Phospholipase D family interactions with the cytoskeleton: isoform δ promotes plasma membrane anchoring of cortical microtubules
Zornitza Andreeva A , Angela Y. Y. Ho A , Michelle M. Barthet A , Martin Potocký B , Radek Bezvoda C , Viktor Žárský B C and Jan Marc A DA School of Biological Sciences, Macleay Building A12, University of Sydney, Sydney, NSW 2006, Australia.
B Institute of Experimental Botany, Academy of Sciences of the Czech Republic, Rozvojová 263, 165 02 Prague 6, Czech Republic.
C Department of Plant Physiology, Faculty of Science, Charles University, Viničná 5, 128 44 Prague 2, Czech Republic.
D Corresponding author. Email: jmarc@bio.usyd.edu.au
Functional Plant Biology 36(7) 600-612 https://doi.org/10.1071/FP09024
Submitted: 23 January 2009 Accepted: 25 April 2009 Published: 2 July 2009
Abstract
Phospholipase D (PLD) is a key enzyme in signal transduction – mediating plant responses to various environmental stresses including drought and salinity. Isotype PLDδ interacts with the microtubule cytoskeleton, although it is unclear if, or how, each of the 12 PLD isotypes in Arabidopsis may be involved mechanistically. We employed RNA interference in epidermal cells of Allium porrum L. (leek) leaves, in which the developmental reorientation of cortical microtubule arrays to a longitudinal direction is highly sensitive to experimental manipulation. Using particle bombardment and transient transformation with synthetic siRNAs targeting AtPLDα, β, γ, δ, ॉ and ζ, we examined the effect of ‘cross-target’ silencing orthologous A. porrum genes on microtubule reorientation dynamics during cell elongation. Co-transformation of individual siRNAs together with a GFP-MBD microtubule-reporter gene revealed that siRNAs targeting AtPLDδ promoted, whereas siRNAs targeting AtPLDβ and γ reduced, longitudinal microtubule orientation in A. porrum. These PLD isotypes, therefore, interact, directly or indirectly, with the cytoskeleton and the microtubule-plasma membrane interface. The unique response of PLDδ to silencing, along with its exclusive localisation to the plasma membrane, indicates that this isotype is specifically involved in promoting microtubule-membrane anchorage.
Additional keywords: Allium, Arabidopsis, F-actin–microtubule interactions, gene silencing, PLD isotypes, synthetic siRNA.
Acknowledgements
We thank RIKEN for kindly providing cDNA for AtPLDδ, Dr Leila Blackman (Australian National University) for Yelow GFP vector, and University of Belgium for Gateway vectors p2FGW7 or p2GWF7. Confocal images were obtained using a Zeiss confocal microscope in Professor Robyn Overall’s laboratory (University of Sydney). This research was supported by University of Sydney Postgraduate research award to Z.A., University of Sydney Sesqui RandD grant and Australian Research Council grant DP0453114 to J.M, and GAAV Czech Republic grant IAA601110916 to V.Z.
Ambrose JC, Wasteneys GO
(2008) CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Molecular Biology of the Cell 19, 4730–4737.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bargmann BO, Munnik T
(2006) The role of phospholipase D in plant stress responses. Current Opinion in Plant Biology 9, 515–522.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bargmann BO,
Laxalt AM,
ter Riet B,
Schouten E,
van Leeuwen W,
Dekker HL,
de Koster CG,
Haring MA, Munnik T
(2006) LePLD beta 1 activation and relocalization in suspension-cultured tomato cells treated with xylanase. The Plant Journal 45, 358–368.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bonetta L
(2004) RNAI, Silencing never sounded better. Nature Methods 1, 79–86.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Chae YC,
Lee S,
Lee HY,
Heo K,
Kim JH,
Kim JH,
Suh P-G, Ryu SH
(2005) Inhibition of muscarinic receptor-linked phospholipase D activation by association with tubulin. Journal of Biological Chemistry 280, 3723–3730.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chalk AM,
Wahlestedt C, Sonnhammer ELL
(2004) Improved and automated prediction of effective siRNA. Biochemical and Biophysical Research Communications 319, 264–274.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chang J-S,
Kim S-K,
Kwon T-K,
Bae SS,
Min DS,
Lee YH,
Kim S-O,
Seo J-K,
Choi JH, Suh P-G
(2005) Pleckstrin homology domains of phospholipase C-G1 directly interact with γ-tubulin for activation of phospholipase C-G1 and reciprocal modulation of β-tubulin function in microtubule assembly. Journal of Biological Chemistry 280, 6897–6905.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chuong SDX,
Good AG,
Taylor GJ,
Freeman MC,
Moorehead GBG, Muench DG
(2004) Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells. Molecular & Cellular Proteomics 3, 970–983.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Clark PR,
Pober JS, Kluger MS
(2008) Knockdown of TNFR1 by the sense strand of an ICAM-1 siRNA: dissection of an off-target effect. Nucleic Acids Research 36, 1082–1097.
DeBolt S,
Gutierrez R,
Ehrhardt DW,
Melo CV,
Ross L,
Cutler SR,
Somerville C, Bonetta D
(2007) Morlin, an inhibitor of cortical microtubule dynamics and cellulose synthase movement. Proceedings of the National Academy of Sciences of the United States of America 104, 5854–5859.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dhonukshe P,
Laxalt AM,
Goedhart J,
Gadella TWJ, Munnik T
(2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. The Plant Cell 15, 2666–2679.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dhonukshe P,
Vischer N, Gadella TWJ
(2006) Contribution of microtubule growth polarity and flux to spindle assembly and functioning in plant cells. Journal of Cell Science 119, 3193–3205.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dixit R, Cyr R
(2004) Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. The Plant Cell 16, 3274–3284.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ehrhardt DW
(2008) Straighten up and fly right – microtubule dynamics and organization of non-centrosomal arrays in higher plants. Current Opinion in Cell Biology 20, 107–116.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Eliáš M,
Potocký M,
Cvrčková F, Žárský V
(2002) Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3, 2.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fan L,
Zheng S,
Cui D, Wang X
(1999) Subcellular distribution and tissue expression of phospholipase Dα, Dβ, and Dγ in Arabidopsis. Plant Physiology 119, 1371–1378.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gardiner JC, Marc J
(2003) Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 222, 61–74.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gardiner JC,
Harper JDI,
Weerakoon ND,
Collings DA,
Ritchie S,
Gilroy S,
Cyr RJ, Marc J
(2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. The Plant Cell 13, 2143–2158.
|
CAS |
Crossref |
PubMed |
Gardiner JC,
Collings D,
Harper JDI, Marc J
(2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant & Cell Physiology 44, 687–696.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Granger CL, Cyr RJ
(2000) Microtubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD. Planta 210, 502–509.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Granger CL, Cyr RJ
(2001) Use of abnormal preprophase bands to decipher division plane determination. Journal of Cell Science 114, 599–607.
|
CAS |
PubMed |
Gredell JA,
Berger AK, Walton SP
(2008) Impact of target mRNA structure on siRNA silencing efficiency: a large-scale study. Biotechnology and Bioengineering 100, 744–755.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Guindon S, Gascuel O
(2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ho AYY,
Day DD,
Brown MH, Marc J
(2009) Arabidopsis phospholipase Dδ as an initiator of cytoskeleton-mediated signalling to fundamental cellular processes. Functional Plant Biology 36, 190–198.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hoebe RA,
Van Oven CH,
Gadella TWJ,
Dhonukshe PB,
Van Noorden CJF, Manders EMM
(2007) Controlled light-exposure microscopy reduces photobleaching and phototoxicity in fluorescence live-cell imaging. Nature Biotechnology 25, 249–253.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Huang S,
Gao L,
Blanchoin L, Staiger CJ
(2006) Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Molecular Biology of the Cell 17, 1946–1958.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jackson AL, Linsley PS
(2004) Noise amidst the silence: off-target effects of siRNAs? Trends in Genetics 20, 521–524.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jackson AL,
Bartz SR,
Schelter J,
Kobayashi SV,
Burchard J,
Mao M,
Li B,
Cavet G, Linsley PS
(2003) Expression profiling reveals off-target gene regulation by RNAi. Nature Biotechnology 21, 635–637.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Karimi M,
Inze D, Depicker A
(2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193–195.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Katagiri T,
Takahashi S, Shinozaki K
(2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDδ, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. The Plant Journal 26, 595–605.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kawamura Y, Uemura M
(2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. The Plant Journal 36, 141–154.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kusner DJ,
Barton JA,
Qin C,
Wang X, Lyer SS
(2003) Evolutionary conservation of physical and functional interactions between phospholipase D and actin. Archives of Biochemistry and Biophysics 412, 231–241.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lee S,
Park JB,
Kim JH,
Kim Y,
Kim JH,
Shin K-J,
Lee JS,
Ha SH,
Suh P-G, Ryu SH
(2001) Actin directly interacts with phospholipase D, inhibiting its activity. Journal of Biological Chemistry 276, 28252–28260.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li G, Xue H-W
(2007) Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. The Plant Cell 19, 281–295.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li W,
Zhang W,
Welti R, Wang X
(2004) The plasma membrane-bound phospholipase Dδ enhance freezing tolerance in Arabidopsis thaliana. Nature Biotechnology 22, 427–433.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li M,
Qin C,
Welti R, Wang X
(2006) Double knockouts of phospholipases Dzeta1 and Dzeta2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiology 140, 761–770.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lin X,
Ruan X,
Anderson MG,
McDowell JA,
Kroeger PE,
Fesik SW, Shen Y
(2005) SiRNA-mediated off-target gene silencing triggered by a 7 nt complementation. Nucleic Acids Research 33, 4527–4535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lloyd C, Chan J
(2004) Microtubules and the shape of plants to come. Nature Reviews. Molecular Cell Biology 5, 13–23.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Marc J,
Granger CL,
Brincat J,
Fischer DD,
Kao T-H,
McCubbin AG, Cyr RJ
(1988) A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. The Plant Cell 10, 1927–1939.
| Crossref |
Marc J,
Sharkey DE,
Durso NA,
Zhang M, Cyr RJ
(1996) Isolation of a 90-kD microtubule-associated protein from tobacco membranes. The Plant Cell 8, 2127–2138.
|
CAS |
Crossref |
PubMed |
Martin L,
Fanarraga ML,
Aloria K, Zabala JC
(2005) Lipid microdomains – plant membranes get organized. Trends in Plant Science 10, 263–265.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Meijer HJG, Munnik T
(2003) Phospholipid-based signaling in plants. Annual Review of Plant Biology 54, 265–306.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Morel J,
Claverol S,
Mongrand S,
Furt F,
Fromentin J,
Bessoule J-J,
Blein J-P, Simon-Plast F
(2006) Proteomics of plant detergent-resistant membranes. Molecular & Cellular Proteomics 5, 1396–1411.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Motes CM,
Pechter P,
Yoo CM,
Wang Y-S,
Chapman KD, Blancaflor EB
(2005) Differential effects of two phospholipase D inhibitors, 1-butanol and N-acylethanolamine, on in vivo cytoskeletal organization and Arabidopsis seedling growth. Protoplasma 226, 109–123.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nick P
(1999) Signals, motors, morphogenesis – the cytoskeleton in plant development. Plant Biology 1, 169–179.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ohashi Y,
Oka A,
Rodrigues PR,
Possenti M,
Ruberti I,
Morelli G, Aoyama T
(2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300, 1427–1430.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ossowski S,
Schwab R, Weigel D
(2008) Gene silencing in plants using artificial microRNAs and other small RNAs. The Plant Journal 53, 674–690.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Pei Y, Tuschl T
(2006) On the art of identifying effective and specific siRNAs. Nature Methods 3, 670–676.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Qin C, Wang X
(2002) The Arabidopsis phospholipase D family: characterization of a Ca2+-independent and phosphatidylcholine-selective PLDζ1 with distinct regulatory domains. Plant Physiology 128, 1057–1068.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Qin C,
Li M,
Qin W,
Bahn SC,
Wang C, Wang X
(2006) Expression and characterization of Arabidopsis phospholipase D gamma 2. Biochimica et Biophysica Acta (BBA) – Molecular and Cell Biology of Lipids 1761, 1450–1458.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Reynolds A,
Leake D,
Boese Q,
Scaringe S,
Marshall WS, Khvorova A
(2004) Rational siRNA design for RNA interference. Nature Biotechnology 22, 326–330.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sainsbury F,
Collings DA,
Mackun K,
Gardiner J,
Harper JDI, Marc J
(2008) Developmental reorientation of transverse cortical microtubules to longitudinal directions: a role for actomyosin-based streaming and partial microtubule-membrane detachment. The Plant Journal 56, 116–131.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sedbrook JC, Kaloriti D
(2008) Microtubules, MAPs and plant directional cell expansion. Trends in Plant Science 13, 303–310.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Shahollari B,
Peskan-Berghöfer T, Oelműller R
(2004) Receptor kinases with leucine-rich repeats are enriched in triton X-100 insoluble plasma membrane microdomains from plants. Physiologia Plantarum 122, 397–403.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Tafer H,
Ameres SL,
Obernosterer G,
Gebeshuber CA,
Schroeder R,
Martines J, Hovacker IL
(2008) The impact of target site accessibility on the design of effective siRNAs. Nature Biotechnology 26, 578–583.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Timmers ACJ,
Vallotton P,
Heym C, Menzel D
(2007) Microtubule dynamics in root hairs of Medicago truncatula. European Journal of Cell Biology 86, 69–83.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang X
(2000) Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. Progress in Lipid Research 39, 109–149.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang X
(2005) Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. Plant Physiology 139, 566–573.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang X,
Devaiah SP,
Zhang W, Welti R
(2006) Signaling functions of phosphatidic acid. Progress in Lipid Research 45, 250–278.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wasteneys GO, Galway ME
(2003) Remodelling the cytoskeleton for growth and form: an overview with some new views. Annual Review of Plant Biology 54, 691–722.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wasteneys GO, Yang Z
(2004) New views on the plant cytoskeleton. Plant Physiology 136, 3884–3891.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
