, Nature.

[43]  R Y Tsien,et al.  Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. , 2000, Science.

[44]  D. Klessig,et al.  SOS - too many signals for systemic acquired resistance? , 2012, Trends in plant science.

[45]  Xiaoli Gao,et al.  A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

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

[47]  J. Lambeth,et al.  Nox enzymes from fungus to fly to fish and what they tell us about Nox function in mammals. , 2010, Free radical biology & medicine.

[48]  N. Saunders,et al.  Transcriptomic Analysis Reveals Calcium Regulation of Specific Promoter Motifs in Arabidopsis[W] , 2011, Plant Cell.