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PMID: 14508002 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phospholipase d activation correlates with microtubule reorganization in living plant cells.

The Plant cell ·Vol. 15 ·No. 11 ·2003-11-00 ·Pages 2666-79

Dhonukshe P, Laxalt AM, Goedhart J, Gadella TW, Munnik T

Abstract

A phospholipase D (PLD) was shown recently to decorate microtubules in plant cells. Therefore, we used tobacco BY-2 cells expressing the microtubule reporter GFP-MAP4 to test whether PLD activation affects the organization of plant microtubules. Within 30 min of adding n-butanol, a potent activator of PLD, cortical microtubules were released from the plasma membrane and partially depolymerized, as visualized with four-dimensional confocal imaging. The isomers sec- and tert-butanol, which did not activate PLD, did not affect microtubule organization. The effect of treatment on PLD activation was monitored by the in vivo formation of phosphatidylbutanol, a specific reporter of PLD activity. Tobacco cells also were treated with mastoparan, xylanase, NaCl, and hypoosmotic stress as reported activators of PLD. We confirmed the reports and found that all treatments induced microtubule reorganization and PLD activation within the same time frame. PLD still was activated in microtubule-stabilized (taxol) and microtubule-depolymerized (oryzalin) situations, suggesting that PLD activation triggers microtubular reorganization and not vice versa. Exogenously applied water-soluble synthetic phosphatidic acid did not affect the microtubular cytoskeleton. Cell cycle studies revealed that n-butanol influenced not just interphase cortical microtubules but also those in the preprophase band and phragmoplast, but not those in the spindle structure. Cell growth and division were inhibited in the presence of n-butanol, whereas sec- and tert-butanol had no such effects. Using these novel insights, we propose a model for the mechanism by which PLD activation triggers microtubule reorganization in plant cells.

MeSH Terms
1-Butanol/pharmacology Cell Division/drug effects,physiology Cell Line Cell Membrane/drug effects,physiology Cells, Cultured Enzyme Activation/drug effects Intercellular Signaling Peptides and Proteins Interphase/drug effects,physiology Microscopy, Confocal Microtubule-Organizing Center/drug effects,physiology Microtubules/drug effects,physiology Peptides Phosphatidic Acids/pharmacology Phospholipase D/metabolism Spindle Apparatus/drug effects,physiology Tobacco/cytology,enzymology Type C Phospholipases/antagonists & inhibitors Wasp Venoms/pharmacology
Chemicals
Intercellular Signaling Peptides and Proteins Peptides Phosphatidic Acids Wasp Venoms mastoparan 1-Butanol Type C Phospholipases Phospholipase D
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Dhonukshe Pankaj
Section of Molecular Cytology, Swammerdam Institute for Life Sciences, University of Amsterdam, NL-1090 GB Amsterdam, The Netherlands.
Laxalt Ana M
Goedhart Joachim
Gadella Theodorus W J
Munnik Teun
References (86)
86 references, click to expand
  1. A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane.
    Plant Cell. 2001 Sep;13(9):2143-58 PMID: 11549769
  2. Organization of cortical microtubules at the plasma membrane in Arabidopsis.
    Planta. 1997;201(3):252-60 PMID: 9129335
  3. A unified hypothesis for the role of membrane bound enzyme complexes and microtubules in plant cell wall synthesis.
    J Theor Biol. 1974 Dec;48(2):445-9 PMID: 4459594
  4. Molecular diversity of phospholipase D in angiosperms.
    BMC Genomics. 2002;3:2 PMID: 11876823
  5. Isolation of a 90-kD Microtubule-Associated Protein from Tobacco Membranes.
    Plant Cell. 1996 Nov;8(11):2127-2138 PMID: 12239375
  6. Microtubule organization in the green kingdom: chaos or self-order?
    J Cell Sci. 2002 Apr 1;115(Pt 7):1345-54 PMID: 11896182
  7. Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein.
    Plant Cell. 2002 Sep;14(9):2145-60 PMID: 12215512
  8. PLANT PHOSPHOLIPASES.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:211-231 PMID: 11337397
  9. Changes in the Plasma Membrane Distribution of Rice Phospholipase D during Resistant Interactions with Xanthomonas oryzae pv oryzae.
    Plant Cell. 1996 Jun;8(6):1079-1090 PMID: 12239412
  10. Gravity-induced reorientation of cortical microtubules observed in vivo.
    Plant J. 1999 May;18(4):449-53 PMID: 11536906
  11. Regulation of plant water loss by manipulating the expression of phospholipase Dalpha.
    Plant J. 2001 Oct;28(2):135-44 PMID: 11722757
  12. Plasma-membrane rosettes involved in localized wall thickening during xylem vessel formation of Lepidium sativum L.
    Planta. 1985 May;164(1):12-21 PMID: 24249494
  13. Characterization of five tomato phospholipase D cDNAs: rapid and specific expression of LePLDbeta1 on elicitation with xylanase.
    Plant J. 2001 May;26(3):237-47 PMID: 11446372
  14. Phosphatidic acid: an emerging plant lipid second messenger.
    Trends Plant Sci. 2001 May;6(5):227-33 PMID: 11335176
  15. The control of cellulose microfibril deposition in the cell wall of higher plants : II. Freeze-fracture microfibril patterns in maize seedling tissues following experimental alteration with colchicine and ethylene.
    Planta. 1982 Jun;154(6):501-15 PMID: 24276345
  16. Structure of cortical microtubule arrays in plant cells.
    J Cell Biol. 1978 Apr;77(1):14-34 PMID: 350889
  17. Plant cell biology through the window of the highly synchronized tobacco BY-2 cell line.
    Methods Cell Sci. 1999;21(2-3):123-7 PMID: 10728644
  18. Transphosphatidylation by phospholipase D.
    J Biol Chem. 1967 Feb 10;242(3):477-84 PMID: 6022844
  19. Plant cell division: building walls in the right places.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):33-9 PMID: 11413463
  20. Stabilization of cortical microtubules by the cell wall in cultured tobacco cells : Effects of extensin on the cold-stability of cortical microtubules.
    Planta. 1990 Oct;182(3):363-9 PMID: 24197186
  21. Microtubule-associated proteins in plants--why we need a MAP.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):40-7 PMID: 11413464
  22. Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate.
    Plant Physiol. 2000 Aug;123(4):1507-16 PMID: 10938366
  23. Phospholipid signaling in plants: holding on to phospholipase D.
    Sci STKE. 2001 Dec 4;2001(111):pe42 PMID: 11734658
  24. Relocalization of phospholipase D activity mediates membrane formation during meiosis.
    J Cell Biol. 1998 Jan 12;140(1):81-90 PMID: 9425156
  25. The plant cytoskeleton: vacuoles and cell walls make the difference.
    Cell. 2002 Jan 11;108(1):9-12 PMID: 11792316
  26. A "MICROTUBULE" IN PLANT CELL FINE STRUCTURE.
    J Cell Biol. 1963 Oct 1;19(1):239-50 PMID: 19866635
  27. The enzymatic synthesis of phosphatidylserine and purification by CM-cellulose column chromatography.
    Biochim Biophys Acta. 1977 Jul 20;488(1):36-42 PMID: 560868
  28. Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity.
    Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2697-702 PMID: 9482950
  29. Distinct Ca2+ binding properties of novel C2 domains of plant phospholipase dalpha and beta.
    J Biol Chem. 2000 Jun 30;275(26):19700-6 PMID: 10777500
  30. A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells
    Plant Cell. 1998 Nov;10(11):1927-40 PMID: 9811799
  31. Plant cytokinesis: motoring to the finish.
    Curr Biol. 2002 Mar 19;12(6):R206-8 PMID: 11909547
  32. Dynamic instability of microtubule growth.
    Nature. 1984 Nov 15-21;312(5991):237-42 PMID: 6504138
  33. Calcium signaling during abiotic stress in plants.
    Int Rev Cytol. 2000;195:269-324 PMID: 10603578
  34. Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12192-7 PMID: 10518598
  35. The regulation of phospholipase D by inositol phospholipids and small GTPases.
    FEBS Lett. 2002 Oct 30;531(1):62-4 PMID: 12401204
  36. Utilization of alcohols by plant and mammalian phospholipase D.
    Biochem Mol Biol Int. 1997 Apr;41(4):715-24 PMID: 9111933
  37. High-resolution model of the microtubule.
    Cell. 1999 Jan 8;96(1):79-88 PMID: 9989499
  38. Microtubules in plant morphogenesis: role of the cortical array.
    Annu Rev Cell Biol. 1994;10:153-80 PMID: 7888175
  39. Spatial relationship between microtubules and plasma-membrane rosettes during the deposition of primary wall microfibrils in Closterium sp.
    Planta. 1988 Jan;173(1):22-30 PMID: 24226174
  40. Visualization of particle complexes in the plasma membrane of Micrasterias denticulata associated with the formation of cellulose fibrils in primary and secondary cell walls.
    J Cell Biol. 1980 Feb;84(2):327-39 PMID: 7189756
  41. Golgi secretion is not required for marking the preprophase band site in cultured tobacco cells.
    Plant J. 2002 Jan;29(1):99-108 PMID: 12060230
  42. Microtubule Components of the Plant Cell Cytoskeleton.
    Plant Physiol. 1994 Jan;104(1):1-6 PMID: 12232055
  43. Phospholipid signalling in plant defence.
    Curr Opin Plant Biol. 2002 Aug;5(4):332-8 PMID: 12179967
  44. Helical microtubule arrays and spiral growth.
    Plant Cell. 2002 Oct;14(10):2319-24 PMID: 12368488
  45. Microtubule polymerization dynamics.
    Annu Rev Cell Dev Biol. 1997;13:83-117 PMID: 9442869
  46. The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLD zeta 1 with distinct regulatory domains.
    Plant Physiol. 2002 Mar;128(3):1057-68 PMID: 11891260
  47. Role of cortical microtubules in the orientation of cellulose microfibril deposition in higher-plant cells.
    Protoplasma. 1999;209(1-2):98-104 PMID: 18987798
  48. Cellulose microfibrils: visualization of biosynthetic and orienting complexes in association with the plasma membrane.
    Proc Natl Acad Sci U S A. 1976 Jan;73(1):143-7 PMID: 1061108
  49. Glycerophospholipid synthesis: improved general method and new analogs containing photoactivable groups.
    Proc Natl Acad Sci U S A. 1977 Oct;74(10):4315-9 PMID: 270675
  50. Plasmalemma abscisic acid perception leads to RAB18 expression via phospholipase D activation in Arabidopsis suspension cells.
    Plant Physiol. 2002 Sep;130(1):265-72 PMID: 12226506
  51. CYTOKINESIS AND BUILDING OF THE CELL PLATE IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:751-784 PMID: 11337415
  52. Phospholipid-based signaling in plants.
    Annu Rev Plant Biol. 2003;54:265-306 PMID: 14502992
  53. Activation of phospholipases C and D is an early response to a cold exposure in Arabidopsis suspension cells.
    Plant Physiol. 2002 Oct;130(2):999-1007 PMID: 12376663
  54. Location of the catalytic nucleophile of phospholipase D of Streptomyces antibioticus in the C-terminal half domain.
    Eur J Biochem. 1999 Sep;264(2):577-81 PMID: 10491106
  55. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation.
    Plant J. 2001 Jan;25(1):55-65 PMID: 11169182
  56. Networking of phospholipases in plant signal transduction.
    Physiol Plant. 2002 Jul;115(3):331-335 PMID: 12081524
  57. Synthetic peptides to mimic the role of GTP binding proteins in membrane traffic and fusion.
    Ann N Y Acad Sci. 1994 Mar 9;710:196-208 PMID: 8154748
  58. The control of cellulose microfibril deposition in the cell wall of higher plants : I. Can directed membrane flow orient cellulose microfibrils? Indirect evidence from freeze-fractured plasma membranes of maize and pine seedlings.
    Planta. 1982 Jun;154(6):489-500 PMID: 24276344
  59. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate.
    Plant J. 2000 Apr;22(2):147-54 PMID: 10792830
  60. Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis.
    J Biol Chem. 2002 Aug 30;277(35):31994-2002 PMID: 12077151
  61. Divide and conquer: cytokinesis in plant cells.
    Curr Opin Plant Biol. 1999 Dec;2(6):447-53 PMID: 10607656
  62. Involvement of phospholipase D in wound-induced accumulation of jasmonic acid in arabidopsis.
    Plant Cell. 2000 Nov;12(11):2237-46 PMID: 11090221
  63. Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum.
    Plant Cell. 2000 Jan;12(1):111-24 PMID: 10634911
  64. The first crystal structure of a phospholipase D.
    Structure. 2000 Jun 15;8(6):655-67 PMID: 10873862
  65. Molecular motors and their functions in plants.
    Int Rev Cytol. 2001;204:97-178 PMID: 11243598
  66. Phospholipase D in hormonal and stress signaling.
    Curr Opin Plant Biol. 2002 Oct;5(5):408-14 PMID: 12183179
  67. Microtubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD.
    Planta. 2000 Feb;210(3):502-9 PMID: 10750909
  68. Phospholipid signalling in plants.
    Biochim Biophys Acta. 1998 Jan 23;1389(3):222-72 PMID: 9512651
  69. Mechanism for Plant Cellular Morphogenesis.
    Science. 1962 Dec 28;138(3548):1404-5 PMID: 17753861
  70. Increase in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves.
    Biochim Biophys Acta. 1998 Jul 31;1393(1):193-202 PMID: 9714802
  71. G Protein Activation Stimulates Phospholipase D Signaling in Plants.
    Plant Cell. 1995 Dec;7(12):2197-2210 PMID: 12242371
  72. The characterization of plasma membrane-bound tubulin of cauliflower using Triton X-114 fractionation.
    Plant Physiol. 1997 Nov;115(3):1001-7 PMID: 9390434
  73. Kinetic analysis of Arabidopsis phospholipase Ddelta. Substrate preference and mechanism of activation by Ca2+ and phosphatidylinositol 4,5-biphosphate.
    J Biol Chem. 2002 Dec 20;277(51):49685-90 PMID: 12397060
  74. On the alignment of cellulose microfibrils by cortical microtubules: a review and a model.
    Protoplasma. 2001;215(1-4):150-71 PMID: 11732054
  75. In vivo substrates and the contribution of the common phospholipase D, PLDalpha, to wound-induced metabolism of lipids in Arabidopsis.
    Biochim Biophys Acta. 2001 Feb 26;1530(2-3):236-48 PMID: 11239826
  76. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants.
    J Cell Biol. 1995 Sep;130(6):1345-57 PMID: 7559757
  77. Inhibition of phospholipase D alpha by N-acylethanolamines.
    Plant Physiol. 2002 Aug;129(4):1892-8 PMID: 12177503
  78. Synthesis of fatty acid anhydrides by reaction with dicyclohexylcarbodiimide.
    J Lipid Res. 1966 Jan;7(1):174-5 PMID: 5900216
  79. Structural insights into microtubule function.
    Annu Rev Biochem. 2000;69:277-302 PMID: 10966460
  80. Mechanical forces in plant growth and development.
    Gravit Space Biol Bull. 2000 Jun;13(2):67-73 PMID: 11543283
  81. Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling.
    Plant Cell. 2003 Mar;15(3):597-611 PMID: 12615935
  82. Isolation of cortical MTs from tobacco BY-2 cells.
    Plant Cell Physiol. 2001 Feb;42(2):162-9 PMID: 11230570
  83. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation.
    Science. 2003 May 30;300(5624):1427-30 PMID: 12775839
  84. Cellulose microfibril orientation in Oocystis solitaria: proof that microtubules control the alignment of the terminal complexes.
    J Cell Sci. 1986 Jul;83:223-34 PMID: 3805142
  85. Differential expression of genes encoding Arabidopsis phospholipases after challenge with virulent or avirulent Pseudomonas isolates.
    Mol Plant Microbe Interact. 2002 Aug;15(8):808-16 PMID: 12182338
  86. Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling.
    Plant J. 2001 Jun;26(6):595-605 PMID: 11489173
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2003-11-00
Epub
2003-00-24
Pages
2666-79
Language
English
Region
England
NLM ID
9208688
PMCID
PMC280570
Subset
IM
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