A single amino-acid substitution at lysine 40 of an arabidopsis thalianaα-tubulin causes extensive cell proliferation and expansion defects

Journal of Integrative Plant Biology

Volumn 55, Issue 3, 2013, Pages 209-220

  Xiong, Xue ^a,b   Xu, Deyang ^a   Yang, Zhongnan ^b   Huang, Hai ^a   Cui, Xiaofeng ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b SHANGHAI NORMAL UNIVERSITY   (China)

Author keywords

tubulin; Arabidopsis; Cell proliferation; Expansion; Microtubule

Indexed keywords

ARABIDOPSIS PROTEIN; TUBULIN;

AMINO ACID; CELL ORGANELLE; EUKARYOTE; PHENOTYPE; PLANT; POLYMER; SUBSTITUTION;

ARABIDOPSIS; ARTICLE; CELL PROLIFERATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROTUBULE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL PROLIFERATION; GENE EXPRESSION REGULATION, PLANT; MICROTUBULES; PLANTS, GENETICALLY MODIFIED; TUBULIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA; VERTEBRATA;

EID: 84874766820     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12003     Document Type: Article

References (53)

1. Abe T, Hashimoto T (2005) Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant J. 43, 191-204.
2. Akella JS, Wloga D, Kim J, Starostina NG, Lyons-Abbott S, Morrissette NS, Dougan ST, Kipreos ET, Gaertig J (2010) MEC-17 is an alpha-tubulin acetyltransferase. Nature 467, 218-222.
3. Ambrose JC, Cyr R (2008) Mitotic spindle organization by the preprophase band. Mol. Plant 1, 950-960.
4. Astrom H (1992) Acetylated alpha-tubulin in the pollen tube microtubules. Cell Biol. Int. Rep. 16, 871-881.
5. Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: A review and a model. Protoplasma 215, 150-171.
6. Baskin TI, Wilson JE, Cork A, Williamson RE (1994) Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant Cell Physiol. 35, 935-942.
7. Black MM, Keyser P (1986) Acetylation of alpha-tubulin (alpha-tub) in cultured neurons. J. Cell Biol. 103, A128-A128.
8. Black MM, Keyser P (1987) Acetylation of alpha-tubulin in cultured neurons and the induction of alpha-tubulin acetylation in PC12 cells by treatment with nerve growth factor. J. Neurosci. 7, 1833-1842.
9. Buschmann H, Lloyd CW (2008) Arabidopsis mutants and the network of microtubule-associated functions. Mol. Plant 1, 888-898.
10. Carpenter JL, Ploense SE, Snustad DP, Silflow CD (1992) Preferential expression of an alpha-tubulin gene of Arabidopsis in pollen. Plant Cell 4, 557-571.
11. Chen C, Wang S, Huang H (2000) LEUNIG has multiple functions in gynoecium development in Arabidopsis. Genesis 26, 42-54.
12. Chen S, Songkumarn P, Liu J, Wang GL (2009) A versatile zero background T-vector system for gene cloning and functional genomics. Plant Physiol. 150, 1111-1121.
13. Chu CW, Hou FJ, Zhang JM, Phu L, Loktev AV, Kirkpatrick DS, Jackson PK, Zhao YM, Zou H (2011) A novel acetylation of beta-tubulin by San modulates microtubule polymerization via down-regulating tubulin incorporation. Mol. Biol. Cell 22, 448-456.
14. Conacci-Sorrell M, Ngouenet C, Eisenman RN (2010) Myc-Nick: A cytoplasmic cleavage product of Myc that promotes alpha-tubulin acetylation and cell differentiation. Cell 142, 480-493.
15. Creppe C, Malinouskaya L, Volvert ML, Gillard M, Close P, Malaise O, Laguesse S, Cornez I, Rahmouni S, Ormenese S, Belachew S, Malgrange B, Chapelle JP, Siebenlist U, Moonen G, Chariot A, Nguyen L (2009) Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136, 551-564.
16. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, Humbert S, Saudou F (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 27, 3571-3583.
17. Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4, 199-211.
18. Gaertig J, Wloga D (2008) Ciliary tubulin and its post-translational modifications. Curr. Top. Dev. Biol. 85, 83-113.
19. Giannoutsou E, Galatis B, Zachariadis M, Apostolakos P (2012) Formation of an endoplasmic reticulum ring associated with acetylated microtubules in the angiosperm preprophase band. Cytoskeleton (Hoboken) 69, 252-265.
20. Greer K, Maruta H, L'Hernault SW, Rosenbaum JL (1985) Alpha-tubulin acetylase activity in isolated Chlamydomonas flagella. J. Cell Biol. 101, 2081-2084.
21. Greer K, Rosenbaum J (1988) An hypothesis on the significance of acetylation of alpha tubulin. Cell Motil. Cytoskel. 11, 206-206.
22. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, 797-806.
23. Hammond JW, Cai D, Verhey KJ (2008) Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20, 71-76.
24. Hashimoto T (2003) Dynamics and regulation of plant interphase microtubules: A comparative view. Curr. Opin. Plant Biol. 6, 568-576.
25. Huang RF, Lloyd CW (1999) Gibberellic acid stabilises microtubules in maize suspension cells to cold and stimulates acetylation of alpha-tubulin. FEBS Lett. 443, 317-320.
26. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, Yoshida M, Wang XF, Yao TP (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458.
27. Janke C, Kneussel M (2010) Tubulin post-translational modifications: Encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci. 33, 362-372.
28. Kaloriti D, Galva C, Parupalli C, Khalifa N, Galvin M, Sedbrook JC (2007) Microtubule associated proteins in plants and the processes they manage. J. Integr. Plant Biol. 49, 1164-1173.
29. Kopczak SD, Haas NA, Hussey PJ, Silflow CD, Snustad DP (1992) The small genome of Arabidopsis contains at least six expressed alpha-tubulin genes. Plant Cell 4, 539-547.
30. L'Hernault SW, Rosenbaum JL (1985) Chlamydomonas alpha-tubulin is posttranslationally modified by acetylation on the epsilon-amino group of a lysine. Biochemistry 24, 473-478.
31. LeDizet M, Piperno G (1987) Identification of an acetylation site of Chlamydomonas alpha-tubulin. Proc. Natl. Acad. Sci. USA 84, 5720-5724.
32. Lloyd C, Chan J (2006) Not so divided: The common basis of plant and animal cell division. Nat. Rev. Mol. Cell Biol. 7, 147-152.
33. Maruta H, Greer K, Rosenbaum JL (1986) The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J. Cell Biol. 103, 571-579.
34. Mathur J, Hulskamp M (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr. Biol. 12, R669-R676.
35. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D, Osada H, Komatsu Y, Nishino N, Khochbin S, Horinouchi S, Yoshida M (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831.
36. +-dependent tubulin deacetylase. Mol. Cell 11, 437-444.
37. Ohkawa N, Sugisaki S, Tokunaga E, Fujitani K, Hayasaka T, Setou M, Inokuchi K (2008) N-acetyltransferase ARD1-NAT1 regulates neuronal dendritic development. Genes Cells 13, 1171-1183.
38. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491-1495.
39. Perdiz D, Mackeh R, Pous C, Baillet A (2011) The ins and outs of tubulin acetylation: More than just a post-translational modification Cell. Signal. 23, 763-771.
40. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16, 2166-2172.
41. Sedbrook JC, Kaloriti D (2008) Microtubules, MAPs and plant directional cell expansion. Trends Plant Sci. 13, 303-310.
42. Shea TB, Beermann ML, Nixon RA (1990) Post-translational modification of alpha-tubulin by acetylation and detyrosination in NB2a/d1 neuroblastoma cells. Brain Res. Dev. Brain Res. 51, 195-204.
43. Shida T, Cueva JG, Xu Z, Goodman MB, Nachury MV (2010) The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc. Natl. Acad. Sci. USA 107, 21517-21522.
44. Smertenko A, Blume Y, Viklicky V, Opatrny Z, Draber P (1997) Post-translational modifications and multiple tubulin isoforms in Nicotiana tabacum L. cells. Planta 201, 349-358.
45. Snustad DP, Haas NA, Kopczak SD, Silflow CD (1992) The small genome of Arabidopsis contains at least nine expressed beta-tubulin genes. Plant Cell 4, 549-556.
46. Solinger JA, Paolinelli R, Kloss H, Scorza FB, Marchesi S, Sauder U, Mitsushima D, Capuani F, Sturzenbaum SR, Cassata G (2010) The Caenorhabditis elegans Elongator complex regulates neuronal alpha-tubulin acetylation. PLoS Genet. 6, e1000820.
47. Tran HT, Nimick M, Uhrig RG, Templeton G, Morrice N, Gourlay R, Delong A, Moorhead GB (2012) Arabidopsis thaliana histone deacetylase 14 (HDA14) is an alpha-tubulin deacetylase that associates with PP2A and enriches in the microtubule fraction with the putative histone acetyltransferase ELP3. Plant J. 71, 263-272.
48. Wang L, Gu X, Xu D, Wang W, Wang H, Zeng M, Chang Z, Huang H, Cui X (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J. Exp. Bot. 62, 761-773.
49. Wang W, Vignani R, Scali M, Sensi E, Cresti M (2004) Post-translational modifications of alpha-tubulin in Zea mays L. are highly tissue specific. Planta 218, 460-465.
50. Westermann S, Weber K (2003) Post-translational modifications regulate microtubule function. Nat. Rev. Mol. Cell Biol. 4, 938-947.
51. Yuan Z, Luo D, Li G, Yao X, Wang H, Zeng M, Huang H, Cui X (2010) Characterization of the AE7 gene in Arabidopsis suggests that normal cell proliferation is essential for leaf polarity establishment. Plant J. 64, 331-342.
52. Zhang Y, Li N, Caron C, Matthias G, Hess D, Khochbin S, Matthias P (2003) HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 22, 1168-1179.
53. Zilberman Y, Ballestrem C, Carramusa L, Mazitschek R, Khochbin S, Bershadsky A (2009) Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J. Cell Sci. 122, 3531-3541.