Reorientation of Cortical Microtubule Arrays in the Hypocotyl of Arabidopsis thaliana Is Induced by the Cell Growth Process and Independent of Auxin Signaling
Abstract
:1. Introduction
2. Results
2.1. Hypotheses Relating Auxin Signaling, Growth Promotion, and Transverse Microtubule Array Reorientation in the Hypocotyl
2.2. Auxin-Induced Reorientation of Cortical Microtubules in Isolated Hypocotyls of A. thaliana
2.3. Auxin Mediates Microtubule Array Reorientation by the Transcriptional Pathway
2.4. An Intact Microtubule Array Is Not Required for Auxin-Mediated Activation of Hypocotyl Growth
2.5. Microtubule Array Reorientation Triggered by Auxin Requires the Presence of Growth
2.6. Growth without Auxin Signaling Is Sufficient to Reorient Microtubule Arrays
3. Discussion
3.1. The Auxin Effect on Cortical Microtubule Orientation in the Hypocotyl is Indirect and Explicable by Underlying Cell Growth
3.2. Microtubule Array Control by Mechanical Forces and Its Connection to Growth
3.3. Auxin-Mediated Inhibition of Root Growth and Longitudinal Microtubule Reorientation
4. Materials and Methods
4.1. Plant Material
4.2. Seedling Growth
4.3. Hypocotyl Handling and Experimental Design
4.4. Imaging and Scoring of Cortical Microtubule Arrays
4.5. Hypocotyl Growth Measurements
4.6. Auxin Signaling Evaluation
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
AHA | autoinhibited H+-ATPase |
ARF | auxin response factor |
Aux/IAA | auxin/indole-3-acetic acid |
CHX | cycloheximide |
CLSM | confocal laser scanning microscopy |
FC | fusicoccin |
GFP | Green fluorescent protein |
IAA | Indole-3-acetic acid |
MAP4 | Microtubule-associated protein 4 |
MS | Murashige and Skoog |
SAUR | small auxin up RNA |
TIR1/AFB | transport inhibitor response 1/auxin signaling F-box protein |
References
- Fischer, K.; Schopfer, P. Interaction of auxin, light, and mechanical stress in orienting microtubules in relation to tropic curvature in the epidermis of maize coleoptiles. Protoplasma 1997, 196, 108–116. [Google Scholar] [CrossRef]
- Chan, J.; Calder, G.; Fox, S.; Lloyd, C. Cortical microtubule arrays undergo rotary movements in Arabidopsis hypocotyl epidermal cells. Nat. Cell Biol. 2007, 9, 171–175. [Google Scholar] [CrossRef] [PubMed]
- Chan, J.; Eder, M.; Crowell, E.F.; Hampson, J.; Calder, G.; Lloyd, C. Microtubules and CESA tracks at the inner epidermal wall align independently of those on the outer wall of light-grown Arabidopsis hypocotyls. J. Cell Sci. 2011, 124, 1088–1094. [Google Scholar] [CrossRef] [PubMed]
- Chan, J. Microtubule and cellulose microfibril orientation during plant cell and organ growth. J. Microsc. 2012, 247, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Crowell, E.F.; Timpano, H.; Desprez, T.; Franssen-Verheijen, T.; Emons, A.-M.; Höfte, H.; Vernhettes, S. Differential Regulation of Cellulose Orientation at the Inner and Outer Face of Epidermal Cells in the Arabidopsis Hypocotyl. Plant Cell 2011, 23, 2592–2605. [Google Scholar] [CrossRef]
- Shibaoka, H. Plant Hormone-Induced Changes in the Orientation of Cortical Microtubules: Alterations in the Cross-linking Between Microtubules and the Plasma Membrane. Annu. Rev. Plant Boil. 1994, 45, 527–544. [Google Scholar] [CrossRef]
- Nick, P.; Furuya, M.; Schafer, E. Do Microtubules Control Growth in Tropism? Experiments with Maize Coleoptiles. Plant Cell Physiol. 1991, 32, 999–1006. [Google Scholar] [CrossRef]
- Chen, X.; Grandont, L.; Li, H.; Hauschild, R.; Paque, S.; Abuzeineh, A.; Rakusová, H.; Benkova, E.; Perrot-Rechenmann, C.; Friml, J. Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. Nature 2014, 516, 90–93. [Google Scholar] [CrossRef]
- Takesue, K.; Shibaoka, H. Auxin-induced longitudinal-to-transverse reorientation of cortical microtubules in nonelongating epidermal cells of azuki bean epicotyls. Protoplasma 1999, 206, 27–30. [Google Scholar] [CrossRef]
- Baskin, T.I. On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma 2001, 215, 150–171. [Google Scholar] [CrossRef]
- Li, S.; Lei, L.; Somerville, C.R.; Gu, Y. Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl. Acad. Sci. USA 2012, 109, 185–190. [Google Scholar] [CrossRef] [PubMed]
- Lei, L.; Li, S.; Gu, Y. Cellulose synthase interactive protein 1 (CSI1) mediates the intimate relationship between cellulose microfibrils and cortical microtubules. Plant Signal. Behav. 2012, 7, 714–718. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bringmann, M.; Landrein, B.; Schudoma, C.; Hamant, O.; Hauser, M.-T.; Persson, S. Cracking the elusive alignment hypothesis: The microtubule–cellulose synthase nexus unraveled. Trends Plant Sci. 2012, 17, 666–674. [Google Scholar] [CrossRef] [PubMed]
- Bringmann, M.; Li, E.; Sampathkumar, A.; Kocabek, T.; Hauser, M.-T.; Persson, S. POM-POM2/Cellulose Synthase Interacting1 Is Essential for the Functional Association of Cellulose Synthase and Microtubules in Arabidopsis. Plant Cell 2012, 24, 163–177. [Google Scholar] [CrossRef] [PubMed]
- Paradez, A.; Wright, A.; Ehrhardt, D.W. Microtubule cortical array organization and plant cell morphogenesis. Curr. Opin. Plant Boil. 2006, 9, 571–578. [Google Scholar] [CrossRef] [PubMed]
- Paredez, A.; Somerville, C.R.; Ehrhardt, D.W. Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules. Science 2006, 312, 1491–1495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fischer, K.; Schopfer, P. Physical strain-mediated microtubule reorientation in the epidermis of gravitropically or phototropically stimulated maize coleoptiles. Plant J. 1998, 15, 119–123. [Google Scholar] [CrossRef] [PubMed]
- Ikushima, T.; Shimmen, T. Mechano-sensitive orientation of cortical microtubules during gravitropism in azuki bean epicotyls. J. Plant Res. 2005, 118, 19–26. [Google Scholar] [CrossRef]
- Himmelspach, R.; Nick, P. Gravitropic microtubule reorientation can be uncoupled from growth. Planta 2001, 212, 184–189. [Google Scholar] [CrossRef]
- Burian, A.; Hejnowicz, Z. Strain rate does not affect cortical microtubule orientation in the isolated epidermis of sunflower hypocotyls. Plant Biol. 2010, 12, 459–468. [Google Scholar] [CrossRef]
- Burian, A.; Hejnowicz, Z. Fusicoccin affects cortical microtubule orientation in the isolated epidermis of sunflower hypocotyls. Plant Biol. 2011, 13, 201–208. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, K.; Hayashi, K.; Kinoshita, T. Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol. 2012, 159, 632–641. [Google Scholar] [CrossRef] [PubMed]
- Fendrych, M.; Leung, J.; Friml, J.; Stacey, G. TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 2016, 5, e19048. [Google Scholar] [CrossRef]
- Leyser, O. Auxin Signaling. Plant Physiol. 2018, 176. [Google Scholar] [CrossRef]
- Lavy, M.; Estelle, M. Mechanisms of auxin signaling. Development 2016, 143, 3226–3229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gray, W.M.; Kepinski, S.; Rouse, D.; Leyser, O.; Estelle, M. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 2001, 414, 271–276. [Google Scholar] [CrossRef] [PubMed]
- Knox, K. AXR3 and SHY2 interact to regulate root hair development. Development 2003, 130, 5769–5777. [Google Scholar] [CrossRef]
- Falhof, J.; Pedersen, J.T.; Fuglsang, A.T.; Palmgren, M. Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol. Plant 2016, 9, 323–337. [Google Scholar] [CrossRef]
- Spartz, A.K.; Ren, H.; Park, M.Y.; Grandt, K.N.; Lee, S.H.; Murphy, A.S.; Sussman, M.R.; Overvoorde, P.J.; Gray, W.M. SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis. Plant Cell 2014, 26, 2129–2142. [Google Scholar] [CrossRef]
- Ren, H.; Gray, W.M. SAUR Proteins as Effectors of Hormonal and Environmental Signals in Plant Growth. Mol. Plant 2015, 8, 1153–1164. [Google Scholar] [CrossRef] [Green Version]
- Van Den Wijngaard, P.W.J.; Sinnige, M.P.; Roobeek, I.; Reumer, A.; Schoonheim, P.J.; Mol, J.N.M.; Wang, M.; De Boer, A.H. Abscisic acid and 14-3-3 proteins control K+ channel activity in barley embryonic root. Plant J. 2005, 41, 43–55. [Google Scholar] [CrossRef] [PubMed]
- Saponaro, A.; Porro, A.; Chaves-Sanjuan, A.; Nardini, M.; Rauh, O.; Thiel, G.; Moroni, A. Fusicoccin Activates KAT1 Channels by Stabilizing Their Interaction with 14-3-3 Proteins[OPEN]. Plant Cell 2017, 29, 2570–2580. [Google Scholar] [PubMed]
- Boudaoud, A. An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci. 2010, 15, 353–360. [Google Scholar] [CrossRef] [PubMed]
- Kutschera, U. Tissue stresses in growing plant organs. Physiol. Plant. 1989, 77, 157–163. [Google Scholar] [CrossRef]
- Kutschera, U.; Niklas, K. The epidermal-growth-control theory of stem elongation: An old and a new perspective. J. Plant Physiol. 2007, 164, 1395–1409. [Google Scholar] [CrossRef] [PubMed]
- Hejnowicz, Z.; Rusin, A.; Rusin, T. Tensile Tissue Stress Affects the Orientation of Cortical Microtubules in the Epidermis of Sunflower Hypocotyl. J. Plant Growth Regul. 2000, 19, 31–44. [Google Scholar] [CrossRef] [PubMed]
- Zandomeni, K.; Schopfer, P. Mechanosensory microtubule reorientation in the epidermis of maize coleoptiles subjected to bending stress. Protoplasma 1994, 182, 96–101. [Google Scholar] [CrossRef]
- Robinson, S.; Kuhlemeier, C. Global Compression Reorients Cortical Microtubules in Arabidopsis Hypocotyl Epidermis and Promotes Growth. Curr. Biol. 2018, 28, 1794–1802. [Google Scholar] [CrossRef]
- Hamant, O.; Heisler, M.G.; Jönsson, H.; Krupinski, P.; Uyttewaal, M.; Bokov, P.; Corson, F.; Sahlin, P.; Boudaoud, A.; Meyerowitz, E.M.; et al. Developmental Patterning by Mechanical Signals in Arabidopsis. Science 2008, 322, 1650–1655. [Google Scholar] [CrossRef]
- Sampathkumar, A.; Krupinski, P.; Wightman, R.; Milani, P.; Berquand, A.; Boudaoud, A.; Hamant, O.; Jönsson, H.; Meyerowitz, E.M. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 2014, 3, e01967. [Google Scholar] [CrossRef]
- Baskin, T.I.; Jensen, O.E. On the role of stress anisotropy in the growth of stems. J. Exp. Bot. 2013, 64, 4697–4707. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baskin, T.I. Auxin inhibits expansion rate independently of cortical microtubules. Trends Plant Sci. 2015, 20, 471–472. [Google Scholar] [CrossRef] [PubMed]
- Schopfer, P.; Palme, K. Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules? A critical comment. Plant Physiol. 2016, 170, 23–25. [Google Scholar] [CrossRef] [PubMed]
- Fendrych, M.; Akhmanova, M.; Merrin, J.; Glanc, M.; Hagihara, S.; Takahashi, K.; Uchida, N.; Torii, K.U.; Friml, J. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 2018, 4, 453–459. [Google Scholar] [CrossRef] [PubMed]
- Marc, J.; Granger, C.L.; Brincat, J.; Fisher, D.D.; Kao, T.-H.; McCubbin, A.G.; Cyr, R.J. A GFP–MAP4 Reporter Gene for Visualizing Cortical Microtubule Rearrangements in Living Epidermal Cells. Plant Cell 1998, 10, 1927–1939. [Google Scholar]
- Moreno-Risueno, M.A.; Van Norman, J.M.; Moreno, A.; Zhang, J.; Ahnert, S.E.; Benfey, P.N. Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching. Science 2010, 329, 1306–1311. [Google Scholar] [CrossRef] [PubMed]
- Rudnicka, M.; Ludynia, M.; Karcz, W. The Effect of Naphthazarin on the Growth, Electrogenicity, Oxidative Stress, and Microtubule Array in Z. mays Coleoptile Cells Treated With IAA. Front. Plant Sci. 2019, 9, 1940. [Google Scholar] [CrossRef]
- Elliott, A.; Shaw, S.L. A Cycloheximide-Sensitive Step in Transverse Microtubule Array Patterning. Plant Physiol. 2019, 178, 684–698. [Google Scholar] [CrossRef]
- Laskowski, M.J. Microtubule orientation in pea stem cells: A change in orientation follows the initiation of growth rate decline. Planta 1990, 181, 44–52. [Google Scholar] [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Adamowski, M.; Li, L.; Friml, J. Reorientation of Cortical Microtubule Arrays in the Hypocotyl of Arabidopsis thaliana Is Induced by the Cell Growth Process and Independent of Auxin Signaling. Int. J. Mol. Sci. 2019, 20, 3337. https://doi.org/10.3390/ijms20133337
Adamowski M, Li L, Friml J. Reorientation of Cortical Microtubule Arrays in the Hypocotyl of Arabidopsis thaliana Is Induced by the Cell Growth Process and Independent of Auxin Signaling. International Journal of Molecular Sciences. 2019; 20(13):3337. https://doi.org/10.3390/ijms20133337
Chicago/Turabian StyleAdamowski, Maciek, Lanxin Li, and Jiří Friml. 2019. "Reorientation of Cortical Microtubule Arrays in the Hypocotyl of Arabidopsis thaliana Is Induced by the Cell Growth Process and Independent of Auxin Signaling" International Journal of Molecular Sciences 20, no. 13: 3337. https://doi.org/10.3390/ijms20133337