dhr. dr. T. (Teun) Munnik
Faculteit der Natuurwetenschappen, Wiskunde en Informatica
Science Park A
Science Park 904 Amsterdam
1090 GE Amsterdam
Phospholipid Signalling in Plant Stress & Development
Plants cannot run away! Instead, over millions of years of evolution, they have 'developed' smart strategies to quickly respond and adapt to sudden environmental changes. The ' stress ' plants usually encounters can be divided into biotic- (i.e. pathogens, herbivores) and abiotic stress (i.e. cold, heat, salinity oxidative stress, drought). Our main focus is to study the role phospholipid signals play in response to temperature- (cold, heat) and water stress (drought, salinity and hypoosmotic stress), and during plant-pathogen interactions (see below).
My lab is interested in the role of phospholipids in Plant Cell Signalling and Development. Especially, phosphatidic acid (PA), DGPP and polyphosphoinositides, like PtdInsP and PtdInsP2, have our interest. These molecules are present at very low concentrations in cellular membranes and rountinely missed by HPLC and MS analyses, simply because structural lipids, such as PC, PE, PI and PG, make up the mass of the membrane. Nonetheless, these minor signalling lipids can easily be picked up by 32P-labelling (see TECHNIQUES), because their turnover is much faster than structural phospholipids and because they are directly labelled by ATP via specific lipid kinases. The key players involved in their metabolism are depicted in a 'simple' cartoon. In short, this involves the so-called PLC-and PLD signalling cascades. They both generate PA but this occurs, very likely, at different locations and has different functions.
32P-labelling and TLC
Phospholipids are routinely labelled in
vivo using 32P-orthophosphate. In general, cells-, seedlings- or
leaf discs are used and labelling times vary from min to hrs or even O/N,
depending on the type of experiment (e.g. turnover, mass levels). To monitor
PLD, transphosphatidylation assays can be conducted using primary
alcohols (see list 'All Publications' 9, 18). Shown is an example using the
green alga Chlamydomonas. Cells were labelled for 4 hrs and then
stimulated for 5 min in the presence of a low concentration of alcohol that the
cells don't mind. Lipids were then extracted and chromatographed using an
Ethylacetate TLC system that separates phosphatidylalcohols from other
phospholipids (panel a). Autoradiography visualises their positions
while PhosphoImaging is used to quantify the individual spots. In this
way, in vivo activation of PLD with mastoparan was shown, resulting in
increased phosphatidylalcohol spots.
Using a similar protocol for time-course experiments, the timing and duration of PLD stimulation can be established. However, samples can also be used to visualise the sequential activities of PLC, DAG kinase and PA kinase. The lipids are now chromatographed in an Alkaline TLC system that separates most phospholipids (panel b). Note the dramatic hydrolysis of PtdInsP2 within 15 sec to produce DAG that is immediately converted to PA by DAG kinase. PI- and PIP-kinase activities also increase to maintain PtdInsP2 levels. Since PLC is down regulated before these lipid kinases are, radioactive PtdInsP and PtdInsP2 are transiently over-produced. In the same time frame, the PA signal is attenuated by PA kinase producing DGPP. Figure is adapted from Ref. 27
Distinguishing between DGK- and PLD-generated PA: the 'differential labelling' protocol
Chlamydomonas cells were metabolically prelabelled with 32P-orthophosphate for the times indicated and subsequently treated for 1 min with either buffer (control; panel A, B) or 1 µM mastoparan (stimulated; panel C, D), both in the presence of 0.1 % n-butanol. Lipids were then extracted, split into half, and either seperated on EtAc TLC (A, C), to separate the PLD-catalyzed phosphatidylbutanol (PBut), or Alkaline TLC (B, D), to visualize the rest of the phospholipids, including PA and its phosphorylated product, diacylglycerolpyrophosphate (DGPP). The point is that all cells are treated for the same time period (1 min) but that the PBut will only be radioactive when its substrate (i.e. PE) becomes labelled (>40min). The same holds of course for the PA that would be coming through the PLD pathway. In contrast, when PA is generated via DGK, then the label comes from ATP and since this is labelled within seconds, a massive radioactive PA response can be witnessed if a DGK was involved. Since PA kinase also uses ATP, a similar response in DGPP can be picked up(panel D). Since the specific radioactivity of 32P-ATP decreases in time, the 1-min response decreases concomitantly. The combined assay is a relative measure and evidence for PA coming through a DGK and/or PLD pathway. See details in Arisz et al. , 2009 (Ref 68).
Visualizing Lipid Signalling using Lipid Biosensors
Using GFP fusions of various lipid-binding domains and expressing them stably in tobacco BY-2 cells and Arabidopsis seedlings, we have been able to topographically visualize where certain lipids are localised, and where they are generated. Currently, we have biosensors for PtdIns3P (ref 28), PtdIns4P (ref 62), PtdIns(4,5)P2 (ref 55) and DAG (in prep). We are working on PA sensors.
Arabidopsis T-DNA insertion mutants
Using T-DNA insertion mutants, we are trying to provide further evidence for the participation of PLC, PLD and DGK in signalling- and developmental pathways. In Arabidopsis , there are 9 PLC, 12 PLD and 7 DGK genes. In addition, there are 11 PIP5K, 12 PI4K, 1 PI3K and multiple PA- and PPI phosphatase genes.
Below, an example of reduced salt tolerance in Arabidopsis pld mutants is shown. Seeds from wild-type (Col-0, black circles), pldα1 (open squares), pldδ (open triangles) or pldα1/pldδ double (open diamonds) knock-out mutant lines were sown on agar plates and grown vertically in a growth chamber. After 3 days seedlings were transferred to fresh plates supplemented with 0, 75 or 150 mM NaCl. Plates were scanned after 8 days (a) and primary root growth was followed and averaged ± SE during 4 days after transfer (b; n=12-16; a representative experiment is presented).
PLANT STRESS AND DEVELOPMENT
Role of Phospholipids in Membrane Trafficking
Heat stress induces an array of physiological adjustments that facilitate continued homeostasis and survival during periods of elevated temperatures. Recently, we found that within minutes of a sudden temperature increase, plants deploy specific phospholipid-based signalling pathways to specific intracellular locations: a PLD and a phosphatidylinositolphosphate kinase (PIPK) are activated, and PA and PIP2 rapidly accumulate. Using our PIP2-specific lipid biosensor, we could show that the heat-induced PIP2 is localized to the plasma membrane, the nuclear envelope, nucleolus and punctate cytoplasmic structures ( see pict below). Increases in the steady-state levels of PA and PIP2 occured within several min of temperature increases from ambient levels of 20-25°C to 35°C and above. Similar patterns were observed in heat stressed Arabidopsis seedlings and rice leaves. The PA which accumulates in response to heat stress results in large part from the activation of PLD rather than the sequential action of PLC and DGK. 32P-Pulse-labelling analysis reveals that the PIP2 response is due to the activation of a PIPK rather than the inhibition of a lipase or PIP2 phosphatase (see ref 64, 69).
Osmotic stress involves salinity, drought but also hypotonic stress . We are investigating which of the phospholipid signalling pathways are activated and where. Using 32P-labelling, specific PA and PPI responses have been uncovered (18, 21, 26, 29, 30, 40, 55). For the latter, different isomers are involved, which can be analyzed by HPLC analysis using a strong anion-exchange column after deacylation of the PPIs, generating so-called GroPIns' (see HPLC profile).
At the moment, we are using lipid biosensor lines to find out where these lipid signals are generated, (55) and T-DNA insertion mutants to pinpoint the genes involved (63; In prep).
PLC and PLD signalling cascades can individually generate PA, an important eukaryotic lipid second messenger. PLC generates it indirectly, via the hydrolysis of PI(4,5)P2 and the subsequent phosphorylation ofdiacylglycerol (DAG) intoPA via DAG kinase (DGK). PLD generates PA directly by hydrolyzing structural pospholipids such as phosphatidylcholine. Earlier, we have provided evidence for the role of PA in plant defence using elicitor-challenged cell suspensions of tomato, parsley and alfalfa. Currently, we are adressing PA's role in the model system Arabidopsis thaliana .
Arabidopsis contains 9 PLCs, 7 DGKs and 12 PLDs. To identify the genes involved in plant defence and to characterise their individual functions, T-DNA insertion lines for most of these genes were collected. Plants were then analysed for their disease resistance and sensitivity using virulent and avirulent strains of the bacterial pathogen, Pseudomonas syringae and its natural pathogen Hyaloperonospora parasitica , the causal agent of downy mildew. A DGK gene was found to be required for full resistance against virulentPseudomonas and H. parasitica while two PLD genes were found to be involved in resistance againstavirulent Pseudomonas strains. .
Pollen Tube Growth
Work from Dr. Laura Zonia is focussing on one of the fastest growing cellsofthis planet, tobacco pollentubes. The goal of this research is to identify key information cascades that control pollen tubegrowth, and to understand how these networkslink to the biomechanics driving cell elongation. We have identified several key cascades, including actin cytoskeleton, ion fluxes and phospholipid signals. Other workers have identified other cascades important for pollen tube growth, including GTPases, protein kinases, and processes involved in cell wall synthesis. When we searched for common themes across these information cascades, osmoregulation and cell volume status emerged as a key component. Further work indicated that indeed many of these networks converge with processes involved in cellular osmoregulation. Our most recent work shows that transcellular hydrodynamic flux drives pollen tube growth and modulates the rates of exocytosis and endocytosis
Time-lapse images of tobacco pollen tubes double-labelled with FM 1-43 (green) and FM 4-64 (red) to identify sites of endocytosis and exocytosis and visualize membrane trafficking patterns. The first 3 images are from a pollen tube undergoing normal growth. The next 3 images are from a pollen tube undergoing hypertonic stress, which stimulates endocytic membrane retrieval at the apex and inhibits exocytosis. The last 2 images are from a pollen tube undergoing hypotonic stress, which stimulates exocytosis and growth and attenuates endocytosis. Together with previous work (Zonia and Munnik, 2007), these data reveal that transcellular hydrodynamic flux is a key integrator ofpollen tube growth, providing a motive force for cell elongation and regulating the rates of membrane insertion( exocytosis ) and retrieval (endocytosis). see refs 40, 49, 51, 53,57,60, 66)
Diacylglycerol Kinase (DGK)
Accumulating evidence suggests that PA plays a pivotal role in the plant's response to environmental signals. Besides PLD activity, PA can also be generated by DGK. To establish which metabolic route is activated, a differential 32P-radiolabelling protocol can be used ( see above). Based on this, and more recently on reverse-genetic approaches, DGK has taken center stage, next to PLD, as a generator of PA in biotic and abiotic stress responses. The DAG substrate is generally thought to be derived from PI-PLC activity. The model plant system Arabidopsis thaliana has 7 DGK isozymes, two of which, AtDGK1 and AtDGK2, resemble mammalian DGKε, containing a conserved kinase domain, a transmembrane domain and two C1 domains. The other DGKs have a much simpler structure, lacking the C1 domains, not matched in animals. Several protein targets have now been discovered that bind PA (Testerink and Munnik, 2011). Whether the PA molecules engaged in these interactions come from PLD or DGK remains to be elucidated.
Phospholipase D (PLD)
In comparison to mammals (which possess only two PLD genes) or yeast (one), plants possess a multitudinous and varied family of PLD genes. The genome of Arabidopsis thaliana contains twelve PLD family members and this diversity has been found in assorted higher plant species. PLD enzymes in eukaryotes are characterized by two highly conserved carboxy-terminal (C-terminal) catalytic domains and an amino-terminal (N-terminal) lipid-binding region (Figure). The two catalytic HxKxxxxD (HKD) motifs interact and are essential for the lipase activity of rat PLD1.
The plant PLD family can be divided into two sub-families, based on their N-terminal lipid-binding domains (see below). In Arabidopsis, two of the 12 PLDs contain a Phox homology- (PX) a pleckstrin homology (PH) domain, whereas the remaining 10 PLDs contain a C2 domain. PX and PH domains have been shown to mediate protein-membrane targeting and are closely linked to PPI signaling. C2 domains also mediate the localization of soluble proteins to membranes by binding lipids in a Ca2+-dependent manner. Importantly, PX, PH and C2 domains have also been implicated in protein-protein interactions. The plant-PLD family can be subdivided further into six classes, on the basis of sequence homology and in vitro enzymatic activity. The Arabidopsis genome contains three α-, two β-, three γ-, one δ-, one ε- and two ζ-class PLD isoforms; the latter class contains the PX and PH domains and shares more homology with yeast and mammalian PLDs than with other plant PLD classes.
Phospholipase C (PLC)
PI-PLCs have been classified into six different subfamilies, i.e. β, γ, δ, ε, η and ζ, based on their domain structure and organization, (Figure; Munnik & Testerink, 2009). Mammalian cells contain all six isoforms (13 in total), whereas plants only exhibit one, i.e PLCζ, the class that lacks the Pleckstrin Homology (PH) domain that is present in all other PI-PLCs. In mammalian cells, PLCζ is only expressed in sperm.
PLCζ represents the most simple PI-PLC isoform, only consisting of the catalytic X- and Y-domain, an EF-hand domain and a C2 lipid-binding domain. Other subfamilies contain, besides the beforementioned domains, conserved sequences that allow them to be regulated by e.g. heterotrimeric G-proteins (PLCβ), tyrosine kinases (PLCγ), or Ras (PLCε). How PLCδ, -η and -ζ isoforms are regulated is not clear but may involve Ca2+.
Domain structure and organization of PI-PLC isozymes. Plant PLCs belong to the most simple group, the PLCζ. PLCη undergoes alternative splicing, generating variable C termini with a PDZ-binding motif being only present in the longer forms.
Abbreviations: EF, EF-hand domain; PH, Pleckstrin homology domain; RA, Ras-binding domain; RasGEF, guanine-nucleotide-exchange factor for Ras; SH, Src homology domain; X and Y, catalytic domain.
Lipid Signaling in Plants . Series: Plant Cell Monographs,
Vol. 16 , Munnik, T. (Ed.) 2010, 330 p. 49 illus., 7 in
color., Hardcover. ISBN: 978-3-642-03872-3. Springer Verlag, Heidelberg,
Plant Lipid Signaling Protocols. Munnik T . and Heilmann I. ( Eds.) 2013. Series: Methods in Molecular Biology 1009, Humana Press, NJ, USA. 305 p.
International (refereed) journals
100. Zarza X, Atanasov K,; Marco F, Arbona V, Carrasco P, Kopka J, Fotopoulos V, Munnik T, Gómez-Cadenas A, Tiburcio AF, & Alcazar R. (2016) Mechanisms of salt tolerance induced by Polyamine Oxidase 5 loss-of-function mutations in Arabidopsis thaliana. Plant Cell Environ. (In Press.)
99. Hirano T, Munnik T, and Sato MH. (2015) FAB1 mediates endosome maturation to establish basal PIN polarity through cortical microtubules interaction in Arabidopsis. Plant Physiol. 2015 169: 1961-1974.
98. Beligni MV, Bagnato C, Prados MB, Bondino H, Laxalt AM, Munnik T, Ten Have A. (2015) The diversity of algal phospholipase D homologs revealed by biocomputational analysis. J. Phycol. 51: 943-962.
97. Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS. (2015) Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development 142: 1437-1446
96. Leprince AS, Magalhaes N, De Vos D, Bordenave M, Clément G, Meyer C, Munnik T and Savouré A. (2015) Involvement of Phosphatidylinositol 3-kinase in the regulation of proline catabolism in Arabidopsis thaliana. Front. Plant Sci.5: 772.
95. Julkowska MM, McLoughlin F, Galvan-Ampudia CS, Rankenberg JM, Kawa D, Klimecka M, Haring MA, Munnik T, Kooijman EE, Testerink C. (2015) Identification and functional characterization of the Arabidopsis Snf1-related protein kinase SnRK2.4 phosphatidic acid-binding domain. Plant Cell Environ. 38: 614-24.
94. Zheng J, Won Han S, Munnik T, Rojas-Pierce M. (2014) Multiple vacuoles in impaired tonoplast trafficking3 mutants are independent organelles. Plant Signal Behav. 9: pii: e29783.
93. Singh MK, Krüger F, Beckmann H, Brumm S, Vermeer JEM, Munnik T, Mayer U, Stierhof YD, Grefen C, Schumacher K, Jürgens G. (2014) Protein Delivery to Vacuole Requires SAND Protein-Dependent Rab GTPase Conversion for MVB-Vacuole Fusion. Curr Biol. 24: 1383-1389.
92. Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H, Heilmann M, van Wijk R, Vermeer JEM, Heilmann I, Munnik T, Friml J. (2014) Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26: 2114-2128.
91. Nováková P, Hirsch S, Feraru E, Tejos R, van Wijk R, Viaene T, Heilmann M, Lerche J, De Rycke R, Feraru MI, Grones P, Van Montagu M, Heilmann I, Munnik T, Friml J. (2014) SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. Proc. Natl. Acad. Sci. USA 111: 2818-23.
90. Simon ML, Platre MP, Assil S, van Wijk R, Chen WY, Chory J, Dreux M, Munnik T, Jaillais Y. (2014) A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J. 77: 322-337
89. Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C. (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23: 2044-2050.
88. Munnik T. (2013) Analysis of D3-, 4-, 5-phosphorylated phosphoinositides using HPLC. Methods Mol. Biol. 1009: 17-24.
87. Arisz SA & Munnik T. (2013) Distinguishing phosphatidic acid pools from de novo synthesis, PLD and DGK. Methods Mol. Biol. 1009: 55-62.
86. Arisz SA & Munnik T. (2013) Use of Phospholipase A2 for the production of lysophospholipids. Methods Mol. Biol. 1009: 63-68.
85. Munnik T. & Laxalt AM. (2013) Measuring PLD activity in vivo. Methods Mol. Biol. 1009: 219-232.
84. Munnik T. & Wierzchowiecka M. (2013) Lipid-binding analysis using a fat blot assay. Methods Mol. Biol. 1009: 253-260.
83. Vermeer JEM. & Munnik T. (2013) Using genetically encoded fluorescent reporters to image lipid signaling in living plants. Methods Mol. Biol. 1009: 283-290.
82. Munnik T. & Zarza X. (2013) Analyzing plant signaling phospholipids through 32Pi-labeling and TLC. Methods Mol. Biol. 1009: 3-16.
81. McLoughlin F, Arisz SA, Dekker HL, Kramer GJ, de Koster CG, Haring MA, Munnik T & Testerink C (2013) Identification of novel candidate phosphatidic acid binding proteins involved in the salt stress response ofArabidopsis thaliana roots. Biochem. J. 450: 573-581
80. Arisz SA, van Wijk R, Roels W, Zhu J-K, Haring MA & Munnik T. (2013) Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Front Plant Sci. 4, 1, p1-15.
79. McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, Laurière C, Munnik T, Haring MA, Testerink C. (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J. 72: 436-449.
78. Horváth I, Glatz A, Nakamoto H, Mishkind ML, Munnik T, Saidi Y, Goloubinoff P, Harwood JL & Vigh L. (2012) Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog. Lipid Res. 51: 208-220.
77. Gonorazky G, Laxalt AM, Dekker HL, Rep M, Munnik T, Testerink C, de la Canal L. (2012) Phosphatidylinositol 4-phosphate is associated to extracellular lipoproteic fractions and is detected in tomato apoplastic fluids. Plant Biol. 14: 41-49.
76. Arisz SA. & Munnik T . (2011) The salt-stress induced lysophosphatidic-acid response in Chlamydomonas is produced via phospholipase A2 hydrolysis of diacylglycerol kinase-generated phosphatidic acid. J. Lipid. Res. 52: 2012-2020.
75. Munnik T & Nielsen, E. Green light for polyphosphoinositide signals in plants. Curr. Opin. Plant Biol. 14: 489-497.
74. Zonia L & Munnik T. (2011) Understanding pollen tube growth. Trends Plant Sci. 16: 347-352.
73. Camehl I, Drzewiecki C, Vadassery J, Shahollari B, Sherameti I, Forzani C, Munnik T, Hirt H, Oelmüller R. (2011) The OXI1 Kinase Pathway Mediates Piriformospora indica -Induced Growth Promotion in Arabidopsis. PLoS Pathogen. 7: e1002051.
72. Testerink C, & Munnik T . (2011) Molecular, cellular and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62: 2349-2361.
71. Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GCM, Ekengren SK, Meijer HJG, Seifi A, Bai Y, ten Have A, Munnik T, Thomma BPHJ, Joosten MHAJ. (2010) Identification of tomato phosphatidylinositol-specific phospholipase C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J . 62: 224-239.
70. Munnik T & Vermeer JEM (2010) Osmotic stress-induced phosphoinositide and inositolphosphate signalling in plants. Plant Cell Environ. 33: 655-669.
69. Mishkind M, Vermeer JEM, Darwish E, Munnik T . (2009) Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. Plant J. 60: 10-21.
68. Arisz SA, Testerink C, MunnikT. (2009)Plant PA signalling via diacylglycerol kinase. Biochim. Biophys. Acta. 1791: 869-875.
67. Zonia L & Munnik T. (2009) Uncovering hidden treasures in pollen tube growth mechanics. Trends Plant Sci. 14: 318-327.
66. Darwish E, Testerink C, Khaleil M, El-Shihy O, Munnik T. (2009) Phospholipid-signaling responses in salt stressed rice leaves. Plant Cell Physiol. 50: 986-997.
65. Bargmann BOR., LaxaltAM, ter Riet B, TesterinkC, MerquiolE, Mosblech A, Leon-Reyes AH, Pieterse, CM, Haring MA, HeilmannI, Bartels D, Munnik T. (2009). Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant Cell Environ. 32: 837-850.
64. Munnik T & Testerink C. (2009). PlantPhospholipid Signalling - 'in a nutshell'. J. Lipid Res. 50: 260-265.
63. Bargmann BOR, Arisz SA, Laxalt AM, ter Riet B, van Schooten B, Merquiol E, Testerink C, Haring MA, Bartels D, Munnik T. (2009). Multiple PLDs required for high salinity- and water deficit tolerance in plants. Plant Cell Physiol. 50: 78-89.
62. Vermeer JEM, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella Jr. TWJ. (2009) Visualisation of PtdIns4P dynamics in living plantcells. Plant J. 57: 356-372.
61. Gonorazky G, Laxalt AM, Testerink C, Munnik T, de la Canal L. (2008) Phosphatidylinositol 4-phosphate accumulates extracellularly upon xylanase treatment in tomato cell suspensions. Plant Cell Environ. 31: 1051-1062.
60. Zonia L, Munnik T. (2008) Still life: Pollen tube growth observed in millisecond resolution. Plant Signal. Behavior. 3: 836-838.
59. Testerink C, Larsen PB,McLoughlin F,vander Does D,van Himbergen JAJ, Munnik T. (2008) PA, a stress-induced short cut to switch-on ethylene signalling by switching-off CTR1? Plant Signal. Behavior. 3: 681-683.
58. Kusano H, Testerink C, Vermeer JEM, Tsuge T, Oka A, Shimada H, Munnik T, Aoyama T. (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator for root hair tip growth. Plant Cell 20: 367-380.
57. Zonia L, Munnik T . (2008) Visualization of vesicle trafficking dynamics in growing tobacco pollen tubes and identification of zones of endocytosis and exocytosis. J. Exp. Bot. 59: 861-873.
56. TesterinkC, Larsen P.B., van der Does D, van Himbergen JAJ, Munnik T. (2007) Phosphatidic acid bindsto and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 14: 3905-3914.
55. Van LeeuwenW, Vermeer JEM, Gadella Jr. TWJ, Munnik T. (2007) Visualisation ofphosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J. 52: 1014-1026.
54. KooijmanEE, Tieleman DP, Testerink C, MunnikT, Rijkers DTS, Burger KNJ, de Kruijff B. (2007) An electrostatic/hydrogenbond switch as basis for the specific interaction of phosphatidic acid with proteins. J. Biol. Chem. 282: 11356-11364.
53. Zonia L, Munnik T. (2007) Life under pressure: Hydrostatic pressure in cell growth and function. Trends Plant Sci. 12: 90-97.
52. Ramos-Diaz A, Brito-Argaez L, Munnik T, Hernandez-Sotomayor SM. (2007) Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway. Planta 225: 393-401.
51. Zonia L, Müller M, and Munnik T . (2006) Cell volume oscillations in the pollen tube apical region are an integral component of the biomechanics of Nicotiana tabacum pollen tube growth. Cell Biochem. Biophys. 46, 209-232.
50. Bargmann BOR, Munnik T. (2006) The role of phospholipase D in plant stress responses. Curr. Opin. Plant Biol. 9: 515-522.
49. Zonia L, Munnik T . (2006). Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell. Biochem. 39: 207-237
48. Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R, LaxaltAM, JonesDR, DivechaN, Gadella Jr. TWJ, Munnik T. (2006) Visualisation of PtdIns3 P dynamics in living plant cells. Plant J. 47: 687-700.
47. Van Schooten B, Testerink C, Munnik T. (2006) Signalling diacylglycerol pyrophosphate, a new phosphatidic acid metabolite. Biochim. Biophys. Acta. 1761: 151-159.
46. Bargmann BOR,Laxalt AM, ter Riet B, Schouten E, van Leeuwen W, Dekker HL, de Koster CG, HaringMA, Munnik T. (2006) LePLDβ1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. Plant J. 45: 358-368.
45. Testerink C & Munnik T. (2005) Phosphatidic acid - a multifunctional stress-signalling lipid in plants. Trends Plant Sci. 10: 368-375.
44. Van Leeuwen W, Okresz L, BögreL, Munnik T. (2004) Learning the lipid language of plant signalling. Trends Plant Sci. 9: 378-384.
43. Testerink C, Dekker HL, Lim Z-Y, Johns MK, Holmes AB, deKoster CG, Ktistakis NT, Munnik T. (2004) Isolation and identification of phosphatidic acid targets from plants. Plant J. 39: 527-536.
42. De Jong CF, Laxalt AM, Bargmann BOR, de Wit PJGM, Joosten MHAJ, Munnik T. (2004). Phosphatidic acid accumulation is an early response in the Cf-4/Avr4interaction. Plant J. 39: 1-12.
41. Anthony RG, Henriques R, Helfer A, Mészáros T, Rios G, Testerink C, Munnik T, Deák M, Koncz C, Bögre L. (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis . EMBO J. 23: 572-581.
40. Zonia LE, Munnik T. (2004) Osmotically-induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol. 134: 813-823.
39. Dhonukshe P, Laxalt AM,Goedhart J, Gadella JrTWJ, Munnik T . (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15: 2666-2679.
38. Arisz SA, Valianpour F, Van GennipAH, Munnik T . (2003) Substrate preference of stress-activated phospholipase D in Chlamydomonas and its contribution to phosphatidic acid formation. Plant J. 34, 595-604.
37. Den Hartog M, Verhoef N, MunnikT. (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol . 132: 311-317.
36. Meijer HJG & Munnik T. (2003) Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54:265-306.
35. Latijnhouwers M, Munnik T, Govers F. (2002)Phospholipase D in Phytophthora infestans and its role in zoospore differentiation. Mol. Plant Microbe Interact. 15: 939-946.
34. Laxalt AM & Munnik T. (2002) Phospholipid signalling in plant defence. Curr. Opin. Plant Biol. 5: 332-338.
33. Meijer HJG, ter Riet B, van Himbergen JAJ, Musgrave A, Munnik T . (2002) KCl activates phospholipase D at two different concentration ranges: distinguishing between hyperosmotic stress and membrane depolarization. Plant J. 31: 51-60.
32. Oprins JCJ, van den Burg C, MeijerHP, Munnik T, GrootJA. (2002) TNFα potentiation secretion induced by histamine ina human intestinal epithelial cell line and in mouse distal colon: Involvement of the phospholipase D pathway. Gut 50: 314-321.
31. Munnik T & Musgrave A. (2001) Phospholipid signaling in plants: Holding on to phospholipase D. Science STKE 111, PE42.
30. Meijer HJG, Berrie CP, Lurisci C, Divecha N, Musgrave A, Munnik T. (2001) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-phosphate and its accumulation upon osmotic stress. Biochem. J . 360: 491-498.
29. Munnik T, Meijer HJG. (2001) Osmotic stress activates distinct lipid- and MAPK signalling pathways in plants. FEBS Lett. 498: 172-178.
28. Laxalt A, ter RietB, Verdonk JC, Parigi L, Tameling WIL, Vossen J, Haring M, Musgrave A, Munnik T.(2001) Characterization of five tomato phospholipase D cDNAs: Rapid and specific expression of LePLDβ1 upon elicitation with xylanase. Plant J. 26: 237-248.
27. Munnik T. (2001) Phosphatidic acid – an emerging plant lipid second messenger. Trends Plant Sci. 6: 227-233.
26. Meijer HJG, Arisz, SA, Himbergen JAJ, Musgrave A, Munnik T. (2001) Hyperosmotic stress rapidly generates lyso-phosphatidic acid in Chlamydomonas. Plant J. 25: 541-548.
25. Oprins JCJ, van den Burg C, Meijer HP, Munnik T, Groot JA. (2001) PLD pathway involved in carbachol-induced Cl- secretion, possible role of TNFα. Am. J. Physiol. Cell Physiol. 280: C789-795.
24. Den Hartog M, Musgrave A, Munnik T. (2001) Nod factor-induced phosphatidic acid and diacylglycerolpyrophosphate formation, a role for phospholipase C and D in root hair deformation. Plant J. 25: 55-66.
23. Oprins JC, Meijer HP, van derBurg C, Munnik T, Groot JA. (2000) Tumor necrosis factor α potentiates ion secretion induced by histamine in HT29cl.19A cells via the phospholipase D pathway. Gastroenterology 118: 5216
22. Van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, Munnik T. (2000) Elicitation of suspension-cultured tomato cells triggers formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol . 123: 1507-1515.
21. Munnik T, Meijer HJG, ter Riet B, Van Himbergen JAJ, Hirt H, Frank W, Bartels D, Musgrave A. (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. PlantJ. 22: 147-154.
20. Kuin H, Koerten H, Ghijsen WE, Munnik T, van den Ende H, Musgrave A. (2000) Chlamydomonas contain calcium stores that are mobilized when phospholipase C is activated. Planta 210: 286-294.
19. Arisz SA, Musgrave A, van den Ende H, Munnik T. (2000) Polar glycerolipids of Chlamydomonas moewusii. Phytochemistry 53: 265-270.
18. Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D. (2000) Water-deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12: 111-124.
17. Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, Musgrave A, Hirt H. (1999) Distinct osmo-sensing protein kinase pathways are involved in signalling moderate and severe hyper-osmotic stress. Plant J. 20: 381-388.
16. Van Himbergen JAJ, ter Riet B, Meijer HJG, van den Ende H, Musgrave A, Munnik T. (1999) Mastoparan analogues activate phospholipase C- and phospholipase D activity in Chlamydomonas: a comparative study. J. Exp. Bot. 50: 1735-1742.
15. Meijer HJG, Divecha N, van den Ende H, MusgraveA, Munnik T. (1999) Hyperosmotic stress induces rapid synthesis of phosphatidyl-D-inositol 3,5-bisphosphate in plant cells. Planta 208: 294-298.
14. Ermilova E, Zalutskaya Z, Munnik T, Van den Ende H, Gromov B. (1998) Calcium in the control of chemotaxis in Chlamydomonas. Biologia 53: 577-581.
13. Munnik T, van Himbergen JAJ, ter Riet B, Braun F-J, Irvine RF, van den Ende H, Musgrave A. (1998) Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipase C and -D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan. Planta 207: 133-145.
12. Munnik T, Irvine RF, and Musgrave A. (1998) Phospholipid signalling in plants. Biochim. Biophys. Acta, 1389: 222-272.
11. De Vrije T and Munnik T. (1997) Activation of phospholipase D by calmodulin antagonists and mastoparan in carnation petal tissue. J. Exp. Bot. 48: 1631-1637.
10. Munnik T, de Vrije T, Irvine RF, Musgrave A. (1996) Identification of diacylglycerol pyrophosphate as a novel metabolic product of phosphatidic acid during G-protein activation in plants. J. Biol. Chem. 271: 15708-15715.
9. Munnik T, Arisz SA, DeVrije T, Musgrave A.(1995) G-protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 1997-2010.
8. Munnik T, Irvine RF, Musgrave A. (1994) Rapid turnover of phosphatidylinositol 3-phosphate in Chlamydomonas eugametos : signs of a phosphoinositide 3-kinase signalling pathway in lower plants? Biochem. J. 298: 269-273.
7. Munnik T, Musgrave A, De Vrije T. (1994) Rapid turnover of polyphosphoinositides in carnation flowerpetals. Planta 193: 89-98.
6. De Nobel JG, Munnik T, Pureveen JBM, Eijkel GB, Mulder MM, Boon JJ, van den Ende H, Klis FM. (1993) Analysis of cell wall mutants of Saccharomyces cerevisiae by pyrolysis mass spectrometry. Acta Bot. Neerl. 42: 505-516.
5. Musgrave A, Schuring F, Munnik T, Visser K. (1993) Inositol 1,4,5-trisphosphate as fertilization signal in plants, testcase Chlamydomonas eugametos. Planta 191: 280-284.
4. Van den Ende H, vandenBriel ML, Lingeman R, van Gulik P, Munnik T. (1992) Zygote formation in the the homothallic green alga Clamydomonas monoica Strehlow. Planta 188: 551-558.
3. De Nobel JG, Klis FM, Ram A, van Unen H, PriemJ, Munnik T, van den Ende H. (1991) Cyclicvariations in the permeability of the cell wall of Saccharomyces cerevisiae. Yeast 7: 589-598.
2. De Nobel JG, Klis FM, Priem J, Munnik T, van den Ende H. (1990) The glucanase-soluble mannoproteins limit cell wall porosity in Saccharomyces cerevisiae. Yeast 6: 491-499.
1. De Nobel JG, Klis FM, Munnik T, Priem J, van den Ende H. (1990) An assay of relative cell wall porosity in Saccharomyces cerevisiae, Kluyveromyces lactis and Schizosaccharomyces pombe. Yeast 6: 483-490.
De Vrije T. & Munnik T. (1998) SignalTransduction pathways and senescence. In: The Post-Harvest Treatment of Fruit and Vegetables - Current Status and Future prospects. Eds. Woltering EJ, Gorris LG, Jongen WMF, McKennaB, Höhn E, Bertolini P, Woolfe ML, de Jager A, Ahvenainen R, Artes Calero F, Luxembourg, European Communities, pp 329-338 (ISBN 92-828-2003-3).
Testerink C. & Munnik T. (2004) Plant responseto stress: phosphatidic acid asa second messenger. In Encyclopedia of Plant and Crop Science(RM Goodman, ed.), Marcel Dekker Inc,New York, 995-998.
de Wit PJGM, Brandwagt BF, van den Burg HA, Gabriëls SHEJ, van der HoornRAL, deJong CF,van 't KloosterJW, de Kock MJD, Kruijt M, Luderer, R, Munnik T, Stulemeijer IJE, Thomma BPHJ, Vervoort JJM, Westerink N, Joosten MHAJ. (2004) Molecular basis of plant response to microbial invasion. In: Biology of Plant-Microbe Interactions, Vol. 4, I. Tikhonovich, B. Lugtenberg and N. Provorov (eds.), International Society for Molecular Plant-Microbe Interactions, St. Paul, Minnesota, USA, pp.203-207.
Zonia L. & Munnik T. (2006) Cracking the green paradigm: Functional coding of phosphoinositide signals in plant stressresponses. In Subcellular Biochemistry, Vol. 39 : Biology of Inositols and Phosphoinositides (AL Majunder and BB Biswas, eds.), Kluwer/Plenum Publishers, London, pp 207-237.
Lee Y, Munnik T, Lee Y. (2010) PlantPhosphatidylinositol 3-kinase. In Lipid Signaling in Plants. Series: Plant CellMonographs, Vol. 16, Munnik, T (Ed.) ISBN: 978-3-642-03872-3. Springer Verlag, Heidelberg, Germany. pp. 95-106
Arisz SA and Munnik T. (2010) Diacylglycerol kinase.In Lipid Signaling inPlants. Series: Plant CellMonographs, Vol. 16, Munnik, T (Ed.) ISBN: 978-3-642-03872-3. Springer Verlag, Heidelberg, Germany. pp. 107-116.
Vermeer JEM and Munnik T. (2010)Imaging lipids in living plants. In Lipid Signaling in Plants. Series: Plant Cell Monographs, Vol. 16, Munnik, T (Ed.) ISBN: 978-3-642-03872-3. Springer Verlag, Heidelberg, Germany. pp. 185-202.
Phospholipid signalling; biochemistry, cell biology, plant biology, (a)biotic stress signalling
- Associate Editor Plant Physiology, section Signaling & Responses
- Visiting Professor - Institute of Microbiology Academy of Sciences of the Czech Republic, Prague, Czech Republic. Pavla Binarova Lab (2007)
- Associate Professor Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam (2005-present).
- Visiting Professor - Rutgers University, New Brunswick, NJ, USA. George Carman Lab (2002)
- Assistant Professor Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam (2000-2005).
- Post-doc - With Alan Musgrave and Ben Cornelissen, Lipid signalling during plant-pathogen interactions (1997-2000).
- Post-doc - Vienna BioCenter, Austria - Heribert Hirt Lab, MAPK signalling. EMBO short-term fellowship (1997/1998)
- Ph.D ( cum laude; <3%) - With Herman van den Ende and Alan Musgrave, University of Amsterdam, The Netherlands; Thesis: Phospholipid metabolism with respect to signal transduction in the green alga Chlamydomonas. (1997)
- PhD student - Cambridge, UK - Robin Irvine Lab, Phosphoinositide signalling (1992/1994)
- PhD student - University of Amsterdam, The Netherlands, PhD student Alan Musgrave Lab, Chlamydomonas (1992-1996)
- Research Assistant - Agrotechnological Research Institute (ATO-DLO; Dr. T. de Vrije), Wageningen, The Netherlands. Topic: Ethylene signalling in carnation flowers. (1991-1992)
- Research Assistant - With Frans Klis, Institute for Molecular Cell Biology, University of Amsterdam. Topic: Yeast cell wall assembly (1988-1990)
- B.S. - Botany, HLO Amsterdam, The Netherlands (1988)
- Editorial boards: Planta (Editor); Frontiers in Plant-Microbe Interactions ( Review Editor ); Plant Signaling & Behavior (Associate Editor); Frontiers in Plant Physiology (Editor); The Open Plant Science Journal (Editor). Frontiers in Plant Metabolism and Chemodiversity ( Review Editor ). Starting 1 jan 2013: Associate Editor Plant Physiology , Signaling & Responses
- Referee for: Nature, Nature Cell Biol, Nature Immunol., Science, PNAS, Curr. Biol., J. Biol. Chem., Biochem. J., FEBS. Lett., Plant Cell, Curr. Opin. Plant Biol., Trends Plant Sci., PLoS One, Plant Physiol., Plant J., Plant Mol. Biol., New Phytol., J. Exp. Bot., Plant Cell Environ., Plant Cell Physiol.
- Evaluation panels: NWO-ALW (panel member MtC; VIDI), NWO-CW (panel member ECHO, TOP), USDA (US), NIH (US), BBSRC (UK), CNRS (Fr), ISF (Isr) AACF (Can) DFG (Ger).
- PhD thesis committees: 23
• British Council Fellowship (1994)
• EMBO short-term Fellowship (1997)
• PULS Fellowship (1998-2001)
• KNAW (Dutch Royal Society of Sciences) Fellowship (2000-2005)
• VIDI fellowship for innovative research (2005-2010)
• ECHO grant (2007)
• VPP grant (2011)
• NPST grant (2012)
Publications: (see All Publications)
• Number of publications in international refereed scientific journals according to WoS: 84
• Contributions to books: 2 books (Ed.); 7 chapters (author)
• Number of citations according to WoS: 4513; average citations: 53.7; H-index: 38
• Lecturer at various International Advanced Courses (e.g. ICRO; FEBS, EPS, UNMP, TWAS)
• Coordinator and teacher of various BSc, MSc and PhD courses
• >100 Invited seminars at (inter)national universities, conferences and symposia, world wide (see below).
- Lipid Signals at Work. Invited seminar. Julius-von-Sachs-Institut für Biowissenschaften, University of Würzburg, May 27, Würzburg, Germany
- PLC meets Auxin: New Data on an Old Story. Auxin Sailing 2013, June 7-9, Leiden, The Netherlands.
- Phospholipid signals in plant stress and development. Invited seminar. The Sainsbury Laboratory, June 21, Norwich, UK.
- Stress-activated, phospholipid-based signaling pathways in plants. Plenary speaker, 54th International Conference on the Biochemistry of Lipids (ICBL): Linking Transcription to Physiology in Lipidomics, Sept 17-21, Bari, Italy.
- Phospholipid signals in plant stress and development. Invited seminar at Agrobios, Sept 23, Metaponto, Mt, Italy.
Visualizing phospholipid signals in plants. Gordon Research Conference (GRC) on Plant Lipids: Structure Metabolism and Function. Jan 26 - Feb 1, Galveston, TX, USA.
- Visualizing phospholipid signals during plant stress and development. Winter Conference POSTECH, Pohang University of Science and Technology, January 12-13, Pohang, South-Korea.
- Phospholipid Signalling in Plant Defence. BARD Workshop on Plant Innate Immunity/Effector Biology. Feb 5-8, Tel Aviv, Israel.
- Visualizing Phospholipid Signalling in Plant Stress and Development. Invited seminar. Hebrew University of Jerusalem. Feb 9, Rehovot, Israel.
- Polyphosphoinositide signalling in plants. Invited lecture. University of Lausanne. April 12, Lausanne, Switzerland.
- Phospholipid signals in plant stress & development. Invitedlecture. University of Zurich. April 13, Zurich, Switzerland.
- Polyamines trigger two distinct phospholipid signalling pathways in Arabidopsis. EPS Theme Symposium, April 26, Utrecht, The Netherlands.
- Phospholipid Signalling in Plant Stress & Development. Agricultural Biotechnology Research Center (ABRC) at Academia Sinica, June 22, Taipei, Taiwan.
- Gordon Research Conference (GRC) on Salt & Water Stress in Plants. June 24-29, Hong Kong. China.
- Lipid Signalling in Plant Stress and Development. 21st National Biology Congress, Sept 3-7, Izmir, Turkey.
- Phospholipid-based signalling. Invited seminar, University of Birmingham, May 31, Birmingham, UK.
- Phospholipid-basedsignalling during plant stress and development. Plant Science Student Conference (PSSC). June 14-17, Halle/Saale, Germany.
- Integration of abiotic and biotic stress responses: phospholipid signalling modules in plants. Annual Meeting of the Society for Experimental Biology (SEB). July 1-4, Glasgow, UK.
- Visualizing Phospholipid Signalling Pathways during Plant Stress and Development. Cell Signalling Networks, 13th IUBMB Conference, Oct 22-27, Merida, Mexico.
- Phospholipid Signalling in Plant Stress and Development.Invited seminar CICY, Yucatan Center for Scientific Research, Oct 29, Merida, Mexico.
- Integration of Abiotic Stress Responses: Phospholipid Signalling Modules in Plants. 4th International INPAS meeting on Salt & Drought Stress in Plants. Nov 18-19, Limasol, Cyprus.
- Phospholipid metabolism in plant stress and development. Plant Abiotic Stress – from Signalling to Crop Improvement. April 22-24, Valencia, Spain.
- Signaling pathways in osmotic stress. Gordon Research Conference (GRC) on Salt & Water Stress in Plants. June 13-18, Les Diablerets, Switzerland.
- Phospholipid signalling in plants. Invited lecture. University of Lausanne. June 19, Lausanne, Switzerland.
- Polyphosphoinositides in membrane trafficking during plant stress and development. EPS workshop - 'Endomembranes in plants'. July 2, Amsterdam, The Netherlands.
- Phospholipid metabolism in plant stressanddevelopment. Keynotelecture at the 19th International Symposium on Plant Lipids (ISPL2010). July 11-16, Cairns, Australia.
- Learning the lipid language of plant signalling, Frontiers in Genomics - Seminar I, National University of México (UNAM). Nov 22, Cuernavaca, Mexico.
- Phospholipid signalling in plant stress and development. Frontiers in Genomics - Seminar II, Center for Genomic Sciences (CCG), Institute of Biotechnology (IBT), National University ofMéxico (UNAM). Nov 23, Cuernavaca, Mexico.
- Phospholipid-based signal transduction. Invited seminar, University of Münster. Jan, 27, Münster, Germany.
- Phospholipid signalling in plant stress and development. Invited seminar, Michigan State University. Jan 29, Ann Arbor, MI, USA.
- Phosphatidic acid signaling in plants. Gordon Research Conference (GRC) on Plant Lipids. Feb 1-6, Galveston, Texas, USA.
- Green light for phospholipid signals. Invited seminar, Universität Bonn. March 11, Bonn, Germany.
- Phospholipid signalling in plant stress and development.Invited seminar, Max Planck Institute for Chemical Ecology. April 1, Jena, Germany.
- Phospholipids in plant stress signalling and development. Invited seminar, Leibniz Instituteof Plant Biochemistry (IPB), Halle University. April 3, Halle, Germany.
- Phosphoinositide signalling in plant stress signalling and development. COST Meeting Plant Abiotic Stress - From signaling to development. May 14-17, Tartu, Estonia.
- Phospholipid signalling in plant stress and development. Invited seminar, Dec 17, Fribourg, Zwitzerland.
- Phospholipid signalling in plant stress. Invited seminar, University of Tübingen. Jan 7, Tübingen, Germany.
- PLD Signalling in tomato. Invited seminar, Institute for Experimental Botany. Czechoslovak Academy of Sciences. Feb 15, Prague, Czech Republic.
- Phospholipid signalling in plant stress and development. Invited seminar, Université Catholique de Louvain. March 14, Louvain-la-Neuve, Belgium.
- Phospholipid-signalling events during abiotic stress. COST Meeting. April 10-13, Matera, Italy.
- Phospholipid signalling events during plant-microbe interactions. The German researchcouncil (DFG) Priority Program 'Microbial Reprogramming of Plant Cell Development'. April 16-18, Bad Honnef, Germany.
- Phospholipid signalling in and cytoskeletal control. Annual meeting of the European Cytoskeleton Club. May 14-16, Vranovská Ves, Moravia, Czech Republic.
- Phospholipid signalling in plant stress and development. 18th International Symposium on Plant Lipids (ISPL2008). July 20-25, Bordeaux, France.
- Visualizing osmotic stress-induced phospholipid signals. Gordon Research Conference (GRC) on Salt & Water Stress in Plants. Sept 7-12, Big Sky, Montana, USA.
- Phospholipid signalling in plants.Invited seminar, Stockholm University. Oct 21, Stockholm, Sweden.
- Lipid signalling in plant Stress and development. Faculty Symposium Swedish University of Agricultural Sciences (SLU), Uppsala BioCenter. Oct 22, Uppsala, Sweden.
- Phospholipid signalling in plant stress and development. International Symposium in Commemoration of 150th BirthAnniversary of Sir J.C. Bose and the Birth Centenary of Prof. SM Sircar: "A Journey from Plant Physiology to Plant Biology". Nov 24-28, Kolkata, India.
- Phospholipid signalling in plants - 'Seeing isbelieving'. 3rd European Symposium on Plant Lipids. April 1-4, York, UK.
- Lipid signalling. 3rd International Symposium on Plant Neurobiology (ISPN). May 14-18, štrbské Pleso, Slovakia.
- Lipid signals in plant defense. XIII International Congress of the International Society for Molecular Plant-Microbes Interaction (IS-MPMI). July 21-27, Sorrento, Italy.
- Lipid signalling in response to stress. Third meeting of the Polish Society of Plant Experimental Biology, Aug 26-30, Warsaw, Poland.
- Lipidomics in Plant Cell Signalling. 4th GERLI Lipidomics Meeting (Groupe d'Etude et de Recherche en Lipidomique). Oct 9-11, Toulouse, France.
- Plant phospholipid signalling. Invited seminar, INRA-CNRS. Oct 11, Castanet-Tolosan, France.
- Phospholipid signalling gets the green light. Invited seminar, University of Würzburg. Nov 22, Würzburg, Germany.
- Visualizing phospholipid-based signalling events in plant cells. Invited seminar, Academy of Sciences of the Czech Republic. Dec 10, Prague, Czech Republic.
- How do lipids signal? Symposium on 'Signal Transduction in Plants', Research School Experimental Plant Sciences (EPS). Feb 2, Amsterdam, the Netherlands.
- Symposium on 'Order and Disorder(s) of Cell Lipids', Netherlands Society for Biochemistry and Molecular Biology. May 19, Utrecht, The Netherlands.
- PA, an emerging lipid second messenger in plant-stress responses. 15th FESPB (Federation of European Societies of Plant Biology). July 17-21, Lyon, France.
- Crosstalk between different stress pathways. Gordon Research Conference (GRC) on Salt & Water Stress in Plants. Sept 3-8, Oxford, UK.
- "Cracking the green paradigm": Functional coding of lipid signals in plant stress responses, Montagskolloquium, University of Freiburg. Jan 24, Freiburg, Germany.
- Water-stress activated phospholipid signalling pathways. International Conference on Biotechnology for Salinity & Drought Tolerance in Plants. March 28-31, Islamabad, Pakistan.
- Phosphatidic acid signalling in plant stress. 2nd International Conference on Stress signals and cellular responses. March 31-April 2, Halle, Germany.
- Diacylglycerol kinase and phosphatidic acid signalling in plants. DGK-day, Dutch Cancer Institute (NKI). Oct 6, Amsterdam, the Netherlands.
- Osmotic stress triggering multiple lipid signaling responses. Invited seminar, University of Connecticut. Oct 25, Storrs, CT, USA.
- Stress-activated PA Signalling. International Conference on Plant Lipid-Mediated Signaling. Oct 26-29, Raleigh, NC, USA.
- Plant phospholipid signalling - What's cooking? University of North Carolina. Nov 1, Chapel Hill, NC, USA.
- Learning the lipid language in plant signalling. TWAS Course on Signal Transduction in Plants, University of Mar del Plata. Nov 24, Mar del Plata, Argentina.
- PA signalling and stress signal integration. TWAS Course on Signal Transduction in Plants, University of Mar del Plata. Nov 25, Mar del Plata, Argentina.
- Phospholipidsignalling in plants - What's cooking? University of Mar del Plata. Dec 1, Mar del Plata, Argentina.
- Phospholipid-based signallingin plants. 10th Congress of the Panamerican Association of Biochemistry and Molecular Biology (PABMB). Dec 3-6, 2005, Pinamar, Argentina.
- Stress-activated phospholipid signaling. Keystone Symposium on Plant Responses to Abiotic Stress. Feb 19-24, Santa Fe, NM, USA.
- Phospholipid signals in biotic- and abiotic-stress signalling. CRISP meeting, Feb 27 - March 1, Radstadt, Austria.
- Phospholipid signalling in plants. Annual Meeting Dutch Experimental Plant Sciences. April 4-5, 2004, Lunteren, the Netherlands.
- Osmotic stress-activated phospholipid signalling. Gordon Research Conference (GRC) on Salt & Water Stress In Plants. June 13-18, Hong Kong, China.
- Phospholipid signalling pathways in abiotic and biotic stress. 2nd European Plant Science Organization (EPSO) Conference. Oct. 10-14, Ischia, Italy.
- Challenging phospholipid signalling in plants. Invited seminar, University of Dundee. March 12, Dundee, Scotland, UK.
- Phospholipid-based signal transduction. Invited seminar, Free University Amsterdam, April 28, Amsterdam, The Netherlands.
- Phospholipid metabolism and signalling in plants. Invited seminar, Academic Medical Center (AMC). May 20, Amsterdam, Netherlands.
- Challenging phospholipid signalling in plants, 1st EuroFed Symposium on Plant Lipids. Sept 10-13, Aachen, Germany.
- Phospholipid signalling in plant stress. Invited seminar, Leipzig Instituteof Plant Biochemistry. Oct 23, Halle, Germany.
- Phospholipid-based signal transduction pathways in plants. Centro de Investigacion Cientifica de Yucatan (CICY). March 15, Merida, Mexico.
- Phospholipid-based signal transduction pathways in plants. NJAES Distinghuished Seminar Series Agricultural and Environmental Genomics, Rutgers University, March 20, New Brunswick, NJ, USA.
- Phospholipid-based signal transduction in plants. Seminar series Plant Cell Biology, University of Wageningen, May 17, Wageningen, The Netherlands.
- Phospholipid signalling in plants. Invited seminar, Royal Holloway, University of London. Nov 11, Egham,UK.
- Phospholipid-basedsignalling in plants. Botanisches Kolloquium, University of Hamburg. Dec 18, Hamburg, Germany.
- Phospholipid-based signalling in plants. Invited seminar, John Innes Centre, The Sainsburry Lab. Feb. 13, Norwich, UK.
- Phospholipid-based signalling triggered upon plant stress. International Conference on Stress Signals and Stress Proteins. March 15-17, Halle,Germany.
- Phospholipid-derived second messengers in plants -Differences and similarities. FEBS Advanced Course: Lipid-mediated signalling in cellular functions. June 23, Santa Maria Imbaro, Italy.
- Phospholipid signalling in plants - Current status and perspectives. FEBS Advanced Course: Lipid-mediated signalling in cellular functions. June 25, Santa Maria Imbaro, Italy.
- Osmotic stress activates distinct MAPK and lipid signalling in plants. 27th Meeting of the Federation of European Biochemical Societies (FEBS). June 30 - July 5, Lisbon, Portugal.
- Phospholipid signalling. International Training Course ICRO, Signalling to Growth and Cell Division in Arabidopsis. July 19-27, London, UK.
- Phospholipid-based signal transduction mechanisms in plant cells. Biologisches Kollo-quium, Rheinische-Friedrich-Wilhelms-Universität Bonn. Jan 10, Bonn, Germany.
- Osmotic stress activates distinct MAPK- and lipid signalling pathways in plants. Keystone symposium on Cell Activation and Signal Transduction: Lipid Second Messengers IV. Feb 5-10, Taos, New Mexico, USA.
- Phospholipid-based signal transduction mechanisms in plant cells. Biochemistry Seminar, Kansas State University. Feb 14, Manhattan, Kansas, USA.
- Phospholipid signalling. International Cell Research Organization (ICRO) - Training Course on 'Signalling to growth and cell division in Arabidopsis'. July 19-21, London, UK.
- Osmotic Stress Activates Distinct MAPK- and Lipid Signalling Pathways in Plants. Gordon Research Conferen (GRC) on Salt & Water Stress in Plants. August 20-25, Tilton, NH, USA.
- Signal transduction pathways using lipids. Invited seminar, University of Vienna. Jan 22, Vienna, Austria
- Phospholipid metabolism and cell signalling in Chlamydomonas. Invited seminar, University of Cologne. Jan 26, Cologne, Germany.
- Phospholipid-based signalling pathways in plant cells. Invited seminar, Max-Planck-Institut für Züchtungsforschung. Jan 27, Cologne, Germany.
- Phospholipid based-signalling mechanisms. International EPS Summer School on 'Signalling in plant development and defence'. July 21-23, Wageningen, The Netherlands.
- Osmotic stress triggers distinct phospholipid-based signalling pathways in plant cells. International Conference on Cellular Responses to Oxidative and Osmotic Stress. Aug 28 - Sept 1, Egmond aan Zee, The Netherlands.
- Phospholipid-derived second messengers in plant cells. IMCB seminar, University of Amsterdam. March April 8, Amsterdam, the Netherlands.
- KCl activates different lipid-derived signalling pathways in Chlamydomonas moewusii. 8th International Conference on the Cell and Molecular Biology of Chlamydomonas. June 2-7, Tahoe City, CA, USA
- Lipid signals meet MAPK. Invited seminar, University of Vienna. Dec 17, Vienna, Austria
- G-protein activated PA formation is generated via PLC and PLD and attenuated by PA kinase: Formation of the novel phospholipid, diacylglycerolpyrophosphate. Annual SON-CW Meeting, Lipids & Biomembranes. March 13-14, Lunteren, The Netherlands.
- Phospholipid-derived second messengers in Chlamydomonas eugametos. Euroconference Experimental Biology of Chlamydomonas. March 29-31, Amsterdam, The Netherlands.
- Phospholipid-derived signals in Chlamydomonas eugametos. Annual SLW Meeting, Experimental Plant Sciences. April 24-25, Lunteren, The Netherlands.
- Phospholipase C and phospholipase D signalling in the green alga Chlamydomonas. 2nd UK Phospholipid Signalling Meeting.Sept28, Cambridge, UK.
- Phospholipase C and phospholipase Dsignaling in Chlamydomonas eugametos. SLW meeting, Molecular Cell Biology of Plants. Nov 4, Wageningen, The Netherlands.
- PLC- and PLD signaling in Chlamydomonas eugametos gametes. 8th Kölner Algentag,nov 6-8, Cologne, Germany.
- Signs of phospholipase C, phospholipase D and phosphoinositide 3-kinase signalling in Chlamydomonas. Sixth International Conference on the Cell and Molecular Biology of Chlamydomonas. May 17-22, Tahoe City, CA, USA.
- Signs of a PI 3-kinase signalling pathway in Chlamydomonas. European Chlamydomonas Conference. May 23-26 may, Amsterdam, The Netherlands.
Stage / Internships
Multiple positions are available:
Lipid second messengers in plant growth and development
Phosphatidic acid (PA) and polyphosphoinositides (PPIs) are minor phospholipids in biological membranes, functioning as signalling molecules at verylow concentrations. Their turnover is much faster than that of structural phospholipids and levels quickly change in response to various biotic-(pathogens) and abiotic- (salt, cold, heat) stresses. How this is regulated and where this occurs within the cell (e.g. plasma membrane, ER, Golgi) and whole plant (e.g. root, stem, stomata) is mostly unknown. In the genome of the model plant system Arabidopsis thaliana, genees encoding various lipid kinases, phosphatases and phospholipases have been identified. Using T-DNA insertion knock-out mutants, we are pinpointing their individual contribution in stress and plant development. Using lipid biosensors - specific lipid-binding domains fused to a fluorescent protein and stably expressed in cell suspensions and whole plants - we can visualize where these lipid-second messengers are present in living cells. Students can be involved in any of the projects.
- Arabidopsis plant physiology (biotic/abiotic stress mutants)
- Arabidopsis cell biology (biotic/abiotic stress, mutants, lipid biosensors)
- Radiolabelling & Lipid biochemistry (TLC, HPLC, GC)
- Molecular cloning strategies (promotor analysis, fusion proteins, gene silencing)
- RNA/DNA ( e.g . Q/RT-PCR, Northern/Southern analysis)
- Protein extraction & analysis (Western, IP, ID by MS)
- Confocal Laser Scanning Microscopy (CLSM)
Stagecoördinator Plant Physiology
Swammerdam Institute for Life Sciences (SILS)
University of Amsterdam (UvA)
Science Park 904,
1098 XH, Amsterdam
Tel: +31 (0)20 525 7763
Phospholipid Signalling Group
Teun Munnik (PI)
Ringo van Wijk (Lab manager)
Xavier Zarza (PhD student)
Qianqian Zhang (PhD student)
Matthew Lefebvre (master student)
Ruy Kortbeek (master student)
Mart Lamers (bachelor student)
Christa Testerink (PI) -> See Testerink Lab
Magdalena Julkowska (PhD student)
Dorota Kawa (PhD student)
Carlos Galvan (post-doc)
Laura Zonia (USA)
Aleksandra Haduch (PhD student, Poland)
Wendy Roels (technician)
Dörte Klaus (PD, Toulouse, F)
Christiane Unger (Germany)
Alan Musgrave (retired)
Ana Laxalt (PI, Mar del Plata, Argentina)
Bas ter Riet (Enza Zaden, Enkhuizen, NL)
Harold Meijer (WUR, Wageningen, NL)
Christa Testerink (PI, SILS, UVA)
Wessel van Leeuwen (WUR, Wageningen, NL)
Rafa Tobeña (Madrid, Spain)
Gert-Jan de Boer (Enza Zaden, Enkhuizen, NL)
John van Himbergen (VROM)
Diewertje van der Does (UU, Utrecht, NL)
Saskia van Wees (UU, Utrecht, NL)
Fabio Formiggini (Italy)
Gaby Gonorazky (Mar del Plata, Argentina)
Martine den Hartog (Covidien, Amsterdam)
Arnold van der Luit (Oncodesign, France)
Bastiaan Bargmann (CA, USA)
Bas van Schooten (UC, CA, USA)
Essam Darwish (Cairo, Egypt)
Joop Vermeer (Lausanne, Switzerland)
Steven Arisz (UvA, Amsterdam)
Muhammad Shahbaz (Faisalabad, Pakistan)
Martine den Hartog
Julian C. Verdonk
Steven A. Arisz
Bas ter Riet
Diewertje van der Does
Jacco van Rheenen
Carlos Jr. Rubio 'Chucho'
Mark aan 't Goor
Michael Miskind (NSF, VA, USA)
Ana Laxalt (Mar del Plata, Argentina)
Joachim Goedhart (WU, Wageningen)
Dorus Gadella (WU, Wageningen)
Bas Tomassen (Erasmus Rotterdam, NL)
Katie Wilkins (Birmingham, UK)
Anne Sophie Leprince (Paris, France)
Noam Reznik (Tel Aviv, Israel)
Magdalena Wierzchowiecka (Poland)
Özgecan Tanyolaç (Izmir, Turkey)
Dorus Gadella (SILS, UvA, NL)
Nullin Divecha (Manchester, UK)
Mats Ellerström (Göteborg University, Sweden)
Takashi Aoyama (Kyoto University, Japan)
Erik Nielsen (Michican, US)
Ana Laxalt (University of Mar del Plata, Argentina)
Matthieu Joosten (WUR, Wageningen, NL)
Charles Brearley (Norwich, UK)
Chris de Koster (SILS, UvA, NL)
Ingo Heilmann (Halle, Germany)
Robin Irvine (Cambridge, UK)
Laura de la Canal (Mar del Plata, Argentina)
Nick Ktistakis (Cambridge, UK)
Ralf Oelmüller (Jena, Germany)
Heribert Hirt (Paris, France)
Jack Vossen (WUR, Wageningen, NL)
Dierk Scheel (Halle, Germany)
Dorothea Bartels (Bonn, Germany)
George Carman (Rutgers, NJ, US)
Laci Bögre (London, UK)
Claudia Jonak (Vienna, Austria)
Susanne Hoffmann-Benning (Michigan, US)
Pavla Binarova (Prague, Czech)
Ingo Heilmann (Halle, Germany)
Jörg Kudla (Münster, Germany)
Bert de Boer, VU, Amsterdam)
Silke Robatzek (Norwich, UK)
Mariusz Pietruszka (University of Silesia, Poland)
Antonio Fernandez Tiburcio (Barcelona, Spain)
Noni Franklin-Tong (University of Birmingham, UK)
Edgar Kooijman (Kent, USA)
Aviah Zilberstein (Tel Aviv, Israel)
İsmail Türkan (Izmir, Turkey)
Pia Harryson (Stockholm, Sweden)
- Hirano, T., Munnik, T., & Sato, M. H. (2015). Phosphatidylinositol 3-Phosphate 5-Kinase, FAB1/PIKfyve Kinase Mediates Endosome Maturation to Establish Endosome-Cortical Microtubule Interaction in Arabidopsis. Plant Physiology, 169(3), 1961-1974. DOI: 10.1104/pp.15.01368 [details] [PDF]
- Julkowska, M. M., McLoughlin, F., Galvan-Ampudia, C. S., Rankenberg, J. M., Kawa, D., Klimecka, M., ... Testerink, C. (2015). Identification and functional characterization of the Arabidopsis Snf1-related protein kinase SnRK2.4 phosphatidic acid-binding domain. Plant, cell and environment, 38(3), 614-624. DOI: 10.1111/pce.12421 [details] [PDF]
- Beligni, M. V., Bagnato, C., Prados, M. B., Bondino, H., Laxalt, A. M., Munnik, T., & Ten Have, A. (2015). The diversity of algal phospholipase D homologs revealed by biocomputational analysis. Journal of phycology, 51(5), 943-962. DOI: 10.1111/jpy.12334 [details]
- Rodriguez-Villalon, A., Gujas, B., van Wijk, R., Munnik, T., & Hardtke, C. S. (2015). Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development - The Company of Biologists, 142(8), 1437-46. DOI: 10.1242/dev.118364 [details / files]
- Munnik, T. (2014). PI-PLC: Phosphoinositide-Phospholipase C in Plant Signaling. In X. Wang (Ed.), Phospholipases in plant signaling. (pp. 27-54). (Signaling and communication in plants; No. 20). Heidelberg: Springer. DOI: 10.1007/978-3-642-42011-5_2 [details]
- Leprince, A. S., Magalhaes, N., de Vos, D., Bordenave, M., Crilat, E., Clément, G., ... Savouré, A. (2014). Involvement of Phosphatidylinositol 3-kinase in the regulation of proline catabolism in Arabidopsis thaliana. Frontiers in Plant Science, 5, . DOI: 10.3389/fpls.2014.00772 [details] [PDF]
- Nováková, P., Hirsch, S., Feraru, E., Tejos, R., van Wijk, R., Viaene, T., ... Friml, J. (2014). SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 111(7), 2818-2823. DOI: 10.1073/pnas.1324264111 [details]
- Simon, M. L. A., Platre, M. P., Assil, S., van Wijk, R., Chen, W. Y., Chory, J., ... Jaillais, Y. (2014). A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant Journal, 77(2), 322-337. DOI: 10.1111/tpj.12358 [details]
- Singh, M. K., Krüger, F., Beckmann, H., Brumm, S., Vermeer, J. E. M., Munnik, T., ... Jürgens, G. (2014). Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion. Current Biology, 24(12), 1383-1389. DOI: 10.1016/j.cub.2014.05.005 [details]
- Tejos, R., Sauer, M., Vanneste, S., Palacios-Gomez, M., Li, H., Heilmann, M., ... Friml, J. (2014). Bipolar Plasma Membrane Distribution of Phosphoinositides and Their Requirement for Auxin-Mediated Cell Polarity and Patterning in Arabidopsis. The Plant Cell, 26(5), 2114-2128. DOI: 10.1105/tpc.114.126185 [details]
- Zheng, J., Han, S. W., Munnik, T., & Rojas-Pierce, M. (2014). Multiple vacuoles in impaired tonoplast trafficking3 mutants are independent organelles. Plant Signaling & Behavior, 9(10), e29783. DOI: 10.4161/psb.29783 [details]
- Arisz, S. A., van Wijk, R., Roels, W., Zhu, J. K., Haring, M. A., & Munnik, T. (2013). Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Frontiers in Plant Science, 4(january), 1. DOI: 10.3389/fpls.2013.00001 [details] [PDF]
- Arisz, S. A., & Munnik, T. (2013). Use of phospholipase A2 for the production of lysophospholipids. Methods in Molecular Biology, 1009, 63-68. DOI: 10.1007/978-1-62703-401-2_7 [details]
- Arisz, S. A., & Munnik, T. (2013). Distinguishing phosphatidic acid pools from de novo synthesis, PLD, and DGK. In T. Munnik, & I. Heilmann (Eds.), Plant lipid signaling protocols. (pp. 55-62). (Methods in molecular biology; No. 1009). New York: Humana Press. DOI: 10.1007/978-1-62703-401-2_6 [details]
- Galvan-Ampudia, C. S., Julkowska, M. M., Darwish, E., Gandullo, J., Korver, R. A., Brunoud, G., ... Testerink, C. (2013). Halotropism is a response of plant roots to avoid a saline environment. Current Biology, 23(20), 2044-2050. DOI: 10.1016/j.cub.2013.08.042 [details]
- McLoughlin, F., Arisz, S. A., Dekker, H. L., Kramer, G., de Koster, C. G., Haring, M. A., ... Testerink, C. (2013). Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochemical Journal, 450(3), 573-581. DOI: 10.1042/BJ20121639 [details]
- Munnik, T. (2013). Analysis of d3-,4-,5-phosphorylated phosphoinositides using HPLC. Methods in Molecular Biology, 1009, 17-24. [details]
- Munnik, T., & Wierzchowiecka, M. (2013). Lipid-binding analysis using a fat blot assay. Methods in Molecular Biology, 1009, 253-259. DOI: 10.1007/978-1-62703-401-2_23 [details]
- Munnik, T., & Zarza, X. (2013). Analyzing Plant Signaling Phospholipids Through (32)P i-Labeling and TLC. Methods in Molecular Biology, 1009, 3-15. DOI: 10.1007/978-1-62703-401-2_1 [details]
- Munnik, T., & Laxalt, A. M. (2013). Measuring PLD Activity In Vivo. Methods in Molecular Biology, 1009, 219-231. DOI: 10.1007/978-1-62703-401-2_20 [details]
- Vermeer, J. E. M., & Munnik, T. (2013). Using genetically encoded fluorescent reporters to image lipid signalling in living plants. Methods in Molecular Biology, 1009, 283-289. DOI: 10.1007/978-1-62703-401-2_26 [details]
- Gonorazky, G., Laxalt, A. M., Dekker, H. L., Rep, M., Munnik, T., Testerink, C., & de la Canal, L. (2012). Phosphatidylinositol 4-phosphate is associated to extracellular lipoproteic fractions and is detected in tomato apoplastic fluid. Plant Biology, 14(1), 41-49. DOI: 10.1111/j.1438-8677.2011.00488.x [details]
- McLoughlin, F., Galvan-Ampudia, C. S., Julkowska, M. M., Caarls, L., van der Does, D., Laurière, C., ... Testerink, C. (2012). The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant Journal, 72(3), 436-449. DOI: 10.1111/j.1365-313X.2012.05089.x [details]
- Horvath, I., Glatz, A., Nakamoto, H., Mishkind, M. L., Munnik, T., Saidi, Y., ... Vigh, L. (2012). Heat shock response in photosynthetic organisms: membrane and lipid connections. Progress in lipid research, 51(3), 208-220. DOI: 10.1016/j.plipres.2012.02.002 [details]
- Arisz, S. A., & Munnik, T. (2011). The salt stress-induced LPA response in Chlamydomonas is produced via PLA(2) hydrolysis of DGK-generated phosphatidic acid. Journal of Lipid Research, 52(11), 2012-2020. DOI: 10.1194/jlr.M016873 [details]
- Munnik, T., & Nielsen, E. (2011). Green light for polyphosphoinositide signals in plants. Current Opinion in Plant Biology, 14, 1-9. DOI: 10.1016/j.pbi.2011.06.007 [details]
- Testerink, C., & Munnik, T. (2011). Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. Journal of Experimental Botany, 62(7), 2349-2361. DOI: 10.1093/jxb/err079 [details]
- Zonia, L., & Munnik, T. (2011). Understanding pollen tube growth: the hydrodynamic model versus the cell wall model. Trends in Plant Science, 16(7), 347-352. DOI: 10.1016/j.tplants.2011.03.009 [details]
- Camehl, I., Drzewiecki, C., Vadassery, J., Shahollari, B., Sherameti, I., Forzani, C., ... Oelmüller, R. (2011). The OXI1 kinase pathway mediates Piriformospora indica-induced growth promotion in Arabidopsis. PLoS Pathogens, 7(5), e1002051. DOI: 10.1371/journal.ppat.1002051 [details] [PDF]
- Arisz, S. A., & Munnik, T. (2010). Diacylglycerol kinase. In T. Munnik (Ed.), Lipid signaling in plants. (pp. 107-114). (Plant cell monographs; No. 16). Heidelberg: Springer. DOI: 10.1007/978-3-642-03873-0_7 [details]
- Munnik, T., & Vermeer, J. E. M. (2010). Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant, cell and environment, 33(4), 655-669. DOI: 10.1111/j.1365-3040.2009.02097.x [details]
- Vermeer, J. E. M., & Munnik, T. (2010). Imaging lipids in living plants. In T. Munnik (Ed.), Lipid signaling in plants. (pp. 185-199). (Plant cell monographs; No. 16). Heidelberg: Springer. DOI: 10.1007/978-3-642-03873-0_13 [details]
- Vossen, J. H., Abd-El-Haliem, A., Fradin, E. F., van den Berg, G. C. M., Ekengren, S. K., Meijer, H. J. G., ... Joosten, M. H. A. J. (2010). Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant Journal, 62(2), 224-239. DOI: 10.1111/j.1365-313X.2010.04136.x [details]
- Lee, Y., & Munnik, T. (2010). Plant phosphatidylinositol 3-kinase. In T. Munnik (Ed.), Lipid signaling in plants. (pp. 95-106). (Plant cell monographs; No. 16). Heidelberg: Spinger. DOI: 10.1007/978-3-642-03873-0_6 [details]
- Arisz, S. A., Testerink, C., & Munnik, T. (2009). Plant PA signaling via diacylglycerol kinase. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, 1791(9), 869-875. DOI: 10.1016/j.bbalip.2009.04.006 [details]
- Bargmann, B. O. R., Laxalt, A. M., ter Riet, B., Testerink, C., Merquiol, E., Mosblech, A., ... Munnik, T. (2009). Reassessing the role of phospholipase D in the Arabidopsis wounding response. Plant, cell and environment, 32(7), 837-850. DOI: 10.1111/j.1365-3040.2009.01962.x [details]
- Bargmann, B. O. R., Laxalt, A. M., ter Riet, B., van Schooten, B., Merquiol, E., Testerink, C., ... Munnik, T. (2009). Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant and Cell Physiology, 50(1), 78-89. DOI: 10.1093/pcp/pcn173 [details] [PDF]
- Darwish, E., Testerink, C., Khalil, M., El-Shihy, O., & Munnik, T. (2009). Phospholipid signaling responses in salt-stressed rice leaves. Plant and Cell Physiology, 50(5), 986-997. DOI: 10.1093/pcp/pcp051 [details] [PDF]
- Mishkind, M., Vermeer, J. E. M., Darwish, E., & Munnik, T. (2009). Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. Plant Journal, 60(1), 10-21. DOI: 10.1111/j.1365-313X.2009.03933.x [details]
- Munnik, T., & Testerink, C. (2009). Plant phospholipid signaling: "in a nutshell". Journal of Lipid Research, 50(Supplement), S260-S265. DOI: 10.1194/jlr.R800098-JLR200 [details]
- Vermeer, J. E. M., Thole, J. M., Goedhart, J., Nielsen, E., Munnik, T., & Gadella (jr.), T. W. J. (2009). Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant Journal, 57(2), 356-372. DOI: 10.1111/j.1365-313X.2008.03679.x [details]
- Zonia, L., & Munnik, T. (2009). Uncovering hidden treasures in pollen tube growth mechanics. Trends in Plant Science, 14(6), 318-327. DOI: 10.1016/j.tplants.2009.03.008 [details]
- Gonorazky, G., Laxalt, A. M., Testerink, C., Munnik, T., & de la Canal, L. (2008). Phosphatidylinositol 4-phosphate accumulates extracellularly upon xylanase treatment in tomato cell suspensions. Plant, cell and environment, 31(8), 1051-1062. DOI: 10.1111/j.1365-3040.2008.01818.x [details]
- Testerink, C., Larsen, P. B., McLoughlin, F., van der Does, D., van Himbergen, J. A. J., & Munnik, T. (2008). PA, a stress-induced short cut to switch-on ethylene signalling by switching-off CTR1? Plant Signaling & Behavior, 3(9), 681-683. [details] [PDF]
- Zonia, L., & Munnik, T. (2008). Still life: Pollen tube growth observed in millisecond resolution. Plant Signaling & Behavior, 3(10), 836-838. [details] [PDF]
- Zonia, L., & Munnik, T. (2008). Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. Journal of Experimental Botany, 59(4), 861-873. DOI: 10.1093/jxb/ern007 [details] [PDF]
- Kusano, H., Testerink, C., Vermeer, J. E. M., Tsuge, T., Shimada, H., Oka, A., ... Aoyama, T. (2008). The Arabidopsis Phosphatidylinositol Phosphate 5-Kinase PIP5K3 is a key regulator of root hair tip growth. The Plant Cell, 20(2), 367-380. DOI: 10.1105/tpc.107.056119 [details] [PDF]
American Society for Plant Biologists
Associate Editor of the journal 'Plant Physiology"