Abscisic acid induces ectopic outgrowth in epidermal cells through cortical microtubule reorganization in Arabidopsis thaliana

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Takatani, Shogo ^a   Hirayama, Takashi ^a   Hashimoto, Takashi ^b   Takahashi, Taku ^a   Motose, Hiroyasu ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID;

ARABIDOPSIS; DRUG EFFECTS; GERMINATION; METABOLISM; MICROTUBULE; PHYSIOLOGY; PLANT EPIDERMIS;

ABSCISIC ACID; ARABIDOPSIS; GERMINATION; MICROTUBULES; PLANT EPIDERMIS;

EID: 84931275096     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11364     Document Type: Article

References (59)

1. Wasteneys, G. O. & Ambrose, J. C. Spatial organization of plant cortical microtubules: Close encounters of the 2D kind. Trend. Cell Sci. 19, 62-71 (2009
2. Hamant, O. et al. Developmental patterning by mechanical signals in Arabidopsis. Science 322, 1650-1655 (2008
3. Uyttewaal, M. et al. Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439-451 (2012
4. Lindeboom, J. J. et al. A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342, 1245533. doi: 10.1126/science.1245533 (2013
5. Ambrose, C., Allard, J. F., Cytrynbaum, E. N. & Wasteneys, G. O. A CLASP-modulated cell edge barrier mechanism drives cellwide cortical microtubule organization in Arabidopsis. Nat. Commun. 2, 430 (2011
6. Baskin, T. I., Wilson, J. E., Cork, A. & Williamson, R. E. Morphology and microtubule organization in Arabidopsis roots exposed to oryzalin or taxol. Plant Cell Physiol. 35, 935-942 (1994
7. Ishida, T., Kaneko, Y., Iwano, M. & Hashimoto, T. Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104, 8544-8549 (2007
8. Furutani, I. et al. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127, 4443-4453 (2000
9. Buschmann, H. et al. Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14, 1515-1521 (2004
10. Nakajima, K., Furutani, I., Tachimoto, H., Matsubara, H. & Hashimoto, T. SPIRAL1 encodes a plant-specific microtubulelocalized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16, 1178-1190 (2004
11. Sedbrook, J. C., Ehrhardt, D. W., Fisher, S. E., Scheible, W. R. & Somerville, C. R. The Arabidopsis SKU6/SPIRAL1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16, 1506-1520 (2004
12. Shoji, T. et al. Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol. 136, 3933-3944 (2004
13. Yao, M., Wakamatsu, Y., Itoh, T. J., Shoji, T. & Hashimoto, T. Arabidopsis SPIRAL2 promotes uninterrupted microtubule growth by suppressing the pause state of microtubule dynamics. J Cell Sci. 121, 2372-2381 (2008
14. 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 Biol. 45, 527-544 (1994
15. Takesue, K. & Shibaoka, H. The cyclic reorientation of cortical microtubules in epidermal cells of azuki bean epicotyls: The role of actin filaments in the progression of the cycle. Planta 205, 539-546 (1998
16. Takesue, K. & Shibaoka, H. Auxin-induced longitudinal-to-transverse reorientation of cortical microtubules in nonelongating epidermal cells of azuki bean epicotyls. Protoplasma 206, 27-30 (1999
17. Vineyard, L., Elliott, A., Dhingra, S., Lucas, J. R. & Shaw, S. L. Progressive transverse microtubule array organization in hormoneinduced Arabidopsis hypocotyl cells. Plant Cell 25, 662-676 (2013
18. Roberts, I. N., Lloyd, C. W. & Roberts, K. Ethylene-induced microtubule reorientations-Mediation by helical arrays. Planta 164, 439-447 (1985
19. Sassi, M. et al. An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis. Curr. Biol. 24, 2335-2342 (2014
20. Shinozaki, K. & Yamaguchi-Shinozaki, K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221-227 (2007
21. Hirayama, T. & Shinozaki, K. Research on plant abiotic stress responses in the post-genome era: Past, present and future. Plant J. 61, 1041-1052 (2010
22. Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R. & Abrams, S. R. Abscisic acid: Emergence of a core signaling network. Ann. Rev. Plant Biol. 61, 651-679 (2010
23. Ma, Y. et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068 (2009
24. Park, S. Y. et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071 (2009
25. Umezawa, T. et al. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl Acad. Sci. USA 41, 17588-17593 (2009
26. Sakiyama, M. & Shibaoka, H. Effects of abscisic acid on the orientation and cold stability of cortical microtubules in epicotyls of the dwarf pea. Protoplasma 157, 165-171 (1990
27. Sakiyama-Sogo, M. & Shibaoka, H. Gibberellin A3 and abscisic acid cause the reorientation of cortical microtubules in epicotyls of the decapitated dwarf pea. Plant Cell Physiol. 34, 431-437 (1993
28. Ishida, K. & Katsumi, M. Effects of gibberellin and abscisic acid on the cortical microtubule orientation in hypocotyl cells of light-grown cucumber seedlings. Int. J. Plant Sci. 153, 155-163 (1992
29. Da Silva, E. A. A., Toorop, P. E., Van Lammeren, A. A. M. & Hilhorst, H. W. M. ABA inhibits embryo cell expansion and early cell division events during coffee (Coffea arabica 'Rubi') seed germination. Ann. Bot. 102, 425-433 (2008
30. Eisinger, W., Ehrhardt, D. & Briggs, W. Microtubules are essential for guard-cell function in Vicia and Arabidopsis. Mol. Plant. 5, 601-610 (2012
31. Jiang, Y. et al. Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis. Planta 239, 565-575 (2014
32. Motose, H., Tominaga, R., Wada, T., Sugiyama, M. & Watanabe, Y. A NIMA-related protein kinase suppresses ectopic outgrowth of epidermal cells through its kinase activity and the association with microtubules. Plant J. 54, 829-844 (2008
33. Sakai, T. et al. Armadillo repeat-containing kinesins and a NIMA-related kinase are required for epidermal-cell morphogenesis in Arabidopsis. Plant J. 53, 157-171 (2008
34. Motose, H. et al. NIMA-related kinases 6, 4, and 5 interact with each other to regulate microtubule organization during epidermal cell expansion in Arabidopsis thaliana. Plant J. 67, 993-1005 (2011
35. Motose, H., Takatani, S., Ikeda, T. & Takahashi, T. NIMA-related kinases regulate directional cell growth and organ development through microtubule function in Arabidopsis thaliana. Plant Signal. Behav. 7, 1552-1555 (2012
36. Lee, S. J., Cho, D. I., Kang, J. Y., Kim, M. D. & Kim, S. Y. AtNEK6 interacts with ARIA and is involved in ABA response during seed germination. Mol. Cells, 29, 559-566 (2010
37. Zhang, B. et al. NIMA-related kinase NEK6 affects plant growth and stress response in Arabidopsis. Plant J. 68, 830-843 (2011
38. Gendreau, E. et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295-305 (1997
39. Hung, C. Y. et al. Common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol. 117, 73-84 (1998
40. Berger, F., Linstead, P., Dolan, L. & Haseloff, J. Stomata patterning on the hypocotyl of Arabidopsis thaliana is controlled by genes involved in the control of root epidermis patterning. Dev Biol. 194, 226-234 (1998
41. Nishimura, N. et al. Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant Cell Physiol. 45, 1485-1499 (2004
42. Nishimura, N. et al. Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J. 44, 972-984 (2005
43. Yoshida, T. et al. ABA-Hypersensitive Germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol. 140, 115-126 (2006
44. Nishimura, N. et al. ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signaling in Arabidopsis seed. Plant J. 50, 935-949 (2007
45. Nishimura, N. et al. ABA hypersensitive germination2-1 causes the activation of both abscisic acid and salicylic acid responses in Arabidopsis. Plant Cell Physiol. 50, 2112-2122 (2009
46. Hirayama, T. et al. A poly(A)-specific ribonuclease directly regulates the poly(A) status of mitochondrial mRNA in Arabidopsis. Nat. Commun. 4, 2247 (2013
47. Hartman, J. J. et al. Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93, 277-287 (1998
48. Bouquin, T., Mattsson, O., Næsted, H., Foster, R. & Mundy, J. The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J. Cell Sci. 116, 791-801 (2003
49. Naoi, K. & Hashimoto, T. A semidominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization. Plant Cell 16, 1841-1853 (2004
50. Fujita, S. et al. An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Curr. Biol. 23, 1969-1978 (2013
51. Nakamura, M., Naoi, K., Shoji, T. & Hashimoto, T. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol. 45, 1330-1334 (2004
52. Nakamura, M. et al. Characterization of the class IV homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiol. 141, 1363-1375 (2006
53. Kim, S. et al. ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol. 136, 3639-3648 (2004
54. Nakamura, M. Enhardt, D. & Hashimoto, T. Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12, 1064-1070 (2010
55. Hamada, T. et al. Purification and characterization of novel microtubule-associated proteins from Arabidopsis cell suspension cultures. Plant Physiol. 163, 1804-1816 (2013
56. Sharp, R. E., LeNoble, M. E., Else, M. A., Thorne, E. T. & Gherardi, F. Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: Evidence for an interaction with ethylene. J. Exp. Bot. 51, 1575-1584 (2000
57. LeNoble, M. E., Spollen, W. G. & Sharp, R. E. Maintenance of shoot growth by endogenous ABA: Genetic assessment of the involvement of ethylene suppression. J. Exp. Bot. 55, 237-245 (2004
58. Barrero, J. M. et al. A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J. Exp. Bot. 56, 2071-2083 (2005
59. Sugimoto, H. et al. Overexpression of a novel Arabidopsis PP2C isoform, AtPP2CF1, enhances plant biomass production by increasing inflorescence stem growth. J. Exp. Bot. 65, 5385-5400 (2014).