Live-cell imaging of phosphatidic acid dynamics in pollen tubes visualized by Spo20p-derived biosensor

New Phytologist

Volumn 203, Issue 2, 2014, Pages 483-494

  Potocký, Martin ^a   Pleskot, Roman ^a   Pejchar, Přemysl ^a   Vitale, Nicolas ^b   Kost, Benedikt ^c   Žárský, Viktor ^a,d  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Live cell microscopy; Nicotiana tabacum (tobacco); Phosphatidic acid (PA); Phospholipase D; Pollen tube; Spo20p

Indexed keywords

CELL ORGANELLE; ENZYME ACTIVITY; FLUORESCENCE; LIPID; MEMBRANE; ORGANIC ACID; POLLEN; PROTEIN; SPATIOTEMPORAL ANALYSIS; VISUALIZATION; YEAST;

NICOTIANA TABACUM;

DIACYLGLYCEROL; HYBRID PROTEIN; PHOSPHATIDIC ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE D; QB SNARE PROTEIN; QC SNARE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SPO20 PROTEIN, S CEREVISIAE;

BINDING SITE; BLEACHING; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; FLUORESCENCE; GENETIC PROCEDURES; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; METABOLISM; POLLEN TUBE; PROCEDURES; TOBACCO;

BINDING SITES; BIOSENSING TECHNIQUES; CELL MEMBRANE; DIGLYCERIDES; FLUORESCENCE; IMAGE PROCESSING, COMPUTER-ASSISTED; PHOSPHATIDIC ACIDS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOLIPASE D; PHOTOBLEACHING; POLLEN TUBE; QB-SNARE PROTEINS; QC-SNARE PROTEINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TOBACCO;

EID: 84902548436     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12814     Document Type: Article

References (61)

1. Andreeva Z, Ho AYY, Barthet MM, Potocký M, Bezvoda R, Žárský V, Marc J. 2009. Phospholipase D family interactions with the cytoskeleton: isoform δ promotes plasma membrane anchoring of cortical microtubules. Functional Plant Biology 36: 600-612.
2. Antonescu CN, Danuser G, Schmid SL. 2010. Phosphatidic acid plays a regulatory role in clathrin-mediated endocytosis. Molecular Biology of the Cell 21: 2944-2952.
3. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proceedings of the National Academy of Sciences, USA 98: 10 037-10 041.
4. Balla T. 2007. Imaging and manipulating phosphoinositides in living cells. The Journal of Physiology 582: 927-937.
5. Balla T, Bondeva T, Várnai P. 2000. How accurately can we image inositol lipids in living cells? Trends in Pharmacological Sciences 21: 238-241.
6. Bove J, Vaillancourt B, Kroeger J, Hepler PK, Wiseman PW, Geitmann A. 2008. Magnitude and direction of vesicle dynamics in growing pollen tubes using spatiotemporal image correlation spectroscopy and fluorescence recovery after photobleaching. Plant Physiology 147: 1646-1658.
7. Chasserot-Golaz S, Coorssen JR, Meunier FA, Vitale N. 2010. Lipid dynamics in exocytosis. Cellular and Molecular Neurobiology 30: 1335-1342.
8. Cole RA, Fowler JE. 2006. Polarized growth: maintaining focus on the tip. Current Opinion in Plant Biology 9: 579-588.
9. Derksen J, Rutten T, Lichtscheidl IK, De Win AHN, Pierson ES, Rongen G. 1995. Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma 188: 267-276.
10. Dowd PE, Coursol S, Skirpan AL, Kao T-h, Gilroy S. 2006. Petunia phospholipase C1 is involved in pollen tube growth. Plant Cell 18: 1438-1453.
11. Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK. 2001. Cellular oscillations and the regulation of growth: the pollen tube paradigm. BioEssays 23: 86-94.
12. Furneisen JM, Carman GM. 2000. Enzymological properties of the LPP1-encoded lipid phosphatase from Saccharomyces cerevisiae. Biochimica et Biophysica Acta 1484: 71-82.
13. Hammond GRV, Sim Y, Lagnado L, Irvine RF. 2009. Reversible binding and rapid diffusion of proteins in complex with inositol lipids serves to coordinate free movement with spatial information. The Journal of Cell Biology 184: 297-308.
14. Helling D, Possart A, Cottier S, Klahre U, Kost B. 2006. Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18: 3519-3534.
15. Hess B, Kutzner C, van der Spoel D, Lindahl E. 2008. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation 4: 435-447.
16. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. Journal of Molecular Graphics 14: 33-38.
17. Hwang JU, Gu Y, Lee YJ, Yang Z. 2005. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Molecular Biology of the Cell 16: 5385-5399.
18. Kassas N, Tryoen-Tóth P, Corrotte M, Thahouly T, Bader M-F, Grant NJ, Vitale N. 2012. Genetically encoded probes for phosphatidic acid. In: Di Paolo G, Wenk MR, eds. Methods in cell biology. Waltham, MA, USA: Academic Press, 445-459.
19. Kay JG, Koivusalo M, Ma X, Wohland T, Grinstein S. 2012. Phosphatidylserine dynamics in cellular membranes. Molecular Biology of the Cell 23: 2198-2212.
20. Kim DE, Chivian D, Baker D. 2004. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Research 32: W526-W531.
21. Klahre U, Becker C, Schmitt AC, Kost B. 2006. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant Journal 46: 1018-1031.
22. Kooijman EE, Tieleman DP, Testerink C, Munnik T, Rijkers DT, Burger KN, de Kruijff B. 2007. An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. Journal of Biological Chemistry 282: 11356-11364.
23. Kost B. 2008. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends in Cell Biology 18: 119-127.
24. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua N-H. 1999. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. Journal of Cell Biology 145: 317-330.
25. Kost B, Spielhofer P, Chua N-H. 1998. A GFP-mouse talin fusion protein labels plant actin filaments in vivo and visualizes the actin cytoskeleton in growing pollen tubes. Plant Journal 16: 393-401.
26. van Leeuwen W, Vermeer JEM, Gadella TWJ Jr, Munnik T. 2007. Visualization of phosphatidylinositol 4, 5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant Journal 52: 1014-1026.
27. Manna M, Róg T, Vattulainen I. 2014. The challenges of understanding glycolipid functions: an open outlook based on molecular simulations. Biochimica et Biophysica Acta. doi: 10.1016/j.bbalip.2013.12.016.
28. Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH. 2007. The MARTINI force field: coarse grained model for biomolecular simulations. Journal of Physical Chemistry B 111: 7812-7824.
29. Marrink SJ, Tieleman DP. 2013. Perspective on the Martini model. Chemical Society Reviews 42: 6801-6822.
30. Meier KE, Gause KC, Wisehart-Johnson AE, Gore AC, Finley EL, Jones LG, Bradshaw CD, McNair AF, Ella KM. 1998. Effects of propranolol on phosphatidate phosphohydrolase and mitogen-activated protein kinase activities in A7r5 vascular smooth muscle cells. Cellular Signalling 10: 415-426.
31. c and membrane secretion. Journal of Experimental Botany 56: 1665-1674.
32. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink S-J. 2008. The MARTINI coarse-grained force field: extension to proteins. Journal of Chemical Theory and Computation 4: 819-834.
33. Moscatelli A, Ciampolini F, Rodighiero S, Onelli E, Cresti M, Santo N, Idilli A. 2007. Distinct endocytic pathways identified in tobacco pollen tubes using charged nanogold. Journal of Cell Science 120: 3804-3819.
34. Nakanishi H, de los Santos P, Neiman AM. 2004. Positive and negative regulation of a SNARE protein by control of intracellular localization. Molecular Biology of the Cell 15: 1802-1815.
35. Pleskot R, Li J, Žárský V, Potocký M, Staiger CJ. 2013. Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends in Plant Science 18: 496-504.
36. Pleskot R, Pejchar P, Bezvoda R, Lichtscheidl IK, Wolters-Arts M, Marc J, Žárský V, Potocký M. 2012a. Turnover of phosphatidic acid through distinct signalling pathways affects multiple aspects of tobacco pollen tube tip growth. Frontiers in Plant Science 3: 54.
37. Pleskot R, Pejchar P, Staiger CJ, Potocký M. 2014. When fat is not bad: the regulation of actin dynamics by phospholipid signaling molecules. Frontiers in Plant Science 5: 5.
38. Pleskot R, Pejchar P, Žárský V, Staiger CJ, Potocký M. 2012b. Structural insights into the inhibition of actin-capping protein by interactions with phosphatidic acid and phosphatidylinositol (4, 5)-bisphosphate. PLoS Computational Biology 8: e1002765.
39. Pleskot R, Potocký M, Pejchar P, Linek J, Bezvoda R, Martinec J, Valentová O, Novotná Z, Žárský V. 2010. Mutual regulation of plant phospholipase D and the actin cytoskeleton. Plant Journal 62: 494-507.
40. Pokotylo I, Pejchar P, Potocký M, Kocourková D, Krčková Z, Ruelland E, Kravets V, Martinec J. 2013. The plant non-specific phospholipase C gene family. Novel competitors in lipid signalling. Progress in Lipid Research 52: 62-79.
41. Potocký M, Eliáš M, Profotová B, Novotná Z, Valentová O, Žárský V. 2003. Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217: 122-130.
42. Potocký M, Pejchar P, Gutkowska M, Jiménez-Quesada MJ, Potocká A, Alché JdD, Kost B, Žárský V. 2012. NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. Journal of Plant Physiology 169: 1654-1663.
43. Qin Y, Yang Z. 2011. Rapid tip growth: insights from pollen tubes. Seminars in Cell & Developmental Biology 22: 816-824.
44. Ramadurai S, Holt A, Schäfer LV, Krasnikov VV, Rijkers DT, Marrink SJ, Killian JA, Poolman B. 2010. Influence of hydrophobic mismatch and amino acid composition on the lateral diffusion of transmembrane peptides. Biophysical Journal 99: 1447-1454.
45. Rizzo MA, Shome K, Watkins SC, Romero G. 2000. The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. Journal of Biological Chemistry 275: 23 911-23 918.
46. Šali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology 234: 779-815.
47. Shin J, Loewen C. 2011. Putting the pH into phosphatidic acid signaling. BMC Biology 9: 85.
48. Stace CL, Ktistakis NT. 2006. Phosphatidic acid- and phosphatidylserine-binding proteins. Biochimica et Biophysica Acta 1761: 913-926.
49. Stansfeld PJ, Sansom MS. 2011. Molecular simulation approaches to membrane proteins. Structure 19: 1562-1572.
50. Vaškovičová K, Žárský V, Rösel D, Nikolič M, Buccione R, Cvrčková F, Brábek J. 2013. Invasive cells in animals and plants: searching for LECA machineries in later eukaryotic life. Biology Direct 8: 8.
51. Vermeer JEM, Munnik T. 2010. Imaging lipids in living plants. In: Munnik T, ed. Lipid signaling in plants. Berlin, Germany: Springer, 185-199.
52. Vermeer JEM, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella TWJ Jr. 2009. Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant Journal 57: 356-372.
53. Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R, Laxalt AM, Jones DR, Divecha N, Gadella TWJ, Munnik T. 2006. Visualization of PtdIns3P dynamics in living plant cells. Plant Journal 47: 687-700.
54. Vidali L, Rounds CM, Hepler PK, Bezanilla M. 2009. Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS ONE 4: e5744.
55. Wang C, Wang X. 2001. A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiology 127: 1102-1112.
56. Xu D, Zhang Y. 2013. Toward optimal fragment generations for ab initio protein structure assembly. Proteins 81: 229-239.
57. Žárský V, Potocký M. 2010. Recycling domains in plant cell morphogenesis: small GTPase effectors, plasma membrane signalling and the exocyst. Biochemical Society Transactions 38: 723-728.
58. Žárský V, Potocký M, Baluška F, Cvrčková F. 2006. Lipid metabolism, compartmentalization and signalling in the regulation of pollen tube growth. In: Malhó R, ed. The pollen tube. Berlin, Germany: Springer, 117-138.
59. Zeniou-Meyer M, Zabari N, Ashery U, Chasserot-Golaz S, Haeberlé A-M, Demais V, Bailly Y, Gottfried I, Nakanishi H, Neiman AM et al. 2007. Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. Journal of Biological Chemistry 282: 21 746-21 757.
60. Zhang Y, McCormick S. 2010. The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth. Sexual Plant Reproduction 23: 87-93.
61. Zonia L, Munnik T. 2004. Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiology 134: 813-823.