Dissecting the mechanism of abscisic acid-induced dynamic microtubule reorientation using live cell imaging
David Seung A B C , Michael W. Webster A , Richard Wang A , Zornitza Andreeva A and Jan Marc A
+ Author Affiliations
- Author Affiliations
A School of Biological Sciences, University of Sydney, NSW 2006, Australia.
B Present address: Department of Biology (D-BIOL), ETH Zurich, 8092 Zurich, Switzerland.
C Corresponding author. Email: seungd@ethz.ch
Functional Plant Biology 40(3) 224-236 https://doi.org/10.1071/FP12248
Submitted: 24 August 2012 Accepted: 13 October 2012 Published: 23 November 2012
Abstract
Abscisic acid (ABA) is involved in plant development and responses to environmental stress including the formation of longitudinal microtubule arrays in elongating cells, although the underlying mechanism for this is unknown. We explored ABA-induced microtubule reorientation in leek (Allium porrum L.) leaf epidermal cells transiently expressing a GFP–MBD microtubule reporter. After 14–18 h incubation with ABA, the frequency of cells with longitudinal arrays of cortical microtubules along the outer epidermal wall increased with dose-dependency until saturation at 20 μM. Time-course imaging of individual cells revealed a gradual increase in the occurrence of discordant, dynamic microtubules deviating from the normal transverse microtubule array within 2–4 h of exposure to ABA, followed by reorientation into a completely longitudinal array within 5–8 h. Approximately one-half of the ABA-induced reorientation occurred independently of cytoplasmic streaming following the application of cytochalasin D. Reorientation occurred also in the elongation zone of Arabidopsis root tips. Transient expression of AtEB1b–GFP reporter and analysis of ‘comet’ velocities in Allium revealed that the microtubule growth rate increased by 55% within 3 h of exposure to ABA. ABA also increased the sensitivity of microtubules to depolymerisation by oryzalin and exacerbated oryzalin-induced radial swelling of Arabidopsis root tips. The swelling was further aggravated in AtPLDδ-null mutant, suggesting PLDδ plays a role in microtubule stability. We propose that ABA-induced reorientation of transverse microtubule array initially involves destabilisation of the array combined with the formation of dynamic, discordant microtubules.
Additional keywords: abscisic acid, Allium, Arabidopsis, AtEB1b, GFP, cytochalasin D, microtubule dynamics.
References
Abdrakhamanova A, Wang QY, Khokhlova L, Nick P (2003) Is microtubule disassembly a trigger for cold acclimation. Plant & Cell Physiology 44, 676–686.| Is microtubule disassembly a trigger for cold acclimation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslGmur0%3D&md5=6b5233209f77164a712bfeaa87a7687bCAS |
Allard JF, Wasteneys GO, Cytrynbaum E (2010) Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations. Molecular Biology of the Cell 21, 278–286.
| Mechanisms of self-organization of cortical microtubules in plants revealed by computational simulations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFynsrY%3D&md5=eda60b713e0109eb3c87fd5420581fddCAS |
Ambrose JC, Wasteneys GO (2008) CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules. Molecular Biology of the Cell 19, 4730–4737.
| CLASP modulates microtubule-cortex interaction during self-organization of acentrosomal microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlKqsbfO&md5=86e39c53adc19f69505c5aee0dcb55b6CAS |
Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007) The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19, 2763–2775.
| The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWhsr7K&md5=48e7f6b6deed172b4abbea918f03ebb5CAS |
Andreeva Z, Ho AYY, Barthet MM, Potocky M, Bezvoda R, Zarsky 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.
| Phospholipase D family interactions with the cytoskeleton: isoform δ promotes plasma membrane anchoring of cortical microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVegu78%3D&md5=e340bdc3349c4a2867aad264ca24d21dCAS |
Bargmann BOR, Laxalt AM, Riet BT, Testerink EM, Mosblech A, Leon-Reyes A, Pieterse MJ, Haring MA, Heilmann I, Bartels D, Munnik T (2009) Reassessing the role of phospholipas D in the Arabidopsis wounding response. Plant, Cell & Environment 32, 837–850.
| Reassessing the role of phospholipas D in the Arabidopsis wounding response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jsLg%3D&md5=3f4a3091a24e159bc20de3d4a813142dCAS |
Barton DA, Vantard M, Overall RL (2008) Analysis of cortical arrays from Tradescantia virginiana at high resolution reveals discrete microtubule subpopulations and demonstrates that confocal images of arrays can be misleading. The Plant Cell 20, 982–994.
| Analysis of cortical arrays from Tradescantia virginiana at high resolution reveals discrete microtubule subpopulations and demonstrates that confocal images of arrays can be misleading.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVeksbg%3D&md5=f5174b9b51487ae6ccb1c87d31dbacbeCAS |
Baskin TI, Wilson JE, Cork A, Williamson RE (1994) Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant & Cell Physiology 35, 935–942.
Baskin TI, Beemster GTS, Judy-March JE, Marga F (2004) Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis. Plant Physiology 135, 2279–2290.
| Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt1GgsLY%3D&md5=3f68ab924bb86c317e9bd40f03b8b87aCAS |
Chan J, Calder G, Fox S, Lloyd C (2007) Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nature Cell Biology 9, 171–175.
| Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFGlsbk%3D&md5=d086ee101f3b5ef9e23834505b0e9788CAS |
Chan J, Sambade A, Calder G, Lloyd C (2009) Arabidopsis cortical microtubules are initiated along, as well as branching from, existing microtubules. The Plant Cell 21, 2298–2306.
| Arabidopsis cortical microtubules are initiated along, as well as branching from, existing microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht12qsLrM&md5=18255aba11e1c12cb8cea7ce8bed1f3fCAS |
Collings DA, Harper JDI, Marc J, Overall RL, Mullen RT (2002) Life in the fast lane: actin-based motility of plant peroxisomes. Canadian Journal of Botany 80, 430–441.
| Life in the fast lane: actin-based motility of plant peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWgurc%3D&md5=c8a44c34e2fba0139b5c87d26daf7045CAS |
Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof Y-D, Schumacher K, Gonneau M, Höfte H, Vernhettes S (2009) Pausing of golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. The Plant Cell 21, 1141–1154.
| Pausing of golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFams7g%3D&md5=7dfd7c3014a7e8762344747b3af60403CAS |
Derry WB, Wilson L, Jordan MA (1995) Substoichiometric binding of taxol suppresses microtubule dynamics. Biochemistry 34, 2203–2211.
| Substoichiometric binding of taxol suppresses microtubule dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjs1CntrY%3D&md5=940b2b704c5a6d89ee7892bb83ec7af2CAS |
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.
| Phospholipase D activation correlates with microtubule reorganization in living plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Orur0%3D&md5=e0afd2e0a73f1d72a4e0d78d41922043CAS |
Dixit R, Cyr R (2004) Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behaviour. The Plant Cell 16, 3274–3284.
| Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behaviour.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKmug%3D%3D&md5=432c3874cdf043c169ddf0ad17974f79CAS |
Dixit R, Chang E, Cyr R (2006) Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Molecular Biology of the Cell 17, 1298–1305.
| Establishment of polarity during organization of the acentrosomal plant cortical microtubule array.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlSqtb4%3D&md5=009cad99d4a8748e7cf67e15273b0d35CAS |
Eisinger W, Ehrhardt D, Briggs W (2012) Microtubules are essential for guard-cell function in Vicia and Arabidopsis. Molecular Plant 5, 601–610.
| Microtubules are essential for guard-cell function in Vicia and Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Fujita M, Himmelspach R, Hocart CH, Williamson RE, Mansfield SD, Wasteneys GO (2011) Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis. The Plant Journal 66, 915–928.
| Cortical microtubules optimize cell-wall crystallinity to drive unidirectional growth in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXosFerur4%3D&md5=50c92144b0708e9f1d26abc1502a9195CAS |
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.
Granger CL, Cyr RJ (2001) Spatiotemporal relationships between growth and microtubule orientation revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP-MBD. Protoplasma 216, 201–214.
| Spatiotemporal relationships between growth and microtubule orientation revealed in living root cells of Arabidopsis thaliana transformed with green-fluorescent-protein gene construct GFP-MBD.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnos1Okug%3D%3D&md5=bc925aab6a593ee8eb3038f5ea8ab8abCAS |
Hamant O, Traas J (2010) The mechanics behind plant development. New Phytologist 185, 369–385.
| The mechanics behind plant development.Crossref | GoogleScholarGoogle Scholar |
Harris MJ, Outlaw WH, Mertens R, Weiler EW (1988) Water-stress-induced changes in abscisic acid content of guard cells and other cells of Vicia faba L. leaves as determined by enzyme-amplified immunoassay. Proceedings of the National Academy of Sciences of the United States of America 85, 2584–2588.
| Water-stress-induced changes in abscisic acid content of guard cells and other cells of Vicia faba L. leaves as determined by enzyme-amplified immunoassay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktVCjtLY%3D&md5=7e4195faa70ee9c1a5651eca93ef420eCAS |
Ho AYY, Day DA, 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.
| Arabidopsis phospholipase Dδ as an initiator of cytoskeleton-mediated signalling to fundamental cellular processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVaht70%3D&md5=f350585545b2e47d1f3fd7c0b0cdb68bCAS |
Hoad GV (1973) Effect of moisture stress on abscisic acid levels in Ricinus communis L. with particular reference to phloem exudate. Planta 113, 367–372.
| Effect of moisture stress on abscisic acid levels in Ricinus communis L. with particular reference to phloem exudate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXisV2mtA%3D%3D&md5=53c2be80e3639e8a8169a104f54db7a4CAS |
Hoad GV (1978) Effect of water stress on abscisic acid levels in white lupin (Lupinus albus L.) fruit, leaves and phloem exudate. Planta 142, 287–290.
| Effect of water stress on abscisic acid levels in white lupin (Lupinus albus L.) fruit, leaves and phloem exudate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXmtFahsLg%3D&md5=626d83ba5d3b9873dfe524cb0d0a61beCAS |
Hong Y, Zheng S, Wang X (2008) Dual functions of phospholipase Dα1 in plant response to drought. Molecular Plant 1, 262–269.
| Dual functions of phospholipase Dα1 in plant response to drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslyks7o%3D&md5=b36a42b66566c3a749b1805a893c176fCAS |
Huang RF, Lloyd CW (1999) Gibberellic acid stabilises microtubules in maize suspension cells to cold and stimulates acetylation of α-tubulin. FEBS Letters 443, 317–320.
| Gibberellic acid stabilises microtubules in maize suspension cells to cold and stimulates acetylation of α-tubulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Sgu7g%3D&md5=7ac59b6e47a1519e476f8584c0e1a701CAS |
Kawamura E, Wasteneys GO (2008) MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo. Journal of Cell Science 121, 4114–4123.
| MOR1, the Arabidopsis thaliana homologue of Xenopus MAP215, promotes rapid growth and shrinkage, and suppresses the pausing of microtubules in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFGmsw%3D%3D&md5=52e7a9c151ff232fcab1f8e24035d43fCAS |
Khokhlova LP, Olinevich OV, Makarova MV, Bochkareva MA (2006) Morphological and physiological changes in roots of various wheat genotypes as related to cytoskeleton disruption. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 53, 373–383.
| Morphological and physiological changes in roots of various wheat genotypes as related to cytoskeleton disruption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xks1Oku7Y%3D&md5=240aae91432e302fb0fc56a711cfe359CAS |
Li M, Hong M, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochimica et Biophysica Acta (BBA) – Molecular and Cell Biology of Lipids 1791, 927–935.
| Phospholipase D- and phosphatidic acid-mediated signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVensbfE&md5=5350c3c87386c6e65ebd6ebbd386d75fCAS |
Lloyd CW, Shaw PJ, Warn RM, Yuan M (1996) Gibberellic-acid-induced reorientation of cortical microtubules in living plant cells. Journal of Microscopy 181, 140–144.
| Gibberellic-acid-induced reorientation of cortical microtubules in living plant cells.Crossref | GoogleScholarGoogle Scholar |
Lucas JR, Shaw SL (2012) MAP65–1 and MAP65–2 promote cell proliferation and axial growth in Arabidopsis roots. The Plant Journal 71, 454–463.
Marc J, Granger CL, Brincat J, Fisher DD, Kao TH, McCubbin AH, Cyr RJ (1998) A GFP-MAP4 reporter gene for visualizing cortical microtubule rearrangements in living epidermal cells. The Plant Cell 10, 1927–1939.
Mishra G, Zhang W, Deng F, Zhao J, Wang X (2006) A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis. Science 312, 264–266.
| A bifurcating pathway directs abscisic acid effects on stomatal closure and opening in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtlOjsr0%3D&md5=a888c41baf393b25d98da4e33e1335c6CAS |
Mita T, Shibaoka H (1984) Gibberellin stabilizes microtubules in onion leaf sheath cells. Protoplasma 119, 100–109.
| Gibberellin stabilizes microtubules in onion leaf sheath cells.Crossref | GoogleScholarGoogle Scholar |
Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of γ-tubulin in higher plants. Nature Cell Biology 7, 961–968.
| Microtubule-dependent microtubule nucleation based on recruitment of γ-tubulin in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGjs7bN&md5=193f85aa7503686370791070c5de1e2aCAS |
Naoi K, Hashimoto T (2004) A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization. The Plant Cell 16, 1841–1853.
| A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFSqtLs%3D&md5=3af4156064ec027024e8d5189dffb759CAS |
Nick P (1999) Signals, motors, morphogenesis - the cytoskeleton in plant development. Plant Biology 1, 169–179.
| Signals, motors, morphogenesis - the cytoskeleton in plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlajsb4%3D&md5=c725b1391dee269749ade1bd8728db09CAS |
Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495.
| Visualization of cellulose synthase demonstrates functional association with microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlGlt70%3D&md5=120980a2bd03b91adb2c36fe42605a2dCAS |
Quettier AL, Bertrand C, Habricot Y, Miginiac E, Agnes C, Jeannette E, Maldiney R (2006) The phs1–3 mutation in a putative dual-specificity protein tyrosine phosphatase gene provokes hypersensitive responses to abscisic acid in Arabidopsis thaliana. The Plant Journal 47, 711–719.
| The phs1–3 mutation in a putative dual-specificity protein tyrosine phosphatase gene provokes hypersensitive responses to abscisic acid in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKgu7g%3D&md5=ae12ddec93949f39cae18b0ea503f9deCAS |
Ritchie S, Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D. Proceedings of the National Academy of Sciences of the United States of America 95, 2697–2702.
| Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhslenu7c%3D&md5=320d9318218655b3769a561940080d55CAS |
Ritchie S, Gilroy S (2000) Abscisic acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane. Plant Physiology 124, 693–702.
| Abscisic acid stimulation of phospholipase D in the barley aleurone is G-protein-mediated and localized to the plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsF2rsLk%3D&md5=918245498727502ffdbc478b9059ddb5CAS |
Sainsbury F, Collings DA, Mackun K, Gardiner J, Harper JDI, Marc J (2008) Developmental re-orientation of transverse cortical microtubules to longitudinal directions: a role for actomyosin-based streaming and partial microtubule-membrane detachment. The Plant Journal 56, 116–131.
| Developmental re-orientation of transverse cortical microtubules to longitudinal directions: a role for actomyosin-based streaming and partial microtubule-membrane detachment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ygtbjN&md5=79e1dc1bb4b53751bd3116d9a437aceeCAS |
Sakiyama M, Shibaoka H (1990) Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea. Protoplasma 157, 165–171.
| Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyl cells of the dwarf pea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFKmuw%3D%3D&md5=914d96bf47316635156e016fd81d038cCAS |
Sakiyama-Sogo M, Shibaoka H (1993) Gibberellin A3 and abscisic acid cause the reorientation of cortical microtubules in epicotyl cells of the decapitated dwarf pea. Plant & Cell Physiology 34, 431–437.
Sambade A, Pratap A, Buschmann H, Morris RJ, Lloyd C (2012) The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. The Plant Cell 24, 192–201.
| The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOksrs%3D&md5=685a1655a8b979a3f10cbc649fac239eCAS |
Sbalzarini IF, Koumoutsakos P (2005) Feature point tracking and trajectory analysis for video imaging in cell biology. Journal of Structural Biology 151, 182–195.
| Feature point tracking and trajectory analysis for video imaging in cell biology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvgtFCjsQ%3D%3D&md5=0ba47ca3927650ea1b3c32c607e04031CAS |
Schiff PB, Fant J, Horwitz SB (1979) Promotion of microtubule assembly in vitro by taxol. Nature 277, 665–667.
| Promotion of microtubule assembly in vitro by taxol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXkvVCitrY%3D&md5=cf775dd17fb0e147065e344656f834fdCAS |
Seung D, Risopatron JPM, Jones BJ, Marc J (2012) Circadian clock-dependent gating in ABA signalling networks. Protoplasma 249, 445–457.
| Circadian clock-dependent gating in ABA signalling networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xpt1yjsrk%3D&md5=51f709556fa634d5a6f27aa71059fb99CAS |
Shaw SL, Kamyar R, Ehrhardt DW (2003) Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715–1718.
| Sustained microtubule treadmilling in Arabidopsis cortical arrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVKis70%3D&md5=b6b9b2112194abb04f52ba2638781f01CAS |
Shibaoka H (1994) Plant hormone induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane. Annual Review of Plant Physiology and Plant Molecular Biology 45, 527–544.
| Plant hormone induced changes in the orientation of cortical microtubules: alterations in the cross-linking between microtubules and the plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt12rsLo%3D&md5=05eb5cbf9fdd6d19345ed5a178270162CAS |
Sugimoto K, Himmelsphach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. The Plant Cell 15, 1414–1429.
| Mutation or drug-dependent microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVektrs%3D&md5=6227de19fb752291977432b42e57b283CAS |
Turner PF, Margolis RL (1984) Taxol-induced bundling of brain-derived microtubules. Journal of Cell Biology 99, 940–946.
| Taxol-induced bundling of brain-derived microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXls1Glur8%3D&md5=d097a2c99134800256ea3e415a261d9eCAS |
Van Damme D, Poucke KV, Boutant E, Ritzenthaler C, Inzé D, Geelen D (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiology 136, 3956–3967.
| In vivo dynamics and differential microtubule-binding activities of MAP65 proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtValsg%3D%3D&md5=64d1f8a16c8212e0432898ab1f31269eCAS |
Vos JW, Dogterom M, Emons AMC (2004) Microtubules become more dynamic but not shorter during preprophase band formation: a possible ‘search-and-capture’ mechanism for microtubule translocation. Cell Motility and the Cytoskeleton 57, 246–258.
| Microtubules become more dynamic but not shorter during preprophase band formation: a possible ‘search-and-capture’ mechanism for microtubule translocation.Crossref | GoogleScholarGoogle Scholar |
Walia A, Lee JS, Wasteneys G, Ellis B (2009) Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. The Plant Journal 59, 565–575.
| Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFChtrrM&md5=f011531e01d3b22e1257cfcb9ac50553CAS |
Wang QY, Nick P (2001) Cold acclimation can induce microtubular cold stability in a manner distinct from abscisic acid. Plant & Cell Physiology 42, 999–1005.
| Cold acclimation can induce microtubular cold stability in a manner distinct from abscisic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntFWksb4%3D&md5=7f307a57f440d2a4b0093134660b02ecCAS |
Wang X, Devaiah SP, Zhang W, Welti R (2006) Signaling functions of phosphatidic acid. Progress in Lipid Research 45, 250–278.
| Signaling functions of phosphatidic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVWqtrY%3D&md5=1882c97ec88987e8945fe016d8763543CAS |
Wang C, Li J, Yuan M (2007) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant & Cell Physiology 48, 1534–1547.
| Salt tolerance requires cortical microtubule reorganization in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVCmt73I&md5=0b2681aa2c6d430766290f922e87942fCAS |
Wasteneys GO, Ambrose JC (2009) Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends in Cell Biology 19, 62–71.
| Spatial organization of plant cortical microtubules: close encounters of the 2D kind.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1amtL4%3D&md5=c333111b61621a6f64f9b65c745e080cCAS |
Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411, 610–613.
| MOR1 is essential for organizing cortical microtubules in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksVSgsr4%3D&md5=8841fbfd694a7987af5c4f9956615a5aCAS |
Wiesler B, Want Q-Y, Nick P (2002) The stability of cortical microtubules depends on their orientation. The Plant Journal 32, 1023–1032.
| The stability of cortical microtubules depends on their orientation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotFeqtw%3D%3D&md5=bcab24b901bee8e857ca286c94ceedd7CAS |
Yao M, Wakamatsu Y, Itoh TJ, Shoji T, Hashimoto T (2008) Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. Journal of Cell Science 121, 2372–2381.
| Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVKqtrw%3D&md5=59cb3c162adbff86f1974893974b7545CAS |
Yuan M, Shaw PJ, Warn RM, Lloyd CW (1994) Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proceedings of the National Academy of Sciences of the United States of America 91, 6050–6053.
| Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXksFCjurw%3D&md5=725d339c1efab9d793675841f2ee7db5CAS |
Zhang SQ, Outlaw WH (2001) The guard-cell apoplast as a site of abscisic acid redistribution in Vicia faba L. Plant, Cell & Environment 24, 347–355.
| The guard-cell apoplast as a site of abscisic acid redistribution in Vicia faba L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1OitL0%3D&md5=0e489a2c57b521a70b4679d39d9e2778CAS |
Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. The Plant Cell 15, 2285–2295.
| The oleate-stimulated phospholipase D, PLDδ, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXotlGmtL8%3D&md5=4895a2b1a05f906a9f84c3cd1dab2137CAS |
Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling. Proceedings of the National Academy of Sciences of the United States of America 101, 9508–9513.
| Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlKjtr4%3D&md5=39f849386d25087e46cf8557f614af07CAS |
