Novel roles for phospholipase C in plant stress signalling and development

Phospholipase C (PLC) is best known for its role in generating second messengers by hydrolysis of phosphatidylinositol 4,5-bisphosphate (PIP 2 ) in mammalian cells. In plants however, PLC’s role is less clear as plants lack the prime targets for both inositol 1,4,5-trisphosphate (i.e. a ligand-gated Ca 2+ channel) and diacylglycerol (i.e. protein kinase C and TRP-type ion channels). The genome of Arabidopsis thaliana encodes for 9 PLC genes. Here, we analyzed the role of PLC3 . Promoter-GUS analyses revealed that PLC3 is specifically expressed in the vascular tissue (most likely phloem) of roots, leaves and flowers, but also in guard cells and at the base of trichomes. Knock-out mutants of PLC3 were found to be affected in seed germination, root development and stomatal closure. Using in vivo 32 P i -lipid labeling analyses, we found that ABA stimulated the formation of PIP 2 in wild type germinating seeds, seedlings and guard cell-enriched leaf peels, but not in plc3 mutants. The latter displayed decreased sensitivity to ABA during seed-germination inhibition and ABA induced-stomatal closure. Overexpression of PLC3 enhanced drought tolerance and decreased stomatal aperture. Together, our results uncovered novel roles for PLC3 in ABA signaling and plant development.

[1]  R. Wijk,et al.  Arabidopsis phosphatidylinositol-phospholipase C2 (PLC2) is required for female gametogenesis and embryo development , 2016, Planta.

[2]  M. Joosten,et al.  Silencing of the tomato phosphatidylinositol-phospholipase C2 (SlPLC2) reduces plant susceptibility to Botrytis cinerea. , 2016, Molecular plant pathology.

[3]  T. Jegla,et al.  Guard cell sensory systems: recent insights on stomatal responses to light, abscisic acid, and CO2. , 2016, Current opinion in plant biology.

[4]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[5]  R. Tenhaken,et al.  Raffinose Family Oligosaccharides Act As Galactose Stores in Seeds and Are Required for Rapid Germination of Arabidopsis in the Dark , 2016, Front. Plant Sci..

[6]  I. Heilmann.  Phosphoinositide signaling in plant development , 2016, Development.

[7]  N. Zheng,et al.  Inositol Polyphosphate Binding Specificity of the Jasmonate Receptor Complex1[OPEN] , 2016, Plant Physiology.

[8]  D. Bartels,et al.  Lipid signalling in plant responses to abiotic stress. , 2016, Plant, cell & environment.

[9]  Xavier Zarza,et al.  Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. , 2016, Plant, cell & environment.

[10]  J. Schroeder,et al.  Mechanisms of abscisic acid-mediated control of stomatal aperture. , 2015, Current opinion in plant biology.

[11]  Yuqing He,et al.  Arabidopsis PLC2 is involved in auxin-modulated reproductive development. , 2015, The Plant journal : for cell and molecular biology.

[12]  S. Sengupta,et al.  Significance of galactinol and raffinose family oligosaccharide synthesis in plants , 2015, Front. Plant Sci..

[13]  C. Hardtke,et al.  Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching , 2015, Development.

[14]  A. Saiardi,et al.  VIH2 Regulates the Synthesis of Inositol Pyrophosphate InsP8 and Jasmonate-Dependent Defenses in Arabidopsis[OPEN] , 2015, Plant Cell.

[15]  J. Bailey-Serres,et al.  Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability , 2015, Nature Reviews Genetics.

[16]  Bing Li,et al.  Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. , 2014, Plant & cell physiology.

[17]  Imara Y. Perera,et al.  Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants. , 2014, The Plant journal : for cell and molecular biology.

[18]  H. Hilhorst,et al.  Physiological and biochemical responses of Ricinus communis seedlings to different temperatures: a metabolomics approach , 2014, BMC Plant Biology.

[19]  J. Vossen,et al.  The tomato phosphatidylinositol-phospholipase C2 (SlPLC2) is required for defense gene induction by the fungal elicitor xylanase. , 2014, Journal of plant physiology.

[20]  C. Bock,et al.  Metabolomic shifts in Brassica napus lines with enhanced BnPLC2 expression impact their response to low temperature stress and plant pathogens. , 2014, GM crops & food.

[21]  Wim Van den Ende.  Multifunctional fructans and raffinose family oligosaccharides , 2013, Front. Plant Sci..

[22]  T. Balla,et al.  Phosphoinositides: tiny lipids with giant impact on cell regulation. , 2013, Physiological reviews.

[23]  B. Han,et al.  Systematic validation of candidate reference genes for qRT-PCR normalization under iron deficiency in Arabidopsis , 2013, BioMetals.

[24]  K. Yamaguchi-Shinozaki,et al.  ABA signaling in stress-response and seed development , 2013, Plant Cell Reports.

[25]  K. Shinozaki,et al.  Osmotic Stress Responses and Plant Growth Controlled by Potassium Transporters in Arabidopsis[C][W] , 2013, Plant Cell.

[26]  Jian-Kang Zhu,et al.  Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase , 2013, Front. Plant Sci..

[27]  Yuwei Luo,et al.  Effect of several germination treatments on phosphatases activities and degradation of phytate in faba bean (Vicia faba L.) and azuki bean (Vigna angularis L.). , 2012, Journal of food science.

[28]  C. García-Mata,et al.  Phospholipase Dδ is involved in nitric oxide-induced stomatal closure , 2012, Planta.

[29]  C. García-Mata,et al.  Phospholipase Dδ is involved in nitric oxide-induced stomatal closure , 2012, Planta.

[30]  A. Glatz,et al.  Heat shock response in photosynthetic organisms: membrane and lipid connections. , 2012, Progress in lipid research.

[31]  Hui Liao,et al.  A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis[W][OA] , 2012, Plant Cell.

[32]  R. Hedrich,et al.  Anion channels: master switches of stress responses. , 2012, Trends in plant science.

[33]  M. Goswami,et al.  Characterization and Functional Validation of Tobacco PLC Delta for Abiotic Stress Tolerance , 2012, Plant Molecular Biology Reporter.

[34]  Shuzhi Zheng,et al.  Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. , 2012, The Plant journal : for cell and molecular biology.

[35]  M. J. Chalmers,et al.  Molecular Mimicry Regulates ABA Signaling by SnRK2 Kinases and PP2C Phosphatases , 2012, Science.

[36]  M. Bucholc,et al.  SnRK2 protein kinases--key regulators of plant response to abiotic stresses. , 2011, Omics : a journal of integrative biology.

[37]  G. Gillaspy.  The cellular language of myo-inositol signaling. , 2011, The New phytologist.

[38]  R. Valluru,et al.  Myo-inositol and beyond--emerging networks under stress. , 2011, Plant science : an international journal of experimental plant biology.

[39]  T. Munnik,et al.  Green light for polyphosphoinositide signals in plants. , 2011, Current opinion in plant biology.

[40]  E. Benková,et al.  Inositol trisphosphate-induced Ca2+ signaling modulates auxin transport and PIN polarity. , 2011, Developmental cell.

[41]  L. Lamattina,et al.  Mechanisms of xylanase-induced nitric oxide and phosphatidic acid production in tomato cells , 2011, Planta.

[42]  A. ten Have,et al.  Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. , 2011, Journal of plant physiology.

[43]  E. Benková,et al.  Lateral root organogenesis - from cell to organ. , 2010, Current opinion in plant biology.

[44]  Imara Y. Perera,et al.  Basal Signaling Regulates Plant Growth and Development1 , 2010, Plant Physiology.

[45]  S. Cutler,et al.  Abscisic acid: emergence of a core signaling network. , 2010, Annual review of plant biology.

[46]  T. Munnik,et al.  Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. , 2010, Plant, cell & environment.

[47]  Y. Kamiya,et al.  Abscisic acid and the control of seed dormancy and germination , 2010, Seed Science Research.

[48]  T. Umezawa,et al.  The PP2C–SnRK2 complex , 2010, Plant signaling & behavior.

[49]  Yuling Bai,et al.  Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. , 2010, The Plant journal : for cell and molecular biology.

[50]  Kenichi Hitomi,et al.  Structural Mechanism of Abscisic Acid Binding and Signaling by Dimeric PYR1 , 2009, Science.

[51]  Y. Fujita,et al.  Structural basis of abscisic acid signalling , 2009, Nature.

[52]  S. Cutler,et al.  A Gate-Latch-Lock Mechanism for Hormone Signaling by Abscisic Acid Receptors , 2009, Nature.

[53]  W. Keller,et al.  Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. , 2009, Plant, cell & environment.

[54]  Chuangye Yan,et al.  Structural insights into the mechanism of abscisic acid signaling by PYL proteins , 2009, Nature Structural &Molecular Biology.

[55]  S. Cutler,et al.  Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. , 2009, The Plant journal : for cell and molecular biology.

[56]  T. Munnik,et al.  Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. , 2009, The Plant journal : for cell and molecular biology.

[57]  B. Péret,et al.  Lateral root emergence: a difficult birth. , 2009, Journal of experimental botany.

[58]  T. Munnik,et al.  Plant PA signaling via diacylglycerol kinase. , 2009, Biochimica et biophysica acta.

[59]  S. Shears.  Diphosphoinositol Polyphosphates: Metabolic Messengers? , 2009, Molecular Pharmacology.

[60]  Tom Beeckman,et al.  Arabidopsis lateral root development: an emerging story. , 2009, Trends in plant science.

[61]  A. Saiardi,et al.  Are inositol pyrophosphates signalling molecules? , 2009, Journal of cellular physiology.

[62]  J. Schroeder,et al.  Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K channels in Arabidopsis guard cells. , 2009, The Plant journal : for cell and molecular biology.

[63]  P. McCourt,et al.  Abscisic Acid Inhibits Type 2C Protein Phosphatases via the PYR/PYL Family of START Proteins , 2009, Science.

[64]  E. Grill,et al.  Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors , 2009, Science.

[65]  T. Munnik,et al.  Phospholipid Signaling Responses in Salt-Stressed Rice Leaves , 2009, Plant & cell physiology.

[66]  T. Munnik,et al.  Plant phospholipid signaling: “in a nutshell” The authors gratefully acknowledge financial support from the Netherlands Organization for Scientific Research (VIDI 864.05.001, VIDI 700.56.429, and ECHO 700.56.007) and the European Union (COST FA0605). Published, JLR Papers in Press, December 20, 2008 , 2009, Journal of Lipid Research.

[67]  Pascal Mäser,et al.  Plant ion channels: gene families, physiology, and functional genomics analyses. , 2009, Annual review of physiology.

[68]  G. Gillaspy,et al.  Inositol phosphate signaling and gibberellic acid , 2009, Plant signaling & behavior.

[69]  Juren Zhang,et al.  Cloning and expression analysis of some genes involved in the phosphoinositide and phospholipid signaling pathways from maize (Zea mays L.). , 2008, Gene.

[70]  Klaus Palme,et al.  Mechanical induction of lateral root initiation in Arabidopsis thaliana , 2008, Proceedings of the National Academy of Sciences.

[71]  Zhen-qi Zhou,et al.  TfPLC1, a gene encoding phosphoinositide-specific phospholipase C, is predominantly expressed in reproductive organs in Torenia fournieri , 2008, Sexual Plant Reproduction.

[72]  C. Brownlee,et al.  Ca2+ signalling in plants and green algae--changing channels. , 2008, Trends in plant science.

[73]  V. Brendel,et al.  Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. , 2008, Plant physiology and biochemistry : PPB.

[74]  Robert H. Michell,et al.  Inositol derivatives: evolution and functions , 2008, Nature Reviews Molecular Cell Biology.

[75]  Q. Gao,et al.  Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize , 2008, Planta.

[76]  Byeong Wook Jeon,et al.  Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening. , 2007, The Plant journal : for cell and molecular biology.

[77]  T. Gadella,et al.  Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. , 2007, The Plant journal : for cell and molecular biology.

[78]  Michal Sharon,et al.  Mechanism of auxin perception by the TIR1 ubiquitin ligase , 2007, Nature.

[79]  B. Kost,et al.  Pollen Tube Tip Growth Depends on Plasma Membrane Polarization Mediated by Tobacco PLC3 Activity and Endocytic Membrane Recycling[W] , 2006, The Plant Cell Online.

[80]  Weidong Huang,et al.  Novel interrelationship between salicylic acid, abscisic acid, and PIP2-specific phospholipase C in heat acclimation-induced thermotolerance in pea leaves. , 2006, Journal of experimental botany.

[81]  T. Gadella,et al.  Visualization of PtdIns3P dynamics in living plant cells. , 2006, The Plant journal : for cell and molecular biology.

[82]  J. York.  Regulation of nuclear processes by inositol polyphosphates. , 2006, Biochimica et biophysica acta.

[83]  R. Irvine.  Nuclear inositide signalling -- expansion, structures and clarification. , 2006, Biochimica et biophysica acta.

[84]  S. Gilroy,et al.  Petunia Phospholipase C1 Is Involved in Pollen Tube Growth[W] , 2006, The Plant Cell Online.

[85]  Weidong Huang,et al.  Contributions of PIP(2)-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. , 2006, Journal of plant physiology.

[86]  Imara Y. Perera,et al.  A Universal Role for Inositol 1,4,5-Trisphosphate-Mediated Signaling in Plant Gravitropism1[W] , 2005, Plant Physiology.

[87]  J. York,et al.  Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[88]  T. Munnik,et al.  Phosphatidic acid: a multifunctional stress signaling lipid in plants. , 2005, Trends in plant science.

[89]  Ottoline Leyser,et al.  The Arabidopsis F-box protein TIR1 is an auxin receptor , 2005, Nature.

[90]  W. Keller,et al.  Cloning of Brassica napus phospholipase C2 (BnPLC2), phosphatidylinositol 3-kinase (BnVPS34) and phosphatidylinositol synthase1 (BnPtdIns S1)—comparative analysis of the effect of abiotic stresses on the expression of phosphatidylinositol signal transduction-related genes in B. napus , 2005, Planta.

[91]  K. Mikami,et al.  Phosphoinositide-specific phospholipase C is involved in cytokinin and gravity responses in the moss Physcomitrella patens. , 2004, The Plant journal : for cell and molecular biology.

[92]  T. Munnik,et al.  Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. , 2004, The Plant journal : for cell and molecular biology.

[93]  J. Lee,et al.  Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. , 2004, The New phytologist.

[94]  H. Xue,et al.  DNA chip-based expression profile analysis indicates involvement of the phosphatidylinositol signaling pathway in multiple plant responses to hormone and abiotic treatments , 2004, Cell Research.

[95]  T. Munnik,et al.  Osmotically Induced Cell Swelling versus Cell Shrinking Elicits Specific Changes in Phospholipid Signals in Tobacco Pollen Tubes1 , 2004, Plant Physiology.

[96]  T. Munnik,et al.  Phospholipid-based signaling in plants. , 2003, Annual review of plant biology.

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

[98]  A. Hetherington,et al.  The effects of manipulating phospholipase C on guard cell ABA-signalling. , 2003, Journal of experimental botany.

[99]  G. Racagni,et al.  Gibberellin signal in barley aleurone: early activation of PLC by G protein mediates amylase secretion , 2003, Plant Growth Regulation.

[100]  A. Webb,et al.  Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[101]  K. Døving,et al.  Photolysis of caged inositol 1,4,5-trisphosphate induces action potentials in frog vomeronasal microvillar receptor neurones , 2003, Neuroscience.

[102]  T. Munnik,et al.  Nod Factor and Elicitors Activate Different Phospholipid Signaling Pathways in Suspension-Cultured Alfalfa Cells1 , 2003, Plant Physiology.

[103]  B. Mueller‐Roeber,et al.  Phospholipase C is required for the control of stomatal aperture by ABA. , 2003, The Plant journal : for cell and molecular biology.

[104]  C. Cantrel,et al.  Activation of Phospholipases C and D Is an Early Response to a Cold Exposure in Arabidopsis Suspension Cells1 , 2002, Plant Physiology.

[105]  B. Mueller‐Roeber,et al.  Inositol Phospholipid Metabolism in Arabidopsis. Characterized and Putative Isoforms of Inositol Phospholipid Kinase and Phosphoinositide-Specific Phospholipase C1 , 2002, Plant Physiology.

[106]  Teun Munnik,et al.  Phospholipid signalling in plant defence. , 2002, Current opinion in plant biology.

[107]  M. Otegui,et al.  Developing Seeds of Arabidopsis Store Different Minerals in Two Types of Vacuoles and in the Endoplasmic Reticulum Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010486. , 2002, The Plant Cell Online.

[108]  J. Gray,et al.  ABA signalling: A messenger's FIERY fate , 2001, Current Biology.

[109]  R. Hedrich,et al.  The role of ion channels in light-dependent stomatal opening. , 2001, Journal of experimental botany.

[110]  T. Martin.  PI(4,5)P(2) regulation of surface membrane traffic. , 2001, Current opinion in cell biology.

[111]  T. Munnik,et al.  Osmotic stress activates distinct lipid and MAPK signalling pathways in plants , 2001, FEBS letters.

[112]  Joseph C. Shope,et al.  Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed arabidopsis. , 2001, Plant physiology.

[113]  N. Chua,et al.  Arabidopsis PLC1 Is Required for Secondary Responses to Abscisic Acid Signals , 2001, Plant Cell.

[114]  T. Munnik.  Phosphatidic acid: an emerging plant lipid second messenger. , 2001, Trends in plant science.

[115]  K. Yamaguchi-Shinozaki,et al.  Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture. , 2001, Plant & cell physiology.

[116]  Susan Flores,et al.  Abscisic acid-induced changes in inositol metabolism in Spirodela polyrrhiza , 2000, Planta.

[117]  T. Boller,et al.  Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. , 2000, Plant physiology.

[118]  C. Brearley,et al.  Inositol hexakisphosphate is a physiological signal regulating the K+-inward rectifying conductance in guard cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[119]  Imara Y. Perera,et al.  Inositol signaling and plant growth , 2000, Trends in plant science.

[120]  M. Kashem,et al.  Possible involvement of phosphoinositide-Ca2+ signaling in the regulation of alpha-amylase expression and germination of rice seed (Oryza sativa L.). , 2000, Plant & cell physiology.

[121]  C. Larsson,et al.  Salinity and Hyperosmotic Stress Induce Rapid Increases in Phosphatidylinositol 4,5-Bisphosphate, Diacylglycerol Pyrophosphate, and Phosphatidylcholine in Arabidopsis thaliana Cells* , 1999, The Journal of Biological Chemistry.

[122]  Imara Y. Perera,et al.  Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[123]  A. Hetherington,et al.  Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[124]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[125]  T. Munnik,et al.  Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipases C and D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan , 1998, Planta.

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

[127]  M. Chang,et al.  Cloning of a Ca(2+)-ATPase gene and the role of cytosolic Ca2+ in the gibberellin-dependent signaling pathway in aleurone cells. , 1997, The Plant journal : for cell and molecular biology.

[128]  S. Assmann,et al.  Abscisic Acid-Induced Phosphoinositide Turnover in Guard Cell Protoplasts of Vicia faba , 1996, Plant physiology.

[129]  K. Shinozaki,et al.  A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[130]  D. Sanders,et al.  Osmotic stress enhances the competence of Beta vulgaris vacuoles to respond to inositol 1,4,5‐trisphosphate , 1994 .

[131]  T. Munnik,et al.  Rapid turnover of polyphosphoinositides in carnation flower petals , 1994, Planta.

[132]  W. Boss,et al.  Changes in Phosphatidylinositol Metabolism in Response to Hyperosmotic Stress in Daucus carota L. Cells Grown in Suspension Culture , 1993, Plant physiology.

[133]  A. Trewavas,et al.  Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure , 1990, Nature.

[134]  M. Blatt,et al.  Reversible inactivation of K+ channels of Vcia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate , 1990, Nature.

[135]  P. P. Murthy,et al.  Phosphoinositides in barley aleurone layers and gibberellic Acid-induced changes in metabolism. , 1989, Plant physiology.

[136]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[137]  T. Munnik.  PI-PLC: Phosphoinositide-Phospholipase C in Plant Signaling , 2014 .

[138]  E. Ruelland,et al.  Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme. , 2014, Biochimie.

[139]  Xavier Zarza,et al.  Analyzing plant signaling phospholipids through 32Pi-labeling and TLC. , 2013, Methods in molecular biology.

[140]  G. Gillaspy.  The role of phosphoinositides and inositol phosphates in plant cell signaling. , 2013, Advances in experimental medicine and biology.

[141]  T. Munnik,et al.  Measuring PLD activity in vivo. , 2013, Methods in molecular biology.

[142]  J. Goedhart,et al.  Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. , 2009, The Plant journal : for cell and molecular biology.

[143]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[144]  M. Blatt.  Cellular signaling and volume control in stomatal movements in plants. , 2000, Annual review of cell and developmental biology.