Phospholipid Signalling in Plant Stress & Development

Plants cannot run away from stress! Whenever it get's cold, too hot, or if there is no water (drought), they have to deal with the conditions themselves. Luckily, millions of years of evolution, plants have evolved various smart strategies to quickly respond to stress and deal with the specific changes in its environment. The main interest of Plant Cell Biology within the  Green Life Science Cluster, is to unravel the molecular mechanisms by which plant cells perceive environmental stress, how these signals are intracellularly transduced, and how they are converted into appropriate responses that allow plants to deal with the particular stress. We are specifically interested in the early signalling pathways that report temperature stress (cold, heat), water stress (drought, salinity, hypo-osmotic stress), and microbes (pathogens, symbionts), in particular, in the role of membranes and the participation of certain lipids in the signal transduction process.

 

PHOSPHOLIPID SIGNALLING 

PLC- & PLD signalling

Research at Plant Cell Biology is primarily focussed on phospholipid signalling during Plant Stress & Development. Especially, the lipid second messengers  PA, DGPP  and polyphosphoinositides (PPIs), like PIP and PIP₂ have our interest. Such molecules are present at relatively low concentrations in membranes and most are rountinely missed by common lipidomic analyses. Nonetheless, they can be easily monitored by labelling cells or tissues with radioactive ³²P_i in vivo, because the turnover of signalling lipids is much faster than of structural phospholipids, and because they are synthesised via kinases that use ATP, which is one of the first compounds to be labelled. Key players in PA and PPI metabolism and signalling are depicted in the scheme above, involving PLC-and PLD signalling and a variety of lipid- and inositolphosphate kinases (e.g. DGK, PI4K, PIP5K, and IPKs). Note that PA can be generated through both PLC- and PLD pathways, which occurs at different cellular- and subcellular locations, and in response to different stimuli, resulting in different outputs.

PI3K signalling

Another important signalling route concerns PPIs that are phosphorylated at the D3-position of the inositol ring. PI is then phosphorylated by a specific PI3K (called VPS34) to form the PIP isomer, PI3P, which plays crucial roles in endomembrane trafficking to the vacuole and in autophagy. PI3P can be further phosphorylated by PI3P 5-kinases (FAB1-4) to form the lipid second messenger, PI(3,5)P₂, which is also involved in membrane trafficking and is activated during osmotic stress.  

Detection of PPIs, PA & DGPP

These signalling lipids are routinely analysed using in vivo ³²P_i-labelling. Cells-, seedlings- or tissues (e.g. leaf discs) can be used with labelling times varying from minutes to hrs or 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 includes  the addition of a primary alcohol  (see 'All Publications' ref 9, 18). An example with the green alga Chlamydomonas is shown, where cells were prelabelled for 4 hrs and then  stimulated for 5 min in the presence or absence of a low concentration of a primary alcohol (methanol, ethanol, propanol, or butanol) that cells don't mind. Extracted lipids were then chromatographed using a TLC solvent that  separates  phosphatidylalcohols from the rest of the phospholipids (panel a). PLD catalyses the transphosphatidylation, so the production of ³²P-phosphatidylalcohol is a relative measure for in vivo PLD activity. PhosphoImaging can be used for their visualization and quantification. We found that PLD is activated by various environmental stresses, including, heat-, drought-, and salt stress, and also by certain pathogens. The genome of Arabidopsis encodes for 12 PLD genes, while rice even rice 17, and this  is in huge contrast to e.g. humans, which only contain two PLDs. We are investigating which PLD does what. 

Similarly, the activation of PLC, and PI-, PIP-, DAG- and PA kinases can be monitored. For this, lipids are chromatographed with another TLC solvent (panel b). As example, the timing and duration of the activation was performed using a time-course experiment. Note the PLC hydrolysis of PIP₂ (PtdInsP₂) within 15 sec to produce InsP₃ and DAG, with the latter being converted into PA by DAG kinase (DGK). PI- and PIP-kinase are also activated to replenish the PIP- and PIP₂ levels. Since PLC is down regulated before the lipid kinases are, a slight overshoot in PIP and PIP₂ production is witnessed. In the same time frame, PA signalling is being attenuated by converting it into DGPP by PA kinase (PAK). The formation of DGPP starts again a new signal.  

Higher plant cells contain minute amounts of PIP₂

Over the years, we discovered that 'flowering plants' contain 30-100 fold lower PIP₂ levels than Chlamydomonas or animal cells. This discrepancy has major consequences for the interpretation of plant PLC signalling  and what it uses as in vivo substrate (see ref. 70), i.e. PI4P rather than PI(4,5)P₂.

Distinghuising between PA_DGK and PA_PLD 

Both PLD and DGK can generate PA as second messenger. To distinguish between both pools, a Differential Labelling Protocol was developed. It uses a difference in kinetics by which PA can become radioactive. Relatively short labelling times are required for PA_DGK while long labelling is needed for PA_PLD, This is because DGK requires ATP to make PA, and ATP is one of the first components to become labelled when cells are incubated with ³²P_i. In contrast, PLD requires  ³²P-labelled structural lipids like PE to generate ³²P-PA, and this takes hours of metabolic labelling (panel top). Moreover, using the transphosphatidylation assay, one can check how long ³²Pi-prelabelling is required before structural phospholipids would generate ³²P-PBut, and thus ³²P-PA_PLD.

The TLC panels (A-D) show what happens in Chlamydomonas cells that were metabolically labelled with ³²P_i for the times indicated (min-> hrs), and subsequently treated for 1 min with buffer  (control; panel A, B) or a stimulus (in this case  1 µM mastoparan  (panel C, D), both in the presence of 0.1 % n-butanol to monitor PLD activity. Extracted lipids were split  and either seperated on EtAc TLC (A, C) to separate the PLD-catalyzed PBut, or Alkaline TLC (B, D) to visualize the rest of the phospholipids, including PA and its phosphorylation into DGPP.

The point is that all cells were treated for exactly the same time period (1 min) but that PBut will only became radioactive when its substrate (i.e. PE) became labelled (>40min). The same would hold for the PA_PLD. In contrast, PA_DGK would receive its label from ATP, and since this compound  is labelled within sec, a much faster increase in ³²P-PA would be witnessed if  PLC/DGK was involved. Since PA kinase also uses ATP, a similar response in DGPP can be expected (panel D). Since the specific radioactivity of ³²P-ATP decreases over time, the 1-min response decreases concomitantly.  The combined assay  is a relative qualitative measure and provides evidence  for PA coming through eeither DGK- and/or PLD pathways. See details in Arisz et al. , 2009 (Ref 68, 84) and  the DGK-specific response to cold stress (ref 80).

Monitoring Lipid Signalling in vivo - Lipid Biosensors

To visualize lipid signalling with confocal imaging, we developed various lipid biosensors. These are genetically encoded lipid-binding domains fused to a Fluorescent-Protein (FP), which can be expressed in cell suspensions or whole plants. The first example, was generated in 2006  for PI3P in tobbaco cells and whole Arabidopsis plants.  This was followed with PI(4,5)P₂ (2007), PI4P (2009), PI(3,5)P₂ (2016), DAG (2017) and PA (2023). In 2014, Yvon Jaillais' lab  (Lyon) added several colors to PI3P, PIP4 and PI(4,5)P₂ markers (ref), and made important new ones for PA and PS. All biosensor lines are publically available.

Connecting genes to function

Using T-DNA insertion KO and OE mutants of the model system Arabidopsis thaliana, the participation of individual PLCs, PLDs, PIP5Ks and DGKs in stress signalling & development is investigated. Arabidopsis contains 9 PLC-, 12 PLD- and 7 DGK genes. In addition, there are 11 PIP5K,  12 PI4K, 1 PI3K, 4 FAB and multiple  PA- and PPI phosphatase (e.g. SAC1-9) genes too. For many of them, we have  mutants that we are happy to share.

Below,  an example of reduced salt tolerance for 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

 

Dynamic Membranes

PPIs play distinct roles in membrane trafficking. This is examplified during cell divison, where PI3P, PI4P and PI(4,5)P₂ exhibit distinct patterns when the new plasma membrane and cell wall is formed, seperating the mother cell into two daughter cells, and the respective lipids were followed via our biosensors (green, YFP or red, mRFP for PI4P). The lipophylic dye, FM4-64 (red) was used to stain membranes in general. While PI3P (green) accumulates  in vesicles (late endosomes) that surround the cell plate, but is never part of the new plasma membrane (panel C), PI4P and DAG were always on the plasma membrane, right from the start when build (panel B, D). PI(4,5)P₂, however, is only present at the leading edges of the plasma membrane following the expanding cell plate (A).  

Temperature Stress: heat-PIP₂ & cold-PA

Heat stress induces an array of physiological adjustments that facilitate continued homeostasis and survival during periods of elevated temperatures. We discovered that plants rapidly produce PIP₂ within minutes of a sudden temperature increase. Using the PIP₂biosensor, we found that the PIP₂  is produced at the plasma membrane, nuclear envelope, nucleolus and at punctate cytoplasmic structures ( see below). Increases in steady-state levels of  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. ³²P-Pulse-labelling analyses revealed that the PIP₂ response is generated through activation of a PIP5K rather than an inhibition of a lipase or PIP₂ phosphatase (see ref 64, 69). Using T-DNA insertion KO mutants we are currenly identifying which of the 11 PIP5Ks is/are involved. The work involves a long-standing collanboration with Dr. Michael Mishkind (NSF).

Interestingly, in response to cold stress, PA is formed as a lipid second messenger (ref 80). Using a novel probe, we are currently aiming to discover novel PA targets than those we identified earlier (ref 41, 43, 45, 54, 56, 59, 79, 81, 95, 101)

Osmotic Stress- PA & PIP₂

Osmotic stress responses not only involves salinity and drought but also hypotonic stress . Using ³²P_i-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 lipid biosensors but also by HPLC analysis, using a strong anion-exchanger after deacylation, which generates the corresponding GroPIns' isomers  (see HPLC profile below).

Lipid biosensor lines are used to find out where lipid signals are generated (55) while KO mutants are used to pinpoint which isoenzymes and genes are involved (63; Zarza et al., 2019, 2020; in prep). 

Plant Defence

PLC and PLD signalling cascades can individually generate PA, an important eukaryotic lipid second messenger. PLC generates it indirectly via the hydrolysis of PI4P 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 KO or KD lines have been collected of most genes. Plants were then analysed for their disease resistance and sensitivity to virulent- and avirulent strains of the bacterial pathogen Pseudomonas syringae and the natural pathogen Hyaloperonospora parasitica , the causal agent of downy mildew. A DGK gene was found to be required for full resistance against virulent Pseudomonas and H. parasitica, while two PLD genes were found to be involved in the resistance against avirulent Pseudomonas (unpublished)

Pollen Tube Growth

Work from Dr. Laura Zonia focussed on one of the fastest growing cells of this planet: pollen tubes. The goal of the research was to identify the key cascades that control pollen tube growth and to understand how these networks link to the biomechanics that drive cell elongation. Several key 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. Common themes emerging across these information cascades are osmoregulation and cell volume status. Further work confirmed that  many of these networks indeed converge at this point, where we revealed that transcellular hydrodynamic flux drives the growth of a pollen tube 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

Diacylglycerol Kinase (DGK)

Accumulating evidence suggests that PA plays a pivotal role in the plant's response to environmental signals. Besides PLD, PA can also be generated by DGK. To establish which metabolic route is activated, a differential ³²P-labelling protocol can be used (see above). Based on this and on reverse-genetic approaches, DGK has taken center stage, next to PLD, as generator of PA in biotic- and abiotic-stress responses. The substrate, DAG is generally thought to be derived from PLC. The model plant system Arabidopsis thaliana contains 7 DGKs, two of which, AtDGK1  and AtDGK2, resemble mammalian DGKε, encoding a conserved kinase domain, a transmembrane domain and two C1 domains. The other DGKs have a simpler structure, lacking C1 domains, which appear absent in animals. Several protein targets that bind PA have been discovered (Testerink and Munnik, 2011). Whether PA comes from PLD or DGK often remains to be elucidated though. For cold stress, this is know, triggering PA via DGK within minutes (ref 107). Freezing (and thus wounding) involves multiple PLD (ref 63, 65).

Phospholipase D (PLD)

In comparison to mammals (which only two possess PLD) or yeast (one), plants contain multiple PLD genes. The genome of Arabidopsis thaliana counts 12 PLD family members and this diversity has been found in assorted higher plant species. Eukaryotic PLD enzymes are characterized by two highly conserved carboxy-terminal (C-terminal) catalytic domains and an amino-terminal (N-terminal) lipid-binding region (see 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) and 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 PI3P signaling. C2 domains also mediate the localization of soluble proteins to membranes by binding lipids in a Ca²⁺-dependent manner. The plant-PLD family can be  further subdivided into six classes,  based on sequence homology and in vitro activity. As such, Arabidopsis contains three α-, two β-, three γ-, one δ-, one ε- and two ζ-class PLD isoforms; the latter contain the PX and PH domains and share homology with the yeast and mammalian PLDs.  

Phospholipase C (PLC) 

PI-PLCs have been classified into six subfamilies, β, γ, δ, ε, η and ζ, based on 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-like, which is the class that lacks the Pleckstrin Homology (PH) domain present in all other PI-PLCs. In mammalian cells, PLCζ is specifically expressed in sperm cells.

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 unclear but may involve Ca²⁺. How plant PLCs are regulated is still completely unknown. Using KO mutants we found that various PLCs  are involved in lateral root formation and are predominantly expressed in or near the phloem. Overexpression of PLC leads to improved drought tolerance (Van Wijk et al., 2018; Zhang et al., 2018a,b).

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.

 

PUBLICATIONS

Books

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, Germany. 

Plant Lipid Signaling Protocols. Munnik T . and Heilmann I. ( Eds.) 2013. Series: Methods in Molecular Biology 1009, Humana Press, NJ, USA. 305 p.

 

 

International (peer reviewed) publications

• Number of publications in international refereed journals according to WoS: 134
• Number of citations according to WoS: 11400 (>5600 papers)
• Average citations per item: 83
• H-index: 59 (March, 2023)

 

134.   Li T, Xiao X, Liu Q, Li W, Li L, Zhang W Munnik T, Wang X, Zhang Q (2023). Dynamic responses of PA to environmental stimuli imaged by a genetically encoded mobilizable fluorescent sensor. Plant Commun. 4: 100500. 133.   Verslues PE, Bailey-Serres J, Brodersen C, Buckley TN, Conti L, Christmann A, Dinneny JR, Grill E, Hayes S, Heckman RW, Hsu PK, Juenger TE, Mas P, Munnik T, Nelissen H, Sack L, Schroeder JI, Testerink C, Tyerman SD, Umezawa T, Wigge PA. (2023) Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress. Plant Cell 35: 67-108 132.    Scholz P, Pejchar P, Fernkorn M, Škrabálková E, Pleskot R, Blersch K, Munnik T, Potocký M, Ischebeck T. (2022) DIACYLGLYCEROL KINASE 5 regulates polar tip growth of tobacco pollen tubes. New Phytol. 233: 2185-2202. 131.    Noack LC, Bayle V, Armengot L, Rozier F, Mamode-Cassim A, Stevens FD, Caillaud MC, Munnik T, Mongrand S, Jaillais Y (2022) A nanodomain anchored-scaffolding complex is required for PI4Kα function and localization in plants. Plant Cell 34: 302-332. 130.    Doumane M, Lebecq A, Colin L, Fangain A, Stevens FD, Bareille J, Hamant O, Belkhadir Y, Munnik T, Jaillais Y, Caillaud M-C. (2021) Inducible depletion of PI(4,5)P2 by the synthetic iDePP system in Arabidopsis. Nature Plant 7: 587-597. 129.    Aliche E, Talsma W, Munnik T, Bouwmeester H (2021) Characterization of maize root microbiome in two different soils by minimizing plant DNA contamination in metabarcoding analysis. Biol Fertil Soil. 57: 731-737. 128.    Hayes S, Schachtschabel J, Mishkind M, Munnik T, Arisz SA (2021) Hot Topic: Thermosensing in Plants. Plant Cell Environ. 44: 2018-2033. 127.    De Jong F. & Munnik T. (2021) Attracted to membranes - Lipid Binding Domains in Plants. Plant Physiol. 185: 707-723. 126.    Munnik T, Mongrand S, Zársky V and Blatt M (2021) Dynamic membranes - The indispensable platform for plant growth, signaling, and development. Plant Phys. 185: 547-549. 125.    Barajas-Lopez JD, Tiwari A, Zarza X, Shaw MW, Pascual JS, Punkkinen M, Bakowska JC, Munnik T, Fujii H. (2021) EARLY RESPONSE TO DEHYDRATION 7 remodels cell membrane lipid composition during cold stress in Arabidopsis. Plant Cell Physiol. 62: 80-91. 124.    Liu F, Hu W, Li F, Marshall RS, Zarza X, Munnik T, and Vierstra RD (2020) AUTOPHAGY-RELATED14 and its associated phosphatidylinositol 3-kinase complex promotes autophagy in Arabidopsis. Plant Cell 32: 3939–3960. 123.   Zarza X, Van Wijk R, Shabala L, Hunkeler A, Lefebvre M, Rodriguez-Villalón A, Shabala S, Tiburcio AF, Heilmann I, Munnik T. (2020) Lipid kinases PIP5K7 and PIP5K9 are required for polyamine-triggered K+ efflux in Arabidopsis roots. Plant J. 104: 416-432.  122.    Schlöffel MA, Salzer A, Wan WL, van Wijk R, Šemanjski M, Symeonidi E, Slaby P, Kilian J, Maček B, Munnik T, Gusta AA. (2020) The BIR2/BIR3-interacting Phospholipase Dγ1 negatively regulates immunity in Arabidopsis. Plant Physiol. 183: 371-384. 121.    Aliche EB, Screpanti C, De Mesmaeker A, Munnik T, Bouwmeester HJ (2020). Science and application of strigolactones. New Phytol. 227: 1001–1011 120.    González-Mendoza VM, Sánchez-Sandoval ME, Munnik T, Hernandez-Sotomayor T (2020) Biochemical characterization of phospholipases C from Coffea arabica in response to aluminium stress. J. Inorg. Biochem. 204: 110951. 119.    Zarza X,  Shabala L,  Fujita M,  Shabala S,  Haring M,  Tiburcio AF, Munnik T. (2019) Extracellular spermine triggers a rapid intracellular phosphatidic acid response in Arabidopsis, involving PLDδ activation and stimulating ion flux. Front Plant Sci. 10, 601, 1-14 118.    Van Wijk R, Zhang Q, Zarza X, Lamers M, Reyes-Marquez F, Guardia A, Scuffi D, García-Mata C, Ligterink W, Haring MA, Laxalt AM,  Munnik T. (2018) Role for Arabidopsis PLC7 in stomatal movement, seed mucilage attachment, and leaf serration. Front. Plant Sci. 9: 1721. 117. Zhang Q, van Wijk R, ZarzaX, Shahbaz M, van Hooren M, Guardia A, Scuffi D, García-Mata C, van den Ende W, Hoffmann-Benning S, Haring M, Laxalt A, Munnik T. (2018). Knock-down of Arabidopsis PLC5 reduces primary root growth and secondary root formation while overexpression improves drought tolerance and causes stunted root hair growth. Plant Cell Physiol.  59: 2004-2019. 116.   Zhang Q, Berkey R, Blakeslee JJ, Lin J, Ma X, King H, Liddle A, Guo L, Munnik T, Wang X, Xiao S. (2018) Arabidopsis phospholipase Dα1 and Dδ oppositely modulate EDS1- and SA-independent basal resistance against adapted powdery mildew. J. Exp. Bot. 69: 3675-3688.  115.   Kuo HF, Hsu YY, Lin WC, Chen KY, Munnik T, Brearley CA, Chiou TJ. (2018) Arabidopsis inositol phosphate kinases, IPK1 and ITPK1, constitute a metabolic pathway in maintaining phosphate homeostasis. Plant J. 95: 613-630. 114.   Zhang Q, van Wijk R, Shahbaz M, Roels W, van Schooten B, Vermeer J, Zarza X, Guardia A, Scuffi D, García-Mata C, Laha D, Williams P, Willems L, Ligterink W, Hoffmann-Benning S, Gillaspy G,  Schaaf G, Haring M, Laxalt A, Munnik T. (2018). Arabidopsis phospholipase C3 is Involved in lateral root initiation and ABA responses in seed germination and stomatal closure. Plant Cell Physiol. 59: 469-486. 113.   Lee NH, Zarza X, Kim JH, Yoon MJ,  Kim S-H, Lee J-H, Paris N, Munnik T, Otegui MS, Chung T. (2018) Vacuolar trafficking protein VPS38 is dispensable for autophagy. Plant Physiol. 176: 1559-1572. 112.   Szymanski D, Bassham D, Munnik T, Sakamoto W. (2018) Cellular dynamics: Cellular systems in the time domain. Plant Phys. 176: 12-15. 111.   Wu C, Tan L, van Hooren M, Tan X, Liu F, Li Y, Zhao Y, Li B, Rui Q, Munnik T, Bao Y. (2017) Arabidopsis EXO70A1 recruits Patellin3 to the cell membrane independent of its role as exocyst subunit. J. Integr. Plant Biol. 59: 851-865. 110.   Gujas B, Cruz TMD, Kastanaki E, Vermeer JEM, Munnik T and Rodriguez-Villalon A. (2017) Perturbing phosphoinositide homeostasis oppositely affects root vascular differentiation in Arabidopsis thaliana roots. Development. 144: 3578-3589. 109.   D’Ambrosio JM, Couto D, Fabro G, Scuffi D, Álvarez ME, Lamattina L, Munnik T, Andersson MX, Zipfel C, Laxalt AM. (2017) PLC2 regulates MAMP-triggered immunity by modulating ROS production in Arabidopsis. Plant Phys. 175: 970-981. 108.   Van Hooren M & Munnik T. (2017) Plant Plasma Membrane. In: eLS. John Wiley & Sons, Ltd: Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001672.pub3]. 107.   Hirano T, Stecker K, Munnik T, Xu H. and Sato MH (2017). Visualization of phosphatidylinositol 3,5-bisphosphate dynamics by tandem ML1N-based fluorescent protein probe in Arabidopsis. Plant Cell Physiol. 58: 1185-1195. 106.   Vermeer JEM, van Wijk R, Goedhart J, Geldner N, Chory J, Gadella Jr. TWJ & Munnik T. (2017) Imaging diacylglycerol in the cytosolic leaflet of plant membranes. Plant Cell Physiol. 58: 1196-1207. 105.   Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, Kopka J, Fotopoulos V, Munnik T, Gómez-Cadenas A, Tiburcio AF, 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 Environ. 40: 527-542. 104.   Di Fino LM, D'Ambrosio JM, Tejos R, van Wijk R, Lamattina L, Munnik T, Pagnussat GC, Laxalt AM. (2017) Arabidopsis phosphatidylinositol-phospholipase C2 (PLC2) is required for female gametogenesis and embryo development. Planta. 245: 717-728. 103.   Meijer HJG, van Himbergen JAJ, Musgrave A & Munnik T. (2017) Acclimation to salt modifies the activation of several osmotic stress-activated signalling pathways in Chlamydomonas. Phytochemistry 135: 64-72. 102.   Hirano T, Munnik T, and Sato MH. (2017). Inhibition of phosphatidylinositol 3,5-bisphosphate production has pleiotropic effects on various membrane trafficking routes in Arabidopsis. Plant Cell Physiol. 58: 120-129. 101.   Putta P, Rankenberg J, Korver RA, van Wijk R, Munnik T, Testerink C, Kooijman EE. (2016) Phosphatidic acid binding proteins display differential binding as a function of membrane curvature stress and chemical properties. Bichim Biophys. Acta 1858: 2709-2716. 100.   Dejonghe W, Kuenen S, Mylle E, Vasileva M, Keech O, Viotti C, Swerts J, Fendrych M, Ortiz-Morea FA, Mishev K, Delang S, Scholl S, Zarza X, Heilmann M, Kourelis J, Kasprowicz J, Nguyen le SL, Drozdzecki A, Van Houtte I, Szatmári AM, Majda M, Baisa G, Bednarek SY, Robert S, Audenaert D, Testerink C, Munnik T, Van Damme D, Heilmann I, Schumacher K, Winne J, Friml J, Verstreken P, Russinova E. (2016) Mitochondrial uncouplers inhibit clathrin-mediated endocytosis largely through cytoplasmic acidification. Nature Commun. 7: 11710. 99.     Hirano T, Munnik T,  Sato MH. (2015) FAB1 mediates endosome maturation to establish basal PIN polarity through cortical microtubules interaction in Arabidopsis. Plant Phys. 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-bisphosphate 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.     Vermeer JEM. & Munnik T. (2013) Using genetically encoded fluorescent reporters to image lipid signaling in living plants. Methods Mol. Biol. 1009: 283-290. 87.     Munnik T. & Wierzchowiecka M. (2013) Lipid-binding analysis using a fat blot assay. Methods Mol. Biol. 1009: 253-260. 86.     Munnik T. & Laxalt AM. (2013) Measuring PLD activity in vivo. Methods Mol. Biol. 1009, 219-232. 85.     Arisz  SA & Munnik T. (2013) Use of Phospholipase A2 for the production of lysophospholipids. Methods Mol. Biol. 1009: 63-68. 84.     Arisz SA & Munnik T. (2013) Distinguishing phosphatidic acid pools from de novo synthesis, PLD and DGK. Methods Mol. Biol. 1009: 55-62. 83.     Munnik T. (2013) Analysis of D3-, 4-, 5-phosphorylated phosphoinositides using HPLC. Methods Mol. Biol. 1009: 17-24. 82.     Munnik T. & Zarza X. (2013) Analyzing plant signaling phospholipids through 32Pi-labeling and TLC. Methods Mol. Biol. 1009: 3-15. 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 of Arabidopsis 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, 1-15.   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. (2011) 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 Pathog. 7: e1002051. 72.     Testerink C, and 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, Munnik T. (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., Laxalt AM, ter Riet B, Testerink C, Merquiol E, Mosblech A, Leon-Reyes AH, Pieterse, CM, Haring MA, Heilmann I, 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). Plant Phospholipid 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 PI4P dynamics in living plant cells. 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, van der 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) TheArabidopsis 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.     Testerink C, Larsen PB, van der Does D, van Himbergen JAJ, Munnik T. (2007) Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J. Exp. Bot. 14: 3905–3914. 55.     Van Leeuwen W, Vermeer JEM, Gadella Jr. TWJ, Munnik T. (2007) Visualisation of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J. 52: 1014-1026. 54.     Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DTS, Burger KNJ, de Kruijff B. (2007) An electrostatic/hydrogen bond 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 LE, Müller M, 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 BO, 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, Laxalt AM, Jones DR, Divecha N, Gadella Jr. TWJ, Munnik T. (2006) Visualisation of PI3P 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, Haring MA, Munnik T. (2006) LePLDb1 activation and re-localization in suspension-cultured tomato cells treated with xylanase. Plant J. 45: 358-368. 45.     Testerink C, and Munnik T. (2005) Phosphatidic acid - a multifunctional stress-signalling lipid in plants. Trends Plant Sci. 10: 368-375. 44.     Van Leeuwen W, Okresz L, Bögre L, 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, de Koster 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/Avr4 interaction. 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 Jr TWJ, 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 Gennip AH, 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, Munnik T. (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, Meijer HP, Munnik T, Groot JA. (2002) TNFa potentiates ion secretion induced by histamine in a 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. and Meijer HJG. (2001) Osmotic stress activates distinct lipid- and MAPK signalling pathways in plants. FEBS Lett. 498: 172-178. 28.     Laxalt A, ter Riet B, Verdonk JC, Parigi L, Tameling WIL, Vossen J, Haring M, Musgrave A, and Munnik T. (2001) Characterization of five tomato phospholipase D cDNAs, Rapid and specific expression of LePLDb1 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 TNFa. Am. J. Physiol. Cell Physiol. 280: C789-795. 24.     Den Hartog M, Musgrave A, Munnik T. (2001) Nod factor-induced phosphatidic acid and diacylglycerol pyropho­sphate formation, a role for phospholipase C and D in root hair deformation. Plant J. 25: 55-66. 23.     Oprins JC, Meijer HP, van der Burg C, Munnik T, Groot JA (2000) Tumor necrosis factor a 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. Plant J. 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 Chlamydomonasmoewusii. 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, Musgrave A, 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, Musgrave A. (1998) Phospholipid signalling in plants. Biochim. Biophys. Acta, 1389: 222-272. 11.     De Vrije T & 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, De Vrije 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 flower petals. 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, van den Briel 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, Priem J, Munnik T, van den Ende H. (1991) Cyclic variations 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.   Book Chapters 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.

EXPERTISE:

Plant Stress Signalling - Signal transduction - Phospholipid signalling - Membrane trafficking - Abiotic Stress (cold, heat, drought, salt) -  Biotic Stress (plant-pathogen) - Arabidopsis Development - Molecular Heaters

Cell Biology, Biochemistry, Molecular Biology, Plant Physiology

 

SCIENTIFIC CAREER:

• Head Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam (2018-present).
• Associate Professor Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam (2016-present).
• Associate Editor Plant Physiology, section Signaling & Responses (2012 - 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  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, Alan Musgrave Lab, Chlamydomonas (1992-1997)
• Research Assistant - Agrotechnological Research Institute (ATO-DLO; Dr. Truus de Vrije), Wageningen, The Netherlands. Topic: Ethylene signalling in carnation flowers (1991-1992).
• Research Assistant - Institute for Molecular Cell Biology, University of Amsterdam. With Hans de Nobel & Frans Klis, Topic: Yeast cell wall assembly (1988-1990).
• BSc - Botany, University of Applied Sciences,  Amsterdam, The Netherlands (1988)

 

SCIENTIFIC SERVICES:

• Associate Editor Plant Physiology,  section Signaling & Response (2012-present)
• Reviewer 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: >32
• Member-, secretary- and chair of the NWO-CW study group, Lipids & Membranes (2005-2008)
• Expert ERC EvaluatorERC (>2014-now)
• Member Examination board BSc and MSc Biology & Biological Sciences, UvA (>2018-2022)
• Chair Examination board BSc and MSc Biology & Biological Sciences, UvA (2022-current)
• Chair Examination board BSc and MSc Earth & Life Sciences, UvA (2023-current)
• NPEC user committee (Platform of Netherlands Plant Eco-phenotyping Centre)
• Advisory board Chemistry of Life, Dutch Research Council (NWO) - Domain Science (Nov 1, 2022 - Oct 31 2024)

 

AWARDS/PRIZES/GRANTS

•   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)

•   EU-FET grant (2019-2024)

•  ENW-Klein (2021-2025)

 

OUTPUT

Publications: (see All Publications)

•   Number of publications in international refereed scientific journals according to WoS: 133

•   Contributions to books:

      - 2 books (Ed. 2010; Ed. 2013, both Springer);

      - 7 chapters

•   Number of citations according to WoS: >11.200; average citations: 82; H-index: 59

Scientific teaching:

•   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)

Outreach activities:

•   >160 Invited seminars at (inter)national universities, conferences and symposia, world wide (see below).

•   Organiser of SILS seminars, University of Amsterdam (2000-2005)

•   Organiser of Plant Science Meetings (PSM) & Green Life Science (GLS) seminars (2017-2019) , SILS, University of Amsterdam

•   Conference chair at various national- and international conferences (>10)

•   Organiser & chair of Gordon Research Conference (GRC)  Salt and Water Stress 2012, Hong Kong, China.

•   Co-organiser of the 15th World Conference of Parasitic Plants (WCPP2019), Amsterdam, The Netherlands.

•   Co-organizer 'Chemical Ecology Amsterdam' Symposium (2018), Amsterdam, The Netherlands.

•   Organiser of the 10th ESPL,  European Symposium on Plant Lipids (2023), Amsterdam, The Netherlands.

 

Invited Lectures

2023        

• Lipid Signaling in Plants, Seminar in Botany, Florida State University, FL, USA , April 6 (Webinar)

2021    

• Polyamine-induced Lipid Signaling in Plants, Annual meeting of the Mexican Biochemical Society (SMB), Nov 24, Mexico (Webinar)

2020    

• Phospholipid Signalling in Plant Stress, Defence, and Development. IRTG seminar series University of Göttingen, Jan 30-31, Göttingen, Germany.
• Abiotic-stress induced lipid signals. 6th International Conference on Plant Abiotic Stress Tolerance, Feb 21-22, Vienna Austria
• Phospholipid Signalling in Plant Stress & Development. VIBT/DAGZ seminar, University of Natural Resources and Life Sciences (BOKU), Feb 16, Vienna, Austria.
• PIP₂ Signalling in Plant Stress & Development. Institute of Science & Technology (IST), Feb 18, Klosterneuburg, Austria.
• Abiotic-stress induced lipid signals. 6^th International Conference on Plant Abiotic Stress Tolerance, Feb 21-22, Vienna, Austria.
• Phospholipid Signalling in Plant Stress & Development. 17^th International İÜGEN Molecular Biology and Genetics Winter School, Dec 11-13, Istanbul, Turkey (Webinar).

2019

• Role for PIP2 in Plant Heat Stress Tolerance. GRC on  Plant Lipids - Structure, Metabolism & Function. Jan 27-Feb 1, Galveston, Texas, USA.
• Minor lipids with Major impact in Plant Stress Signalling and Development. Invited seminar Texas A&M University, Feb 6, College Station, TX, USA 
• Molecular heaters. Kick-off Meeting EU-FET network BoostCrop, Feb 14, Amsterdam The Netherlands.
• Inositol Phospholipids: Lubrigating Membrane Traffic and Transport in Plant Stress and Development. Keynote lecture. International Workshop on Plant Membrane Biology, session Membrane organisation, Organelles and Signalling. July 7-12 July, Glasgow, UK.
• Molecular Heaters in Plant Biology. EU-FET BoostCrop Meeting, Nov 5-7, University of Warrick, Warrick, UK.
• Phospholipid Signalling in Plant Stress & Development. Instituto de Biología Molecular y Celular de Plantas, Consejo Superior de Investigaciones Cientificas-Universidad Politecnica de Valencia, Nov 13, Valencia, Spain.
• Molecular Heaters. Presentation IXAnext project, IXA UvA-HvA, Nov 22, Amsterdam, Netherlands.

 

 

2018

• 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. 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.
• Signalling through membranes. Chemical Ecology Amsterdam Symposium, Nov 5, Amsterdam, The Netherlands

2017

• 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.

2016

• 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.

2015

• 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. 6^th International Singapore Lipid Symposium (Nov 30-Dec 2) and 6^th Asian Symposium on Plant Lipids, Dec 2-4, Singapore.

2014

• 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 – 3^rd 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. 

2013

• 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, 54^th 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.

2012

• 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. 21^st National Biology Congress, Sept 3-7, Izmir, Turkey.

2011

• 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, 13^th 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. 4^th International INPAS meeting on Salt & Drought Stress in Plants. Nov 18-19, Limasol, Cyprus. 

2010

• 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 19^th 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. 

2009

• 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. 

2008

• 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 150^th 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.

2007

• Phospholipid signalling in plants - 'Seeing is believing'. 3rd European Symposium on Plant Lipids. April 1-4, York, UK.
• Lipid signalling. 3^rd 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. 4^th 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.

2006

• 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.  

2005

• "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. 2^nd 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. 10^th Congress of the Panamerican Association of Biochemistry and Molecular Biology (PABMB). Dec 3-6, 2005, Pinamar, Argentina. 

2004

• 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. 

2003

• 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, 1^st 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. 

2002

• 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. 

2001

• 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. 27^th 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.

  2000

• 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.

1999

• 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.

1998

• 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. 8^th International Conference on the Cell and Molecular Biology of Chlamydomonas. June 2-7, Tahoe City, CA, USA

1997

• Lipid signals meet MAPK. Invited seminar, University of Vienna. Dec 17, Vienna, Austria

1995

• 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. 2^nd UK Phospholipid Signalling Meeting. Sept28, Cambridge, UK.

  1994

• 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. 8^th 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. 

1993

• Signs of a PI 3-kinase signalling pathway in Chlamydomonas. European Chlamydomonas Conference. May 23-26 may, Amsterdam, The Netherlands.

 

 

Vacancies

Currently, no vacancies

 

For personal fellowship applications:

(e.g. FEBS, EMBO, Marie Curie, etc) - please contact:  t.munnik @ uva.nl

 

Fellowships/Internships

Phosphatidic acid (PA) and polyphosphoinositides (PPIs) are minor phospholipids in biological membranes that function as cellular signalling molecules at 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) stress. How this is activated, regulated and where this occurs in cells (e.g. plasma membrane, ER, Golgi) or tissues (e.g. root, stem, stomata) has our particular interest. The  model plant Arabidopsis thaliana contains various lipid kinases, phosphatases and phospholipases, and by using knock-out mutants, overexpression lines, and FP fusions, we are unraveling their role in plant stress signalling and development. Personal felowships or students can be involved in any of these projects.

Tools & Expertise :

• Stress physiology (e.g. root system architecture; root hairs; pollen tubes; tolerance assays for biotic- (PAMPs, Pseudomonas) & abiotic stress (i.e. cold, freezing, heat, salt, hyperosmotic, hyoosmotic, drought); tropisms.
• Cell biology  (Confocal Imaging; lipid biosensors, FP-tagged kinases, -lipases; Protein targets for PIP₂- and PA, phosphomimetics; MT cytoskeleton; endocytosis; exocytosis; membrane trafficking).
• Lipid biochemistry (TLC-, HPLC-, GC-analyses; Lipid binding - liposomes, Fat blots; Radiolabelling, e.g. ³²P/¹⁴C/³H-Ins
• Protein Biochemistry (enzyme kinetics, phospholipase, kinase, phosphatases; Protein kinase, MAPKs; lipid targets, lipid binding;  SDS-PAGE, Western blot, IP, Mass Spec. on  lipids, proteins and metabolome).
• Molecular Biology (gene cloning; promoter-reporter analyses, fusion proteins, gene silencing, T-DNA-insertion KO & KD mutants; overexpression; q/RT-PCR, RNA-Seq analyses, GWAS).

 

 

SILS - Plant Cell Biology

Teun Munnik (PI) 

Ing. Ringo van Wijk (Lab manager)   

Dr. Steven Arisz (Post-doc)  

Drs. Max van Hooren (PhD student)

Ms. Hui Sheng (PhD student)

Drs. Xandra Schrama (technician)

Dr. Michael Mishkind (permanent guest) 

 

Ex-group members

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)

Nazish Annum (Agricultural Biotechnogy Division, National Institute for Biotechnology and Genetic Enginering, Faisalabad, Pakistan)

Ruud Korver  (ENZA) 

Mhyrte Praat (Utrecht University)

Safrina Ahmad 

Drs. Floris Stevens (PhD student GLS-SILS)

Drs. Stella Prelovšek

Dr. Leonardo Hinojosa (PhD student IBED)

Dr. Xavier Zarza

Dr. Femke de Jong

 

Ex-undergraduate students

Wladimir Tameling  

Martine den Hartog  

Julian C. Verdonk  

Steven A. Arisz  

Bas ter Riet  

Elske Schouten  

Diewertje van der Does  

Monique Raats  

Tamara Chessa  

Jacco van Rheenen  

Nathalie Verhoef  

Tessa Nauta  (MSc student)

Thanh Le

Maarten Reitsema (MSc student)

Jiorgos Kourelis (MSc student)

Carlos Jr. Rubio 'Chucho' (HBO student)

Mark aan 't Goor (MSc student)

Matthew Lefebvre (MSc student)

Ruy Kortbeek (MSc student)

Mart Lamers (BSc student)

Max Stam (MSc student)

Kinwai Fung (MSc student Leiden)

Milan Plasmeijer (MSc student)

Martijn van Ophem (MSc student)

Floris Stevens (MSc student)

Rui Alvez (Erasmus student)

Babette Vlieger (BSc student)

Ludo Cialdella (BSc student) 

Jack Dickenson (MSc student)

Eveline Bosman (BSc student)

Valerie de Ridder (BSc student)

Willard Bout (MSc student)

Sjors Huizinga (MSc student)

Pauline Caris (MSc student)

Tijmen Blokzijl (MSc student)

Divya Jagger (MSc student)

Eva van Doore (MSc)

Sjors Huizinga (MSc)

Inam Barakat (BSc & MSc)

Guests

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)

Dr. 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)

MSc. Nazish Annum (University of Faisalabad, Pakistan)

Dr. Aansa Rukya Saleem (Bahria University, Islamabad, Pakistan)

Dr. Ania Kasprowicz-Maluśki (Uniwersytetu Poznańskiego, Poznań, Poland)

 

Collaborating Labs 

Dorus Gadella (SILS, UvA, NL)  

Nullin Divecha (Manchester, UK)   

Takashi Aoyama (Kyoto University, Japan) 

Erik Nielsen (Michigan, US) 

Ana Laxalt (University of Mar del Plata, Argentina)  

Charles Brearley (Norwich, UK)   

Gertjan Kramer (SILS-MS, UvA, NL) 

Harro Bouwmeester (GLS-PHB, 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)

Gerard van der Linden (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)  

Jörg Kudla (Münster, Germany) 

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 of Lausanne,  Switzerland)

Joop Vermeer (Uni of Neuchatelle, Switzerland)

Wybren Jan Buma (HIMS, Molecular photonics UvA)

Jan van Maarseveen (HIMS, Organisc chemistry, UvA)

Jiri Friml (IST Austria)

Dominique van der Straeten (Ghent, Belgium)