First published online December 29, 2005; 10.1104/pp.105.075119
Plant Physiology 140:746-760 (2006)
© 2006 American Society of Plant Biologists
CELL BIOLOGY AND SIGNAL TRANSDUCTION
A Universal Role for Inositol 1,4,5-Trisphosphate-Mediated Signaling in Plant Gravitropism1,[W]
Imara Y. Perera*,
Chiu-Yueh Hung,
Shari Brady,
Gloria K. Muday and
Wendy F. Boss
Department of Botany, North Carolina State University, Raleigh, North Carolina 27695–7612 (I.Y.P., C.-Y.H., W.F.B.); and Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109–7325 (S.B., G.K.M.)
Inositol 1,4,5-trisphosphate (InsP3) has been implicated in the early signaling events of plants linking gravity sensing to the initiation of the gravitropic response. However, at present, the contribution of the phosphoinositide signaling pathway in plant gravitropism is not well understood. To delineate the role of InsP3 in plant gravitropism, we generated Arabidopsis (Arabidopsis thaliana) plants constitutively expressing the human type I inositol polyphosphate 5-phosphatase (InsP 5-ptase), an enzyme that specifically hydrolyzes InsP3. The transgenic plants show no significant differences in growth and life cycle compared to wild-type plants, although basal InsP3 levels are reduced by greater than 90% compared to wild-type plants. With gravistimulation, InsP3 levels in inflorescence stems of transgenic plants show no detectable change, whereas in wild-type plant inflorescences, InsP3 levels increase approximately 3-fold within the first 5 to 15 min of gravistimulation, preceding visible bending. Furthermore, gravitropic bending of the roots, hypocotyls, and inflorescence stems of the InsP 5-ptase transgenic plants is reduced by approximately 30% compared with the wild type. Additionally, the cold memory response of the transgenic plants is attenuated, indicating that InsP3 contributes to gravisignaling in the cold. The transgenic roots were shown to have altered calcium sensitivity in controlling gravitropic response, a reduction in basipetal indole-3-acetic acid transport, and a delay in the asymmetric auxin-induced  -glucuronidase expression with gravistimulation as compared to the controls. The compromised gravitropic response in all the major axes of growth in the transgenic Arabidopsis plants reveals a universal role for InsP3 in the gravity signal transduction cascade of plants.
1 This work was supported by the National Aeronautics and Space Administration (grant no. NAGW–4984 awarded to the Specialized Center of Research and Training in Gravitational Biology at North Carolina State University and grant no. NAG2–1502 to I.Y.P.)
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Imara Y. Perera (imara_perera{at}ncsu.edu).
[W] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.075119.
* Corresponding author; e-mail imara_perera{at}ncsu.edu; fax 919–515–3436.
Received December 5, 2005;
returned for revision December 5, 2005;
accepted December 13, 2005.
This article has been cited by other articles:
|
|
|
|
 
Z. Barjaktarovic, W. Schutz, J. Madlung, C. Fladerer, A. Nordheim, and R. Hampp
Changes in the effective gravitational field strength affect the state of phosphorylation of stress-related proteins in callus cultures of Arabidopsis thaliana
J. Exp. Bot.,
March 1, 2009;
60(3):
779 - 789.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. A. Ananieva, G. E. Gillaspy, A. Ely, R. N. Burnette, and F. L. Erickson
Interaction of the WD40 Domain of a Myoinositol Polyphosphate 5-Phosphatase with SnRK1 Links Inositol, Sugar, and Stress Signaling
Plant Physiology,
December 1, 2008;
148(4):
1868 - 1882.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Y. Perera, C.-Y. Hung, C. D. Moore, J. Stevenson-Paulik, and W. F. Boss
Transgenic Arabidopsis Plants Expressing the Type 1 Inositol 5-Phosphatase Exhibit Increased Drought Tolerance and Altered Abscisic Acid Signaling
PLANT CELL,
October 1, 2008;
20(10):
2876 - 2893.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Mosblech, S. Konig, I. Stenzel, P. Grzeganek, I. Feussner, and I. Heilmann
Phosphoinositide and Inositolpolyphosphate Signalling in Defense Responses of Arabidopsis thaliana Challenged by Mechanical Wounding
Mol Plant,
March 1, 2008;
1(2):
249 - 261.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Toyota, T. Furuichi, H. Tatsumi, and M. Sokabe
Cytoplasmic Calcium Increases in Response to Changes in the Gravity Vector in Hypocotyls and Petioles of Arabidopsis Seedlings
Plant Physiology,
February 1, 2008;
146(2):
505 - 514.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Konig, A. Mosblech, and I. Heilmann
Stress-inducible and constitutive phosphoinositide pools have distinctive fatty acid patterns in Arabidopsis thaliana
FASEB J,
July 1, 2007;
21(9):
1958 - 1967.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. J. Im, I. Y. Perera, I. Brglez, A. J. Davis, J. Stevenson-Paulik, B. Q. Phillippy, E. Johannes, N. S. Allen, and W. F. Boss
Increasing Plasma Membrane Phosphatidylinositol(4,5)Bisphosphate Biosynthesis Increases Phosphoinositide Metabolism in Nicotiana tabacum
PLANT CELL,
May 1, 2007;
19(5):
1603 - 1616.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. F. M. Abreu and F. J. L. Aragao
Isolation and Characterization of a myo-inositol-1-phosphate Synthase Gene from Yellow Passion Fruit (Passiflora edulis f. flavicarpa) Expressed During Seed Development and Environmental Stress
Ann. Bot.,
February 1, 2007;
99(2):
285 - 292.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
O. Krinke, Z. Novotna, O. Valentova, and J. Martinec
Inositol trisphosphate receptor in higher plants: is it real?
J. Exp. Bot.,
February 1, 2007;
58(3):
361 - 376.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
