dhr. dr. T. (Teun) Munnik
Faculteit der Natuurwetenschappen, Wiskunde en Informatica
Swammerdam Institute for Life Sciences
Science Park A
Science Park 904 Kamernummer: C2.212
1000 BE 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 changes in their environment. Such changes are experienced as stress, which can be biotic- (e.g. pathogens, herbivores) or abiotic stress (e.g. cold, heat, salinity, drought). Our main focus is to understand the role of phospholipid-based signal transduction pathways in temperature- (cold, heat) and water stress (drought, salinity and hypoosmotic stress), and during plant-pathogen interactions (see below).
Research in the lab of Plant Cell Biology is focussed on the role of phospholipids in Plant Cell Signalling and Development. Especially, phosphatidic acid (PA), DGPP and polyphosphoinositides, like PIP and PIP2, have our interest. These molecules are present at very low concentrations in cellular membranes and are rountinely missed by HPLC and MS analyses, simply because structural lipids, such as PC, PE, PI and PG, that make up the mass of all membranes, are too abundant. Nonetheless, these minor signalling lipids can easily be picked up by 32Pi-labelling (see TECHNIQUES), because their turnover is much faster than structural phospholipids and because they are synthesised via lipid kinases which use ATP that is one of the first compounds to be labelled. The key players involved in their metabolism are depicted in the scheme above. Routinely, this involves PLC-and PLD signalling cascades and a variety of lipid and inositolphosphate kinases. PA can be generated through both PLC- and PLD pathways, likely at different locations and in response to different stimuli resulting in different outputs.
32Pi-labelling and TLC
Phospholipids are routinely analysed using in vivo 32P-orthophosphate (32Pi)-labelling. In general, cells-, seedlings- or tissues like 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 vs mass levels). To monitor PLD activity in vivo, transphosphatidylation assays are conducted, which uses primary alcohols as substrate (see 'All Publications' ref 9, 18). Shown is an example of the green alga Chlamydomonas. Cells were prelabelled for 4 hrs and then stimulated for 5 min in the presence and absence of a low concentration of a primary alcohol that cells don't mind. Lipids were then extracted and chromatographed using an Ethylacetate TLC system that separates phosphatidylalcohols from other phospholipids (panel a). PLD catalyses the transphosphatidylation so the production of 32P-labelled phosphatidylalcohols is a relative measure for in vivo PLD activity. Autoradiography visualises their positions while PhosphoImaging is used for their quantification. As such, we have shown that PLD is activated in response to various environmental stresses, including, heat, drought, salt, and in response to pathogens. Arabidopsis contains 12 PLDs, rice 17. We are still investigating which PLD does what.
Using time-course experiments, the timing and duration of PLD activation can be established. Similarly, the activation of PLC, and PI-, PIP-, DAG- and PA kinase can be analysed. For this, lipids are chromatographed by an Alkaline TLC system that separates each of the phospholipids (panel b). Note the hydrolysis of PIP2 (PtdInsP2) within 15 sec to produce DAG that is converted to PA by DAG kinase. PI- and PIP-kinase activities also increase to maintain PIP2 levels. Since PLC is down regulated before these lipid kinases are, PIP and PIP2 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. Note that 'land plants' contain 30- 100- fold lower levels of PIP2 that Chlamydomonas or animal cells. This discrepancy has majoy consequences for the interpretatiuon of lipid signalling in plants and what PLC takes as substrate in vivo (see ref. 70).
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, 84) and in response to cold stress (ref 80).
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 PI3P (ref 28), PI4P (ref 62), PI(4,5)P2 (ref 55), PI(3,5)P2 (ref 107) and DAG (ref 106). We are still working on PA sensors. The one published for Spo20 does not work in our hands (ref 106). Biosensor lines are shared with whoever wants them.
Arabidopsis T-DNA insertion mutants
Using T-DNA insertion mutants, evidence for the participation of individual PLC, PLD and DGK in stress signalling- and development is investigated. Arabidopsis contains 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 too. For most of them we have mutants, which we are happy to share with other labs.
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). (ref 63)
LIPID SIGNALLING DURING PLANT STRESS & DEVELOPMENT
Role of Phospholipids in Membrane Trafficking
Polyphosphoinositides play distinct roles in membrane trafficking. This is examplified during cell divison, where PI3P, PI4P and PI(4,5)P2 exhibit distinct roles in generating a new membrane and cell wall for the seperating mother cell into two daughter cells, were the respective lipids were followed via genetically-encoded biosensors (green YFP or red mRFP for PI4P). The lipophylic dye, FM4-64 was used to stain membranes in general (red). While PI3P accumulates vesicles (late endosomes) surrounding the cell plate and is never part of the new plasma membrane (panel C), PI4P and DAG are always on the plasma membrane, right from the start when it is build (panel B, D), whereas PI(4,5)P2 is only present at the leading edges of the forming cell plate (A).
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 stressresponses involve not only salinity, or drought but also hypotonic stress . Using 32Pi-labelling, specific PA and PPI responses have been uncovered (18, 21, 26, 29, 30, 40, 55). For the PPIs, different isomers are involved, which can be analyzed by HPLC using a strong anion-exchanger after deacylation, generating so-called GroPIns' (see HPLC profile below).
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 which isoenzymes and genes involved (63; Zarza et al., 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 of diacylglycerol (DAG) into PA via DAG kinase (DGK). PLD generates PA directly by hydrolyzing structural pospholipids, such as phosphatidylcholine (PC). 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 genetically using the model system, Arabidopsis thaliana .
Arabidopsis contains 9 PLCs, 7 DGKs and 12 PLDs. To identify the genes involved in plant defence and characterise their individual functions, T-DNA insertion lines of most genes have been 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 against avirulent Pseudomonas.
Pollen Tube Growth
Work from Dr. Laura Zonia has been focussing on one of the fastest growing cells on this planet, pollen tubes. The goal of this research is to identify key information cascades that control pollen tube growth and to understand how these networks link to the biomechanics that drive cell elongation. Severalkey cascades were identified, including actin cytoskeleton, ion fluxes and various 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 indicates 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 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 of pollen 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)
Signalling Enzymes with Special Attention:
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. Cold stress rapidly triggers PA formation via DGK within minutes (ref 107).
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 present in all other PI-PLCs. In mammalian cells, PLCζ is specifically 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
- Number of publications in international refereed journals according to WoS: 117
- Number of citations according to WoS: 7920
- Average citations per item: 67
- H-index: 54 (Oct 9, 2018)
1. De Nobel JG, Munnik T, Priem J, van den Ende H, Klis FM. (1990) Conditions for increased cell wall porosity in Yeast. Proceedings 3rdNetherlands Biotechnology Congress, Amsterdam, April 3-4, 1990. H Breteler, RF Beudeker and KChAM Luyben (Eds), pp. 300-304.
2. De Vrije T. & Munnik T. (1998) Signal Transduction pathways and senescence. In: The Post-Harvest Treatment of Fruit and Vegetables - Current Status and Future prospects. Eds. Woltering EJ, Gorris LG, Jongen WMF, McKenna B, 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).
3. Testerink C. & Munnik T. (2004) Plant response to stress: phosphatidic acid as a second messenger. In Encyclopedia of Plant & Crop Science(RM Goodman, ed.), Marcel Dekker Inc, New York, 995-998.
4. De Wit PJGM, Brandwagt BF, van den Burg HA, Gabriëls SHEJ, van der Hoorn RAL, de Jong CF, van ‘t Klooster JW,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, Tikhonovich I, Lugtenberg B, Provorov N (Eds.), International Society for Molecular Plant-Microbe Interactions, St. Paul, Minnesota, USA, pp. 203-207.
5. 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 (Majunder AL and Biswas BB, eds.), Kluwer/Plenum Publishers, London, UK, pp207-237.
6. Lee Y, Munnik T, Lee Y (2010) Plant Phosphatidylinositol 3-kinase. In Lipid Signaling in Plants. Series: Plant Cell Monographs, Vol. 16, Munnik, T. (Ed.), Springer-Verlag, Heidelberg, Germany, pp95-106.
7. Arisz SA and Munnik T. (2010) Diacylglycerol kinase. InLipid Signaling in Plants. Series: Plant Cell Monographs, Vol. 16, Munnik, T. (Ed.), Springer-Verlag, Heidelberg, Germany, pp107-114.
8. 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.), Springer-Verlag, Heidelberg, Germany, pp185-199.
9. Munnik T. (2014) PI-PLC: Phosphoinositide-phospholipase C in plant signaling. In: Phospholipases in Plant Signaling. Wang X. (Ed.), Signaling and Communication in Plants 20, Springer-Verlag, Berlin Heidelberg. pp 27-54.
Phospholipid signalling; Signal transduction; Membrane trafficking; Stress signalling (cold, heat, drought, salt, pathogen); biochemistry; cell biology; molecular biology; genetics, physiology
- Associate Professor Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam (2016-present).
- Associate Editor Plant Physiology, section Signaling & Responses (2013 - present)
- 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 (2005-2016).
- 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 & Ben Cornelissen, Lipid signalling in 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%) University of Amsterdam, 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)
- BSc - Botany, University of Applied Sciences, Ir. W. van den Broek Institute, Amsterdam, The Netherlands (1988)
- Associate Editor Plant Physiology, section Signaling & Response
- Referee for: Nature, Nature Cell Biol, Nature Immunol, Science, PNAS, Current Biology, 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, eLife.
- Evaluation panels: NWO-ALW (panel member MtC; VIDI), NWO-CW (panel member ECHO, TOP), ERC (EU), USDA (US), NIH (US), BBSRC (UK), CNRS (Fr), ISF (Isr) AACF (Can) DFG (Ger).
- PhD thesis committees: 30
- Member, secretary and chair NWO-CW study group, Lipids & Membranes (2005-2008)
- Expert Evaluator ERC >2014
• 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)
• NWO-DBT grant (2015-2020)
• ECHO grant (2018-2021)
• IXA grant (2018)
Publications: (see All Publications)
• Number of publications in international refereed scientific journals according to WoS: 117
• Contributions to books:
- 2 books (Ed. 2010; Ed. 2013, both Springer);
- 7 chapters
• Number of citations according to WoS: 7921; average citations: 67; H-index: 54
• Lecturer at various International Advanced Courses (e.g. ICRO; FEBS, EPS, UNMP, TWAS)
• Coordinator and teacher of various BSc, MSc and PhD courses (molecular cell biology, biochemistry, cellular physiology, plant-abiotic stress)
• >145 Invited seminars at (inter)national universities, conferences and symposia, world wide (see below).
• Organiser of internal seminars for SILS, Green Life Sciences, and Plant Sciences at the University of Amsterdam
• Conference chair of numerous national- and international conferences
• Organiser and chair of Gordon Research Conference (GRC) Salt and Water Stress 2012, Hong Kong, China.
- Lipids: Building plant tolerance to environmental stress. Plantum Matchmaking, Sept 20, De Meern, The Netherlands
- PIP2 Signalling in Plants. Invited seminar Eidgenössische Technische Hochschule (ETH) Zürich, Feb 22, Zürich, Switzerland.
- Phospholipid Signalling in Plant Stress & Development. Syngenta,Feb 27, Stein, Switzerland.
- Phosphoinositide Signalling in Plant Stress & Development. University of London,Royal Halloway, April 30, London, UK.
- Osmotic Stress Triggers PIP2Signalling by Activation of Arabidopsis PIPK7 and PIPK9. Gordon Research Conference on Salt & Water Stress in Plants. June 3-8, Waterville Valley, NH, USA.
- Heat Stress-Activated Lipid Signalling. Biannual International Plant Thermomorphogenesis Meeting, 27‐29 August, Utrecht, The Netherlands.
- New Roles for PLC in Plant Stress & Development. GRC on Plant Lipids: Structure, Metabolism & Function. Jan 29-Feb 3, Galveston, Texas, USA.
- Lipid signals greasing stress- and developmental responses in plants. Invited seminar, University of Geneva, March 22, Geneva, Switzerland.
- New Roles for PPIs in Plant Development and Stress Signalling. The Yucatan Center for Scientific Research (CICY), June 12-14, Merida, Mexico.
- Phospholipid Signaling in Plant Stress & Development. Plant Biology 2017 (ASPB), June 24-28, Honalulu, Hawaii, USA.
- PIP2 Signalling in Plants. Invited seminar ETH Zürich, Oct 26, Zürich, Switzerland.
- Phospholipid signalling in plant stress & development. Invited seminar. University of Ghent, Feb 10, Ghent, Belgium.
- Phospholipid signals in plant stress and development. Invited seminar Institute for Bioscience and Biotechnology Research, Department of Plant Sciences and Landscape Architecture, University of Maryland, March 31, Rockville, MD, USA.
- Phosphoinositides - lipid signals in plant stress and development. Invited seminar, University of Lausanne. Juli 15, Lausanne, Switzerland.
- Shining light on 'plant PLC signalling' Gordon Research Conference (GRC) on Plant Lipids: Structure, Metabolism, and Function, Feb 1-6, Galveston, TX, USA.
- Lipid Signals at Work. Texas A&M University, Feb 6, College Station, TX, USA
- Phospholipids in plant stress signalling and development. Feb 9, University of Arizona, Tempe, AZ, USA.
- Polyphosphoinositide signaling in plant stress & development. Invited speaker at 3rd SPOT-ITN conference on "Stress Biology and Crop Fertility", March 18 - 22, Sorrento, Italy.
- Phospholipid signalling in plant stress & development. Invited seminar. Shanghai Center for Plant Stress Biology (PSC). May 12, Shanghai, China.
- Phospholipid signalling in plant stress & development. Invited seminar. Shanghai Institute of Plant Physiology and Ecology (SIPPE), Chinese Academy of Science (CAS), May 13, Shanghai, China.
- Phospholipid signalling in plant stress & development. Invited seminar. College of Life Science, Nanjing Agricultural University, May 15, Nanjing, China.
- Green Light for Lipid Second Messengers in Plants. Invited speaker at Biochemical Society/FEBS Signalling 2015 - Cellular functions of phosphoinositides and inositol phosphates. Sept 1-4, Robinson College, Cambridge, UK.
- Phospholipid Signaling in Plant Stress & development. Invited seminar. UNAM, Oct 19, Mexico City, Mexico.
- Phospholipid Signaling in Plant Stress & development. Invited seminar. Universidad Autónoma de Nuevo León, Oct 20-21, Nuevo León, Monterrey, Mexico.
- Green Light for Lipid Second Messengers in Signalling Stress & Development. Centro de Investigacion Cientifica de Yucatan (CICY), Oct 23, Merida, Mexico.
- Phospholipid-based Signalling in Plant Stress & Development. Invited speaker. 6th International Singapore Lipid Symposium (Nov 30-Dec 2) and 6th Asian Symposium on Plant Lipids, Dec 2-4, Singapore.
- Phospholipid signals in plant stress and development. Invited seminar at Centre of the Region Hana for Biotechnological and Agricultural Research, Palacky University Olomouc, March 25, Olomouc, Czech Republic.
- Polyphosphoinositides – molecular beacons in plant membranes. Invited seminar, Academy of Sciences of the Czech Republic. March 27, Prague, Czech Republic.
- Phospholipid signalling in salt- and water stress. COST FA0901 Conference: Putting Halophytes to Work - From Genes to Ecosystems, April 9-10, Coimbra, Portugal.
- Role of polyphosphoinositides in auxin signalling. Auxentric 2014 – 3rd International Meeting on Early Auxin Research. May 23-25, Norwich, UK.
- Salt stress triggers distinct PI4P- and PI(4,5)P2 responses at the plasma membrane of Arabidopsis thaliana. Gordon Research Conference on Salt & Water Stress in Plants. Aug 3-8, Newry, ME, USA.
- Polyphosphoinositide signalling in plants. University of Barcelona. Sept 5, Barcelona, Spain.
- Phospholipid signaling in plant stress & development. Invited seminar at section Molecular Physiology of Plants and Micro-organisms, Catholic University of Leuven, Nov 19, Leuven, Belgium.
- PIP2 Signaling in Plant Stress and Development. Invited seminar at Institute of Life Sciences, Université Catolique de Louvain (UCL), Nov 20, Louvain-la-Neuve, Belgium.
- Visualizing phospholipid signals in plants. Gordon Research Conference (GRC) on Plant Lipids: Structure Metabolism and Function. Jan 26 - Feb 1, Galveston, TX, USA.
- 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 & development. Invited seminar Agrobios, Sept 23, Metaponto, Italy.
- 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. Keynote lecture 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 of México (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 is believing'. 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.
- Phospholipid signalling 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 D signaling 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.
Currently, there are no vacancies
For personal fellowship applications:
(e.g. FEBS, EMBO, Marie Curie) - please contact: t.munnik @ uva.nl
Phosphatidic acid (PA) and polyphosphoinositides (PPIs) are minor phospholipids in biological membranes that function as cellular signalling molecules at very low concentrations. Their turnover is much faster than of structural phospholipids and levels quickly change in response to biotic- (pathogens) and abiotic- (salt, cold, heat, drought) stresses. How this is regulated and where this occurs in the cell (e.g. plasma membrane, ER, Golgi) or in the whole plant (e.g. root, stem, stomata) has our particular interest. The genome of the model plant system Arabidopsis thaliana, encodes genes for various lipid kinases, phosphatases and phospholipases, and by using T-DNA insertion knock-out mutants, overexpression lines, and FP fusions, we are pinpointing their individual contribution in stress and/or development. Over the years we constructed various lipid biosensor lines, which are plants expressing specific lipid-binding domains that are fused to a fluorescent protein that are used to study the dynamics of lipid-second messengers in living cells. Personal felowships or students can be involved in any of the projects.
- Arabidopsis physiology (development, biotic/abiotic stress)
- Cell biology (development, biotic/abiotic stress, mutants, FP-tagged kinases, lipases & targts, lipid biosensors, phosphomimetics)
- Radiolabelling & Lipid biochemistry (TLC, HPLC, GC, liposoimes, fat blots)
- Molecular cloning (promoter analysis, fusion proteins, gene silencing, overexpression)
- RNA/DNA (e.g . q/RT-PCR, RNA-Seq)
- Protein (extraction, SDS-PAGE, Western, IP, Mass Spec, enzyme kinetcs, lipid targets, lipid binding)
- Confocal Imaging
SILS - Plant Cell Biology
Teun Munnik (PI)
Ringo van Wijk (Lab manager)
Xavier Zarza (Post-doc)
Femke de Jong (Post-doc)
Steven Arisz (senior Post-doc)
Max van Hooren (PhD student)
Ruud Korver (PhD student)
Safrina Ahmad (PhD student)
Jack Dickenson (MSc student)
Eveline Bosman (BSc student)
Michael Mishkind (permanent guest)
Essam Darwish (guest)
Nazish Annum (guest)
Laura Zonia (Washington University in St. Louis, MO, USA)
Aleksandra Haduch (PhD student, Poland)
Wendy Roels (Naktuinbouw)
Dörte Klaus (PD, Toulouse, F)
Christiane Unger (MSc, Halle, Germany)
Alan Musgrave (UvA, retired)
Ana Laxalt (PI, Mar del Plata, Argentina)
Bas ter Riet (Enza Zaden, Enkhuizen, NL)
Harold Meijer (WUR, Wageningen, NL)
Christa Testerink (Prof. Plant Physiology, WUR)
Wessel van Leeuwen (Hazera Seeds, 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 (Uni of Mar del Plata, Argentina)
Martine den Hartog (Covidien, Amsterdam)
Arnold van der Luit (Oncodesign, France)
Bastiaan Bargmann (CA, USA)
Bas van Schooten (NWO)
Essam Darwish (Uni. Cairo, Egypt)
Joop Vermeer (Prof. Plant Cell Biology, Uni of Zürich, Switzerland)
Muhammad Shahbaz (Prof. Uni of Faisalabad, Pakistan)
Qianqian Zhang (Nikon, Shanghai, China)
Jessica Meyer (technician WUR)
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
Martijn van Ophem
Rui Alvez (Erasmus student)
Babette Vlieger (BSc student)
Ludo Cialdella (BSc student)
Dr. Michael Mishkind (NSF, VA, USA)
Dr. Ana Laxalt (Mar del Plata, Argentina)
Dr. Joachim Goedhart (WU, Wageningen)
Dr. Dorus Gadella (WU, Wageningen)
Dr. Bas Tomassen (Erasmus Rotterdam, NL)
Dr. Katie Anne Wilkins (Birmingham, UK)
Dr. Anne Sophie Leprince (Paris, France)
Dr. Noam Reznik (Tel Aviv, Israel)
Dr. Magdalena Wierzchowiecka (Poland)
MSc. Özgecan Tanyolaç (Izmir, Turkey)
MSc. Maria Alejandra Schlöffel (University of Tübingen, Germany)
Dr. Bojan Gujas (ETH, Zürich, Switzerland)
Dr. Necla Pehlivan (Turkey)
Dr. Theodora Farmaki, (Thessaloniki, Greece)
Dr. Wojciech Rymaszewski (Warsaw, Poland)
Dr. Hui-fen Kuo (Academia Sinica, Taiwan)
MSc. Kelly Stecker (University of Wisconsin, USA)
Dr. Muhammad Jamil (WUR)
MSc Madiha Butt (Faisalabad, Pakistan)
Dr. Tomoko Hirano (Kyoto Prefectural University, Japan)
Dr. Jyothilakshmi Vadassery (Max Planck, Germany)
MSc. Dominik Novák (Palacky University, Olomouc, Czech Republic)
Dorus Gadella (SILS, UvA, NL)
Nullin Divecha (Manchester, UK)
Mats Ellerström (Göteborg University, Sweden)
Takashi Aoyama (Kyoto University, Japan)
Erik Nielsen (Michigan, US)
Ana Laxalt (University of Mar del Plata, Argentina)
Charles Brearley (Norwich, UK)
Chris de Koster (SILS, UvA, NL)
Ingo Heilmann (Halle, Germany)
Robin Irvine (Cambridge, UK, retired)
Laura de la Canal (Mar del Plata, Argentina)
Nick Ktistakis (Cambridge, UK)
Ralf Oelmüller (Jena, Germany)
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 Republic)
Ingo Heilmann (Halle, Germany)
Jörg Kudla (Münster, Germany)
Bert de Boer (VU, Amsterdam)
Silke Robatzek (Münich, Germany)
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)
Tzyy-Jen Chiou (Academia Sinica, Taiwan)
Libo Shan (Texas A&M University, US)
Ping He (Texas A&M University, US)
Glenda Gillaspy (Virginia Tech, US)
Yee-yung Charng (Academia Sinica, Taiwan)
Taijoon Chung (Pusan National University, Republic of Korea)
Jenny Russinova (VIB, Ghent University, Belgium)
Gabriel Schaaf (University of Bonn, Germany)
Luis Lopez-Molina (University of Geneva, Switzerland)
Antia Rodriguez-Villalon (ETH, Zürich, Sitzerland)
Christian S. Hardtke (Lausanne, Sitzerland)
Niko Geldner (Uni Lausanne, Sitzerland)
Joop Vermeer (Uni Zürich, Sitzerland)
Wybren Jan Buma (HIMS,Molecular photonics UvA)
Jan van Maarseveen (HIMS, Organisc chemistry, UvA)
Jiri Friml (IST Austria)
- Zhang, Q., van Wijk, R., Shahbaz, M., Roels, W., van Schooten, B., Vermeer, J. E. M., ... Munnik, T. (2018). Arabidopsis Phospholipase C3 is Involved in Lateral Root Initiation and ABA Responses in Seed Germination and Stomatal Closure. Plant and Cell Physiology, 59(3), 469–486. . DOI: 10.1093/pcp/pcx194 [details]
- Lee, H. N., Zarza, X., Kim, J. H., Yoon, M. J., Kim, S-H., Lee, J-H., ... Chung, T. (2018). Vacuolar Trafficking Protein VPS38 Is Dispensable for Autophagy. Plant Physiology, 176 (2), 1559–1572. DOI: 10.1104/pp.17.01297 [details]
- Szymanski, D., Bassham, D., Munnik, T., & Sakamoto, W. (2018). Cellular Dynamics: Cellular Systems in the Time Domain. Plant Physiology, 176(1), 12-15. DOI: 10.1104/pp.17.01777 [details]
- Wu, C., Tan, L., van Hooren, M., Tan, X., Liu, F., Li, Y., ... Bao, Y. (2017). Arabidopsis EXO70A1 recruits Patellin3 to the cell membrane independent of its role as an exocyst subunit. Journal of Integrative Plant Biology, 59(12), 851-865. DOI: 10.1111/jipb.12578 [details]
- D'Ambrosio, J. M., Couto, D., Fabro, G., Scuffi, D., Lamattina, L., Munnik, T., ... Laxalt, A. M. (2017). Phospholipase C2 Affects MAMP-Triggered Immunity by Modulating ROS Production. Plant Physiology, 175(2), 970-981. DOI: 10.1104/pp.17.00173 [details]
- Gujas, B., Cruz, T. M. D., Kastanaki, E., Vermeer, J. E. M., Munnik, T., & Rodriguez-Villalon, A. (2017). Perturbing phosphoinositide homeostasis oppositely affects vascular differentiation in Arabidopsis thaliana roots. Development - The Company of Biologists, 144(19), 3578-3589. DOI: 10.1242/dev.155788 [details]
- Vermeer, J. E. M., van Wijk, R., Goedhart, J., Geldner, N., Chory, J., Gadella, T. W. J., & Munnik, T. (2017). In Vivo Imaging of Diacylglycerol at the Cytoplasmic Leaflet of Plant Membranes. Plant and Cell Physiology, 58(7), 1196-1207. DOI: 10.1093/pcp/pcx012 [details]
- Hirano, T., Stecker, K., Munnik, T., Xu, H., & Sato, M. H. (2017). Visualization of Phosphatidylinositol 3,5-Bisphosphate Dynamics by a Tandem ML1N-Based Fluorescent Protein Probe in Arabidopsis. Plant and Cell Physiology, 58(7), 1185-1195. DOI: 10.1093/pcp/pcx011 [details]
- Zarza, X., Atanasov, K. E., Marco, F., Arbona, V., Carrasco, P., Kopka, J., ... Alcázar, R. (2017). Polyamine Oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant, cell and environment, 40(4), 527–542 . DOI: 10.1111/pce.12714 [details]
- Meijer, H. J. G., van Himbergen, J. A. J., Musgrave, A., & Munnik, T. (2017). Acclimation to salt modifies the activation of several osmotic stress-activated lipid signalling pathways in Chlamydomonas. Phytochemistry, 135, 64-72. DOI: 10.1016/j.phytochem.2016.12.014 [details]
- Di Fino, L. M., D'Ambrosio, J. M., Tejos, R., van Wijk, R., Lamattina, L., Munnik, T., ... Laxalt, A. M. (2017). Arabidopsis phosphatidylinositol-phospholipase C2 (PLC2) is required for female gametogenesis and embryo development. Planta, 245(4), 717-728. DOI: 10.1007/s00425-016-2634-z [details]
- Hirano, T., Munnik, T., & Sato, M. H. (2017). Inhibition of phosphatidylinositol 3,5-bisphosphate production has pleiotropic effects on various membrane trafficking routes in Arabidopsis. Plant and Cell Physiology, 58(1), 120-129. DOI: 10.1093/pcp/pcw164 [details]
- Dejonghe, W., Kuenen, S., Mylle, E., Vasileva, M., Keech, O., Viotti, C., ... Russinova, E. (2016). Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification. Nature Communications, 7, . DOI: 10.1038/ncomms11710 [details]
- Putta, P., Rankenberg, J., Korver, R. A., van Wijk, R., Munnik, T., Testerink, C., & Kooijman, E. E. (2016). Phosphatidic acid binding proteins display differential binding as a function of membrane curvature stress and chemical properties. Biochimica et Biophysica Acta, 1858(11), 2709-2716. DOI: 10.1016/j.bbamem.2016.07.014 [details]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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]
- 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., & Lee, Y. (2010). Plant phosphatidylinositol 3-kinase. In T. Munnik (Ed.), Lipid signaling in plants (pp. 95-106). (Plant cell monographs; Vol. 16). Heidelberg: Springer. 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]
- 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]
- 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, 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]
- Zonia, L., & Munnik, T. (2008). Still life: Pollen tube growth observed in millisecond resolution. Plant Signaling & Behavior, 3(10), 836-838. [details]
- 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]
- 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]
American Society for Plant Biologists
Associate Editor of the journal 'Plant Physiology"