Advertisement

Protoplasma

, Volume 226, Issue 3–4, pp 109–123 | Cite as

Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth

  • Christy M. Motes
  • Priit Pechter
  • Cheol Min Yoo
  • Yuh-Shuh Wang
  • Kent D. Chapman
  • Elison B. Blancaflor
Article

Summary.

Plant development is regulated by numerous chemicals derived from a multitude of metabolic pathways. However, we know very little about the biological effects and functions of many of these metabolites in the cell. N-Acylethanolamines (NAEs) are a group of lipid mediators that play important roles in mammalian physiology. Despite the intriguing similarities between animals and plants in NAE metabolism and perception, not much is known about the precise function of these metabolites in plant physiology. In plants, NAEs have been shown to inhibit phospholipase Dα (PLDα) activity, interfere with abscisic acid-induced stomatal closure, and retard Arabidopsis seedling development. 1-Butanol, an antagonist of PLD-dependent phosphatidic acid production, was reported to induce defects in Arabidopsis seedling development that were somewhat similar to effects induced by elevated levels of NAE. This raised the possibility that the impact of NAE on seedling growth could be mediated in part via its influence on PLD activity. To begin to address this possibility, we conducted a detailed, comparative analysis of the effects of 1-butanol and N-lauroylethanolamine (NAE 12:0) on Arabidopsis root cell division, in vivo cytoskeletal organization, seed germination, and seedling growth. Although both NAE 12:0 and 1-butanol induced profound cytoskeletal and morphological alterations in seedlings, there were distinct differences in their overall effects. 1-Butanol induced more pronounced modifications in cytoskeletal organization, seedling growth, and cell division at concentrations severalfold higher than NAE 12:0. We propose that these compounds mediate their differential effects on cellular organization and seedling growth, in part through the differential modulation of specific PLD isoforms.

Key words: Actin; 1-Butanol; Lipid; Microtubule; N-Acylethanolamine; Phospholipase D. 

Abbreviations

GFP

green-fluorescent protein

LA

lauric acid

NAE

N-acylethanolamine

NAPE

N-acylphosphatidylethanolamine

PLD

phospholipase D

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Austin-Brown, S, Chapman, KD 2002Inhibition of phospholipase Dα by N-acylethanolamines.Plant Physiol12918921898CrossRefPubMedGoogle Scholar
  2. Baluska, F, Volkmann, D, Barlow, PW 1996Specialized zones of development in roots: view from the cellular level.Plant Physiol11234PubMedGoogle Scholar
  3. Bao, Y, Kost, B, Chua, NH 2001Reduced expression of alpha-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism.Plant J28145157CrossRefPubMedGoogle Scholar
  4. Blancaflor, EB, Hou, G, Chapman, KD 2003Elevated levels of N-lauroylethanolamine, an endogenous constituent of desiccated seeds, disrupt normal root development in Arabidopsis thaliana seedlings.Planta217206217PubMedGoogle Scholar
  5. Buckley, NE, McKoy, KL, Mezey, E, Bonner, T, Felder, CC, Glass, M, Zimmer, A 2000Immunomodulation by cannabinoids is absent in mice deficient for the CB2 receptor.Eur J Pharmacol396141149CrossRefPubMedGoogle Scholar
  6. Chapman, KD 1998Phospholipase activity during plant growth and development and in response to environmental stress.Trends Plant Sci3419426CrossRefGoogle Scholar
  7. – (2000) Emerging physiological roles for N-acylphosphatidylethanolamine metabolism in plants: signal transduction and membrane protection. Chem Phys Lipids 108: 221–230Google Scholar
  8. – (2004) The occurrence, metabolism and prospective functions of N-acylethanolamines in plants. Prog Lipid Res 43: 302–327Google Scholar
  9. – Tripathy S, Venables B, Desouza A (1998) N-acylethanolamines: formation and molecular composition of a new class of plant lipids. Plant Physiol 116: 1163–1168Google Scholar
  10. Charron, D, Pingret, J-L, Chabaud, M, Journet, E-P, Barker, DG 2004Pharmacological evidence that multiple phospholipid signaling pathways link rhizobium nodulation factor perception in Medicago truncatula root hairs to intracellular responses, including Ca2+ spiking and specific ENOD gene expression.Plant Physiol13635823593CrossRefPubMedGoogle Scholar
  11. Cockcroft, S 2001Signaling roles of mammalian phospholipase D1 and D2.Cell Mol Life Sci5816741687PubMedGoogle Scholar
  12. Cohen, G, Rubinstein, S, Gur, Y, Breitbart, H 2004Crosstalk between protein kinase A and C regulates phospholipase D and F-actin formation during sperm capacitation.Dev Biol267230241CrossRefPubMedGoogle Scholar
  13. Colon-Carmona, A, You, R, Haimovitch-Gal, T, Doerner, P 1999Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein.Plant J20503508CrossRefPubMedGoogle Scholar
  14. Cravatt, BF, Saghatelian, A, Hawkins, EG, Clement, AB, Bracey, MH, Lichtman, AH 2004Functional disassociation of the central and peripheral fatty acid amide signaling systems.Proc Natl Acad Sci USA1011082110826CrossRefPubMedGoogle Scholar
  15. Cruz-Ramirez, A, Lopez-Bucio, J, Ramirez-Pimentel, G, Zurita-Silva, A, Sanchez-Calderon, L, Ramirez-Chavez, E, Gonzalez-Ortega, E, Herrera-Estrella, L 2004The xipotl mutant of Arabidopsis reveals a critical role for phospholipid metabolism in root system development and epidermal cell integrity.Plant Cell1620202034CrossRefPubMedGoogle Scholar
  16. Dhonukshe, P, Laxalt, AM, Goedhart, J, Gadella, TW, Munnik, T 2003Phospholipase D activation correlates with microtubule reorganization in living plant cells.Plant Cell1526662679PubMedGoogle Scholar
  17. Drobak, BK, Franklin-Tong, VE, Staiger, CJ 2004The role of the actin cytoskeleton in plant cell signaling.New Phytol1631330CrossRefGoogle Scholar
  18. Fowler, CJ 2003Plant-derived, synthetic and endogenous cannabinoids as neuroprotective agents. Non-psychoactive cannabinoids, ‘entourage’ compounds and inhibitors of N-acylethanolamine breakdown as therapeutic strategies to avoid psychotropic effects.Brain Res Brain Res Rev412643CrossRefPubMedGoogle Scholar
  19. Gardiner, JC, Harper, JDI, Weerakoon, ND, Collings, DA, Ritchie, S, Gilroy, S, Cyr, RJ, Marc, J 2001A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane.Plant Cell1321432158CrossRefPubMedGoogle Scholar
  20. – Collings DA, Harper JD, Marc J (2003) The effects of phospholipase D antagonist 1-butanol on seedling development and microtubule organization in Arabidopsis. Plant Cell Physiol 44: 687–696Google Scholar
  21. Granger, CL, Cyr, RJ 2001Spatiotemporal relationships between growth and microtubule orientation as revealed in living root cells of Arabidopsis thaliana transformed with the green-fluorescent protein gene construct GFP-MBD.Protoplasma216201214PubMedGoogle Scholar
  22. Hodgkin, MN, Clark, JM, Rose, S, Saqib, K, Wakelam, MJ 1999Characterization of the regulation of phospholipase D activity in the detergent-insoluble fraction of HL60 cells by protein kinase C and small G-proteins.Biochem J3398793CrossRefPubMedGoogle Scholar
  23. Hwang, JU, Lee, Y 2001Abscisic acid-induced actin reorganization in guard cells of dayflower is mediated by cytosolic calcium levels and by protein kinase and protein phosphatase activities.Plant Physiol12521202128CrossRefPubMedGoogle Scholar
  24. Jacob, T, Ritchie, SM, Assman, SM, Gilroy, S 1999Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity.Proc Natl Acad Sci USA961219212197PubMedGoogle Scholar
  25. Komati, H, Naro, F, Mebarek, S, De Arcangelis, V, Adamo, S, Lagarde, M, Prigent, AF, Nemoz, G 2005Phospholipase D is involved in myogenic differentiation through remodeling of actin cytoskeleton.Mol Biol Cell1612321244CrossRefPubMedGoogle Scholar
  26. Kunos, G, Jarai, Z, Batkai, S, Goparaju, SK, Ishac, EJ, Liu, J, Wang, L, Wagner, JA 2000Endocannabinoids as vascular modulators.Chem Phys Lipids108159168PubMedGoogle Scholar
  27. Kusner, DJ, Barton, JA, Wen, K-K, Wang, X, Rubenstein, PA, Iyer, SS 2002Regulation of phospholipase D by actin.J Biol Chem2775068350692CrossRefPubMedGoogle Scholar
  28. – – Qin C, Wang X, Iyer SS (2003) Evolutionary conservation of physical and functional interaction between phospholipase D and actin. Arch Biochem Biophys 412: 231–241Google Scholar
  29. Lemichez, E, Wu, Y, Sanchez, J-P, Mettouchi, A, Mathur, J, Chua, N-H 2001Inactivation of AtRac1 by abscisic acid is essential for stomatal closure.Genes Dev1518081816CrossRefPubMedGoogle Scholar
  30. Marc, J, Granger, CL, Brincat, J, Fisher, DD, Kao, Th, McCubbin, AG, Cyr, RJ 1998A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells.Plant Cell1019271940CrossRefPubMedGoogle Scholar
  31. Munnik, T 2001Phosphatidic acid: an emerging plant lipid second messenger.Trends Plant Sci6227233CrossRefPubMedGoogle Scholar
  32. – Musgrave A (2001) Phospholipid signaling in plants: holding on to phospholipase D. Science’s STKE http://stke.sciencemag.org/cgi/content/full/sigtrans;2001/111/pe42
  33. – Arisz SA, De Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7: 2197–2210Google Scholar
  34. Ohashi, Y, Oka, A, Rodriguez-Pousada, R, Possenti, M, Ruberti, I, Morelli, G, Aoyama, T 2003Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation.Science30014271430CrossRefPubMedGoogle Scholar
  35. Pappan, K, Austin-Brown, S, Chapman, KD, Wang, X 1998Substrate selectivities and lipid modulation of plant phospholipase Dα, β and γ.Arch Biochem Biophys353131140CrossRefPubMedGoogle Scholar
  36. Paria, BC, Dey, SK 2000Ligand-receptor signaling with endocannabinoids in preimplantation embryo development and implantation.Chem Phys Lipids108211220PubMedGoogle Scholar
  37. Park, JB, Kim, JH, Kim, Y, Ha, SH, Yoo, JS, Du, G, Frohman, MA, Suh, PG, Ryu, SH 2000Cardiac phospholipase D2 localizes to sarcolemmal membranes and is inhibited by alpha-actinin in an ADP-ribosylation factor-reversible manner.J Biol Chem2752129521301PubMedGoogle Scholar
  38. Qin, C, Wang, X 2002The Arabidopsis phospholipase D family, characterization of a calcium-independent and phosphatidylcholine-selective PLDζ1 with distinct regulatory domains.Plant Physiol12810571068PubMedGoogle Scholar
  39. Ritchie, S, Gilroy, S 1998Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity.Proc Natl Acad Sci USA9526972702CrossRefPubMedGoogle Scholar
  40. Sang, Y, Zheng, S, Li, W, Huang, B, Wang, X 2001Regulation of plant water loss by manipulating the expression of phospholipase Dα.Plant J28111CrossRefGoogle Scholar
  41. Schmid, HH, Schmid, PC, Natarajan, V 1996The N-acylation-phosphodiesterase pathway and cell signaling.Chem Phys Lipids80133142PubMedCrossRefGoogle Scholar
  42. Shrestha, R, Dixon, RA, Chapman, KD 2003Molecular identification of a functional homologue of the mammalian fatty acid amide hydrolase in Arabidopsis thaliana.J Biol Chem2783499034997CrossRefPubMedGoogle Scholar
  43. Smertenko, AP, Bozhkov, PV, Filinova, LH, von Arnold, S, Hussey, PJ 2003Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos.Plant J33813824CrossRefPubMedGoogle Scholar
  44. Staiger, CJ 2000Signaling to the actin cytoskeleton in plants.Annu Rev Plant Physiol Plant Mol Biol51257288CrossRefPubMedGoogle Scholar
  45. Tripathy, S, Kleppinger-Sparace, K, Dixon, RA, Chapman, KD 2003N-Acylethanolamine signaling in tobacco is mediated by a membrane associated, high-affinity binding protein.Plant Physiol13117811791CrossRefPubMedGoogle Scholar
  46. Ueda, K, Matsuyama, T, Hashimoto, T 1999Visualization of microtubules in living cells of transgenic Arabidopsis thaliana.Protoplasma206201206CrossRefGoogle Scholar
  47. van Der Stelt, M, Di Marzo, V 2004Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels.Eur J Biochem27118271834CrossRefPubMedGoogle Scholar
  48. – Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, Veldink GA, Vliegenthart JF, Di Marzo V, Nicolay K (2001) Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci 21: 8765–8771Google Scholar
  49. Wang, X 2002Phospholipase D in hormonal and stress signaling.Curr Opin Plant Biol5408414PubMedGoogle Scholar
  50. Wang, Y-S, Motes, CM, Mohamalawari, DR, Blancaflor, EB 2004Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots.Cell Motil Cytoskeleton597993CrossRefPubMedGoogle Scholar
  51. Wilson, RI, Nicoll, RA 2002Endocannabinoid signaling in the brain.Science296678682CrossRefPubMedGoogle Scholar
  52. Zhang, W, Qin, C, Zhoa, J, Wang, X 2004Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling.Proc Natl Acad Sci USA10195089513PubMedGoogle Scholar
  53. Zolese, G, Wozniak, M, Mariani, P, Saturni, L, Bertoli, E, Ambrosini, A 2003Different modulation of phospholipase A2 activity by saturated and monounsaturated N-acylethanolamines.J Lipid Res44742753PubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2005

Authors and Affiliations

  • Christy M. Motes
    • 1
  • Priit Pechter
    • 1
  • Cheol Min Yoo
    • 1
  • Yuh-Shuh Wang
    • 1
  • Kent D. Chapman
    • 2
  • Elison B. Blancaflor
    • 1
  1. 1.Plant Biology DivisionSamuel Roberts Noble FoundationArdmoreOklahoma
  2. 2.Center for Plant Lipid Research, Department of Biological SciencesUniversity of North TexasDentonTexas

Personalised recommendations