Scientia Agricultura Sinica ›› 2012, Vol. 45 ›› Issue (21): 4351-4360.doi: 10.3864/j.issn.0578-1752.2012.21.003

• TILLAGE & CULTIVATION·PHYSIOLOGY & BIOCHEMISTRY·AGRICULTURE INFORMATION TECHNOLOGY • Previous Articles     Next Articles

Microtubules in Guard Cells Involve in Serine/Threonine Phosphorylation During Stomatal Movement

 YE  Zi, HUANG  Cong-Cong, YU  Rong   

  1. 1.首都师范大学生命科学学院,北京100048
  • Received:2012-06-14 Online:2012-11-01 Published:2012-08-23

Abstract: 【Objective】 The interaction between microtubules (MTs) and protein serine/threonine phosphorylation in guard cells was investigated in order to provide a reliable evidence for better understanding of the mechanism of stomatal movment. 【Method】Pharmacological analysis, confocal laser scanning microscopy, and western blotting were used to explore the possible interaction of these two elements. 【Result】 In vivo stomatal aperture assays revealed that staurosporine (STS), one well-known specific inhibitor of serine/threonine protein kinase, enhanced the light-induced stomatal opening. While, okadaic acid (OA) and calyculin A (CalA), another two inhibitors of 1/2A phosphatase, showed the opposite effects under the same condition. In addition, it was found that these changes of stomatal movement could be reversed or became intensified to some extent when microtubule-specific drug, taxol or vinblastine was present during the treatments above. Furthermore, OA and CalA also had significant influences on the MT organization in the opening guard cells. In the presence of OA or CalA, the fine radial MT arrays tended to be broken down or rearranged into random network. And guard cells kept in STS showed increase in radial MT arrays and stomatal aperture. MT-targeted drugs, taxol and vinblastine, also altered the effects of three inhibitors (OA, CalA, STS) on MT organization partiallly in a similar manner. Immunoblot detection of total extract from guard cells confirmed that tubulin-subunits were phosphorylated on serine. 【Conclusion】 The results suggest that reversible protein serine/threonine phosphorylation may regulate the MT dynamics of guard cells during stomatal movement.

Key words: microtubule, protein serine/threonine phosphorylation, stomatal movement

[1]马鲜歌, 贺军民. 异三聚体G-蛋白在UV-B诱导拟南芥气孔关闭中的作用. 中国农业科学,2012,45(5): 848-853.

Ma X G, He J M. Role of heterotrimeric G protein in UV-B-induced Arabidopsis stomatal closure. Scientia Agricultura Sinica, 2012, 45(5): 848-853. ( in Chinese)

[2]Kohler B, Blatt M R. Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant Journal, 2002, 32:185-194.

[3]MacRobbie E A C. Evidence for a role for protein tyrosine phosphatase in the control of ion release from the guard cell vacuole in stomatal closure. Proceedings of the National Academy of Science, USA, 2002, 9(18): 11963-11968.

[4]Takemiya A, Kinoshita T, Asanuma M, Shimazaki K. Protein phosphatase 1 positively regulates stomatal opening in response to blue light in Vicia faba. Proceedings of the National Academy of Science, USA, 2006, 103(36): 13549-13554.

[5]Sokolovski S, Hills A, Gay R, Garcia-Mata C, Lamattina L, Blatt M R. Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant Journal, 2005, 43: 520-529.

[6]Burnett E C, Desikan R, Moser R C, Neill S J. ABA activation of an MBP kinase in Pisum sativum epidermal peels correlates with stomatal responses to ABA. Journal of Experimental Botany, 2000, 51(343):197-205.

[7]Gudesblat G E, Iusem N D, Morris P C. Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to ABA and hydrogen peroxide. New Phytologist, 2007, 173(4): 713-721.

[8]MacRobbie E A C, Kurup S. Signalling mechanisms in the regulation of vacuolar ion release in guard cell. New Phytologist, 2007, 175:630-640.

[9]Kim M, Hepler P K, Eun S O, Lee Y. Actin filaments in mature guard cells are radially distributed and involved in stomatal movement. Plant Physiology, 1995, 109: 1077-1084.

[10]Dzierzynska A. The role of cytoskeleton in stomata functioning. Acta Physiologiae Plantarum, 2006, 28(1):59-79.

[11]Lahav M, Abu-Abied M, Belausov E, Schwartz A, Sadot E. Microtubules of guard cells are light sensitive. Plant Cell Physiology, 2004, 45:573-582.

[12]Marcus A I, Moore R C, Cyr R J. The role of microtubules in guard cell function. Plant Physiology, 2001, 125:387-395.

[13]Yu R, Huang R F, Wang X C, Yuan M. Microtubule dynamics are involved in stomatal movement of Vicia faba L. Protoplasma, 2001, 21:113-118.

[14]Zhang W, Fan L M, Wu W H. Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiology, 2007, 143:1140-1151.

[15]Wang X L, Gao X Q, Wang X C. Stochastic dynamics of actin filaments in guard cells regulating chloroplast localization during stomatal movement. Plant Cell and Environment, 2011, 34: 1248-1257.

[16]Higaki T, Kutsuna N, Sano T, Kondo N, Hasezawa S. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. The Plant Journal, 2010, 61:156-165.

[17]Hwang J U, Lee Y. Abscisic acid-induced actin reorganization in guard cells of dayflower is mediated by cytosolic calcium levels and by protein kinase and protein phosphatase activities. Plant Physiology, 2001, 125:2120-2128.

[18]Pandey S, Wang X Q, Coursol S A, Assmann S M. Preparation and applications of Arabidopsis thaliana guard cell protoplasts. New Phytologist, 2002, 153: 517-526.

[19]Blume Y, Yemets A, Sulimenko V, Sulimenko T, Chan J, Lloyd C, Draber P. Tyrosine phosphorylation of plant tubulin. Planta, 2008, 229:143-150.

[20]Rudrabhatla, Pei Z M. Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Molecular Biology, 2006, 60:293-319.

[21]Zi H J, Xiang Y, Li M, Wang T, Ren H Y. Reversible protein tyrosine phosphorylation affects pollen germination and pollen tube growth via the actin cytoskeleton. Protoplasma, 2007, 230:183-191.

[22]Eisinger W, Ehrhardt D, Briggs W. Microtubules are essential for guard-cell function in Vicia and Arabidopsis. Molecular Plant, 2012, 5(3):601-610.

[23]Zhang Y M, Wu Z Y, Wang X C, Yu R. Rearrangement of microtubule cytoskelenton in stomatal closure of Arabibopsis induced by nitric oxide. Chinese Science Bulletin, 2008, 53:848-852.

[24]Mizuno K. Induction of cold stability of microtubules in cultured tobacco cells. Plant Physiology, 1992, 100: 740-748.

[25]Ayaydin F, Vissi E, Mészáros T, Miskolczi P, Kovács I, Fehér A, Dombrádi V, Erdödi F, Gergely P, Dudits D. Inhibition of serine/threonine-specific protein phosphatases causes premature activation of cdc2MsF kinase at G2/M transition and early mitotic microtubule organisation in alfalfa. Plant Journal, 2000, 23: 85-96.

[26]Yemets A, Sheremet Y, Vissenberg K, Van Orden J, Verbelen J P, Blume Y B. Effects of tyrosine kinase and phosphatase inhibitors on microtubules in Arabidopsis root cells. Cell Biology International, 2008, 32: 630-637.

[27]Li W, Luan S, Schreiber S L, Assmann S M. Evidence for protein phosphatase 1 and 2A regulation of K+ channels in two types of leaf cells. Plant Physiology, 1994, 106: 963-970.

[28]Schmidt C, Schelle I, Liao Y J, Schroeder J I. Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. Proceedings of the National Academy of Science, USA, 1995, 92: 9535-9539.

[29]Liu B Q, Jin L F, Zhu L, Li J J, Huang S L, Yuan M. Phosphorylation of microtubule-associated protein SB401 from Solanum berthaultii regulates its effect on microtubules. Journal of Integrative Plant Biology, 2009, 51(3):235-242.

[30]Smertenko A P, Chang H Y, Sonobe S, Fenyk S I, Weingartner M, Bögre L, Hussey P J. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. Journal of Cell Science, 2006, 119:3227-3237.

[31]Fourest-Lieuvin A, Peris L, Gache V, Garcia-Saez I, Juillan-Binard C, Lantez V, Job D. Microtubule regulation in mitosis: tubulin phosphorylation by the cyclin-dependent kinase Cdk1. Molecular Biology of the Cell, 2006, 17:1041-1050.

[32]Nissan G B, Cui W, Kim D J, Yang Y D, Yoo B C, Lee J Y. Arabidopsis Casein Kinase 1-Like 6 contains a microtubule-bingding domain and affects the organization of cortical microtubules. Plant Physiology, 2008, 148:1897-1907.
[1] LI Hui-Min-12, HU Jie-1, HE Jun-Min-1. Effect of Phosphatidylinositol 3-Phosphate on UV-B-Induced H2O2 Production in Guard Cells and Stomatal Closure of Broad Bean [J]. Scientia Agricultura Sinica, 2013, 46(20): 4246-4253.
[2] MA Xian-Ge, HE Jun-Min. Role of Heterotrimeric G Protein in UV-B-Induced Arabidopsis Stomatal Closure [J]. Scientia Agricultura Sinica, 2012, 45(5): 848-853.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!