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Review

The interplay between ROS and tubulin cytoskeleton in plants

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Article: e28069 | Received 06 Jan 2014, Accepted 31 Jan 2014, Published online: 12 Feb 2014

References

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci 2004; 9:490 - 8; http://dx.doi.org/10.1016/j.tplants.2004.08.009; PMID: 15465684
  • Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 2006; 141:312 - 22; http://dx.doi.org/10.1104/pp.106.077073; PMID: 16760481
  • Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55:373 - 99; http://dx.doi.org/10.1146/annurev.arplant.55.031903.141701; PMID: 15377225
  • Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011; 194:7 - 15; http://dx.doi.org/10.1083/jcb.201102095; PMID: 21746850
  • Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V. Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 2007; 174:742 - 51; http://dx.doi.org/10.1111/j.1469-8137.2007.02042.x; PMID: 17504458
  • Martin MV, Fiol DF, Sundaresan V, Zabaleta EJ, Pagnussat GC. oiwa, a female gametophytic mutant impaired in a mitochondrial manganese-superoxide dismutase, reveals crucial roles for reactive oxygen species during embryo sac development and fertilization in Arabidopsis. Plant Cell 2013; 25:1573 - 91; http://dx.doi.org/10.1105/tpc.113.109306; PMID: 23653473
  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003; 422:442 - 6; http://dx.doi.org/10.1038/nature01485; PMID: 12660786
  • Pitzschke A, Forzani C, Hirt H. Reactive oxygen species signaling in plants. Antioxid Redox Signal 2006; 8:1757 - 64; http://dx.doi.org/10.1089/ars.2006.8.1757; PMID: 16987029
  • Kwak JM, Nguyen V, Schroeder JI. The role of reactive oxygen species in hormonal responses. Plant Physiol 2006; 141:323 - 9; http://dx.doi.org/10.1104/pp.106.079004; PMID: 16760482
  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 2010; 33:453 - 67; http://dx.doi.org/10.1111/j.1365-3040.2009.02041.x; PMID: 19712065
  • Torres MA. ROS in biotic interactions. Physiol Plant 2010; 138:414 - 29; http://dx.doi.org/10.1111/j.1399-3054.2009.01326.x; PMID: 20002601
  • Møller IM, Sweetlove LJ. ROS signalling-specificity is required. Trends Plant Sci 2010; 15:370 - 4; http://dx.doi.org/10.1016/j.tplants.2010.04.008; PMID: 20605736
  • Kost B, Mathur J, Chua N-H. Cytoskeleton in plant development. Curr Opin Plant Biol 1999; 2:462 - 70; http://dx.doi.org/10.1016/S1369-5266(99)00024-2; PMID: 10607658
  • Nick P. Microtubules, signalling and abiotic stress. Plant J 2013; 75:309 - 23; http://dx.doi.org/10.1111/tpj.12102; PMID: 23311499
  • Hardham AR. Microtubules and biotic interactions. Plant J 2013; 75:278 - 89; http://dx.doi.org/10.1111/tpj.12171; PMID: 23480445
  • Potters G, Pasternak TP, Guisez Y, Jansen MAK. Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ 2009; 32:158 - 69; http://dx.doi.org/10.1111/j.1365-3040.2008.01908.x; PMID: 19021890
  • Livanos P, Apostolakos P, Galatis B. Plant cell division: ROS homeostasis is required. Plant Signal Behav 2012; 7:771 - 8; http://dx.doi.org/10.4161/psb.20530; PMID: 22751303
  • Livanos P, Galatis B, Quader H, Apostolakos P. Disturbance of reactive oxygen species homeostasis induces atypical tubulin polymer formation and affects mitosis in root-tip cells of Triticum turgidum and Arabidopsis thaliana.. Cytoskeleton (Hoboken) 2012; 69:1 - 21; http://dx.doi.org/10.1002/cm.20538; PMID: 21976360
  • Potters G, De Gara L, Asard H, Horemans N. Ascorbate and glutathione: guardians of the cell cycle, partners in crime?. Plant Physiol Biochem 2002; 40:537 - 48; http://dx.doi.org/10.1016/S0981-9428(02)01414-6
  • Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier PJ, Foyer CH. Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 2010; 64:825 - 38; http://dx.doi.org/10.1111/j.1365-313X.2010.04371.x; PMID: 21105929
  • Eleftheriou EP, Adamakis I-DS, Fatsiou M, Panteris E. Hexavalent chromium disrupts mitosis by stabilizing microtubules in Lens culinaris root tip cells. Physiol Plant 2013; 147:169 - 80; http://dx.doi.org/10.1111/j.1399-3054.2012.01652.x; PMID: 22607451
  • Urbanek A, Zechmann B, Zellnig G, Müller M. Aspects of glutathione treatment on the cytoskeleton in different cells of Picea abies.. Phyton 2003; 43:319 - 33
  • Wang S, Kurepa J, Smalle JA. Ultra-small TiO(2) nanoparticles disrupt microtubular networks in Arabidopsis thaliana.. Plant Cell Environ 2011; 34:811 - 20; http://dx.doi.org/10.1111/j.1365-3040.2011.02284.x; PMID: 21276012
  • Wang C, Li J, Yuan M. Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant Cell Physiol 2007; 48:1534 - 47; http://dx.doi.org/10.1093/pcp/pcm123; PMID: 17906320
  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 2006; 9:436 - 42; http://dx.doi.org/10.1016/j.pbi.2006.05.014; PMID: 16759898
  • Jaspers P, Kangasjärvi J. Reactive oxygen species in abiotic stress signaling. Physiol Plant 2010; 138:405 - 13; http://dx.doi.org/10.1111/j.1399-3054.2009.01321.x; PMID: 20028478
  • Smertenko A, Franklin-Tong VE. Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Differ 2011; 18:1263 - 70; http://dx.doi.org/10.1038/cdd.2011.39; PMID: 21566662
  • Monshausen GB, Gilroy S. Feeling green: mechanosensing in plants. Trends Cell Biol 2009; 19:228 - 35; http://dx.doi.org/10.1016/j.tcb.2009.02.005; PMID: 19342240
  • Landrein B, Hamant O. How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 2013; 75:324 - 38; http://dx.doi.org/10.1111/tpj.12188; PMID: 23551516
  • Fluhr R. Reactive oxygen-generating NADPH oxidases in plants. In: Reactive oxygen species in plant signaling, signaling and communication in plants. del Ryo LA, Puppo A, eds. Heidelberg: Spinger-Verlag, 2009; 1-23.
  • Yao L-L, Zhou Q, Pei B-L, Li Y-Z. Hydrogen peroxide modulates the dynamic microtubule cytoskeleton during the defence responses to Verticillium dahliae toxins in Arabidopsis.. Plant Cell Environ 2011; 34:1586 - 98; http://dx.doi.org/10.1111/j.1365-3040.2011.02356.x; PMID: 21707649
  • Chang X, Nick P. Defence signalling triggered by Flg22 and Harpin is integrated into a different stilbene output in Vitis cells. PLoS One 2012; 7:e40446; http://dx.doi.org/10.1371/journal.pone.0040446; PMID: 22792328
  • Zhu Y, Zuo M, Liang Y, Jiang M, Zhang J, Scheller HV, Tan M, Zhang A. MAP65-1a positively regulates H2O2 amplification and enhances brassinosteroid-induced antioxidant defence in maize. J Exp Bot 2013; 64:3787 - 802; http://dx.doi.org/10.1093/jxb/ert215; PMID: 23956414
  • Zhang A, Zhang J, Ye N, Cao J, Tan M, Zhang J, Jiang M. ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroid-induced antioxidant defence in leaves of maize. J Exp Bot 2010; 61:4399 - 411; http://dx.doi.org/10.1093/jxb/erq243; PMID: 20693409
  • Livanos P, Galatis B, Gaitanaki C, Apostolakos P. Phosphorylation of a p38-like MAPK is involved in sensing cellular redox state and drives atypical tubulin polymer assembly in angiosperms. Plant Cell Environ 2013; •••; http://dx.doi.org/10.1111/pce.12222; PMID: 24138172
  • Rodriguez MC, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 2010; 61:621 - 49; http://dx.doi.org/10.1146/annurev-arplant-042809-112252; PMID: 20441529
  • Smertenko AP, Chang H-Y, Sonobe S, Fenyk SI, Weingartner M, Bögre L, Hussey PJ. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 2006; 119:3227 - 37; http://dx.doi.org/10.1242/jcs.03051; PMID: 16847052
  • Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Röhrig H, Weckwerth W, Conrath U, Beckers GJ. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Mol Cell Proteomics 2013; 12:369 - 80; http://dx.doi.org/10.1074/mcp.M112.020560; PMID: 23172892
  • Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis.. Plant Cell 2012; 24:4555 - 76; http://dx.doi.org/10.1105/tpc.112.104182; PMID: 23150630
  • Komis G, Quader H, Galatis B, Apostolakos P. Macrotubule-dependent protoplast volume regulation in plasmolysed root-tip cells of Triticum turgidum: involvement of phospholipase D. New Phytol 2006; 171:737 - 50; http://dx.doi.org/10.1111/j.1469-8137.2006.01784.x; PMID: 16918545
  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X. Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 2009; 21:2357 - 77; http://dx.doi.org/10.1105/tpc.108.062992; PMID: 19690149
  • Jiang J, Song C-P. MEK1/2 and p38-like MAP kinase successively mediate H(2)O(2) signaling in Vicia guard cell. Plant Signal Behav 2008; 3:996 - 8; PMID: 19704432
  • D’Souza JS, Johri MM. ABA and NaCl activate myelin basic kinase in the chloronema cells of the moss Funaria hygrometrica.. Plant Physiol Biochem 2002; 40:17 - 24; http://dx.doi.org/10.1016/S0981-9428(01)01344-4
  • Liu Y. Roles of mitogen-activated protein kinase cascades in ABA signaling. Plant Cell Rep 2012; 31:1 - 12; http://dx.doi.org/10.1007/s00299-011-1130-y; PMID: 21870109
  • Gianì S, Qin X, Faoro F, Breviario D. In rice, Oryzalin and abscisic acid differentially affect tubulin mRNA and protein levels. Planta 1998; 205:334 - 41; http://dx.doi.org/10.1007/s004250050328; PMID: 9640661
  • Jiang C-J, Nakajima N, Kondo N. Disruption of microtubules by abscisic acid in guard cells of Vicia faba L. Plant Cell Physiol 1996; 37:697 - 701; http://dx.doi.org/10.1093/oxfordjournals.pcp.a029001
  • 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 Physiol Plant Mol Biol 1994; 45:527 - 44; http://dx.doi.org/10.1146/annurev.pp.45.060194.002523
  • Baluška F, Volkmann D, Barlow PW. Hormone-cytoskeleton interactions in plant cells. In: Biochemistry and molecular biology of plant hormones. Hooykaas PJJ, Hall MA, Libbenga KR, eds. Amsterdam: Elsevier, 1999; 363-90.
  • Blume YB, Krasylenko YA, Yemets AI. Effects of phytohormones on the cytoskeleton of the plant cell. Russ J Plant Physiol 2012; 59:515 - 29; http://dx.doi.org/10.1134/S1021443712040036
  • Tognetti VB, Mühlenbock P, Van Breusegem F. Stress homeostasis - the redox and auxin perspective. Plant Cell Environ 2012; 35:321 - 33; http://dx.doi.org/10.1111/j.1365-3040.2011.02324.x; PMID: 21443606
  • Locascio A, Blázquez MA, Alabadí D. Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 2013; 23:804 - 9; http://dx.doi.org/10.1016/j.cub.2013.03.053; PMID: 23583555
  • Achard P, Renou J-P, Berthomé R, Harberd NP, Genschik P. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 2008; 18:656 - 60; http://dx.doi.org/10.1016/j.cub.2008.04.034; PMID: 18450450
  • Santa-María I, Smith MA, Perry G, Hernández F, Avila J, Moreno FJ. Effect of quinones on microtubule polymerization: a link between oxidative stress and cytoskeletal alterations in Alzheimer’s disease. Biochim Biophys Acta 2005; 1740:472 - 80; http://dx.doi.org/10.1016/j.bbadis.2004.11.024; PMID: 15949717
  • Ludueña RF. A hypothesis on the origin and evolution of tubulin. Int Rev Cell Mol Biol 2013; 302:41 - 185; http://dx.doi.org/10.1016/B978-0-12-407699-0.00002-9; PMID: 23351710
  • Landino LM, Hasan R, McGaw A, Cooley S, Smith AW, Masselam K, Kim G. Peroxynitrite oxidation of tubulin sulfhydryls inhibits microtubule polymerization. Arch Biochem Biophys 2002; 398:213 - 20; http://dx.doi.org/10.1006/abbi.2001.2729; PMID: 11831852
  • Wang H, Wang S, Lu Y, Alvarez S, Hicks LM, Ge X, Xia Y. Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis.. J Proteome Res 2012; 11:412 - 24; http://dx.doi.org/10.1021/pr200918f; PMID: 22050424
  • Dixon DP, Skipsey M, Grundy NM, Edwards R. Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 2005; 138:2233 - 44; http://dx.doi.org/10.1104/pp.104.058917; PMID: 16055689
  • Rouhier N, Lemaire SD, Jacquot J-P. The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annu Rev Plant Biol 2008; 59:143 - 66; http://dx.doi.org/10.1146/annurev.arplant.59.032607.092811; PMID: 18444899
  • Clark HM, Hagedorn TD, Landino LM. Hypothiocyanous acid oxidation of tubulin cysteines inhibits microtubule polymerization. Arch Biochem Biophys 2014; 541:67 - 73; http://dx.doi.org/10.1016/j.abb.2013.10.026; PMID: 24215946
  • Landino LM, Moynihan KL, Todd JV, Kennett KL. Modulation of the redox state of tubulin by the glutathione/glutaredoxin reductase system. Biochem Biophys Res Commun 2004; 314:555 - 60; http://dx.doi.org/10.1016/j.bbrc.2003.12.126; PMID: 14733943
  • Ban Y, Kobayashi Y, Hara T, Hamada T, Hashimoto T, Takeda S, Hattori T. α-tubulin is rapidly phosphorylated in response to hyperosmotic stress in rice and Arabidopsis. Plant Cell Physiol 2013; 54:848 - 58; http://dx.doi.org/10.1093/pcp/pct065; PMID: 23628996
  • Nick P. Why to spend tax money on plant microtubules? In: Applied Plant Cell Biology. Nick P, Opatrný Z. eds. Plant Cell Monographs. Berlin: Springer-Verlag, 2014; 22:39-67.
  • Cai G. Assembly and disassembly of plant microtubules: tubulin modifications and binding to MAPs. J Exp Bot 2010; 61:623 - 6; http://dx.doi.org/10.1093/jxb/erp395; PMID: 20080825
  • Fosket DE, Morejohn LC. Structural and functional organization of tubulin. Annu Rev Plant Physiol Plant Mol Biol 1992; 43:201 - 40; http://dx.doi.org/10.1146/annurev.pp.43.060192.001221
  • Hepler PK, Hush JM. Behavior of microtubules in living plant cells. Plant Physiol 1996; 112:455 - 61; PMID: 12226402
  • Burk DH, Zhong R, Ye Z-H. The katanin microtubule severing protein in plants. J Integr Plant Biol 2007; 49:1174 - 82; http://dx.doi.org/10.1111/j.1672-9072.2007.00544.x
  • Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R, Ketelaar T, Emons AM, Mulder BM, Kirik V, Ehrhardt DW. A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 2013; 342:1245533; http://dx.doi.org/10.1126/science.1245533; PMID: 24200811
  • Wen F, Xing D, Zhang L. Hydrogen peroxide is involved in high blue light-induced chloroplast avoidance movements in Arabidopsis.. J Exp Bot 2008; 59:2891 - 901; http://dx.doi.org/10.1093/jxb/ern147; PMID: 18550599
  • Panteris E, Komis G, Adamakis I-DS, Šamaj J, Bosabalidis AM. MAP65 in tubulin/colchicine paracrystals of Vigna sinensis root cells: possible role in the assembly and stabilization of atypical tubulin polymers. Cytoskeleton (Hoboken) 2010; 67:152 - 60; PMID: 20217678
  • Mao T, Jin L, Li H, Liu B, Yuan M. Two microtubule-associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiol 2005; 138:654 - 62; http://dx.doi.org/10.1104/pp.104.052456; PMID: 15908607
  • Smertenko AP, Kaloriti D, Chang H-Y, Fiserova J, Opatrny Z, Hussey PJ. The C-terminal variable region specifies the dynamic properties of Arabidopsis microtubule-associated protein MAP65 isotypes. Plant Cell 2008; 20:3346 - 58; http://dx.doi.org/10.1105/tpc.108.063362; PMID: 19060108

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