First published online January 28, 2005; 10.1104/pp.104.054494
Plant Physiology 137:663-670 (2005)
© 2005 American Society of Plant Biologists
DEVELOPMENT AND HORMONE ACTION
Nitric Oxide Mediates Gravitropic Bending in Soybean Roots1,[w]
Xiangyang Hu2,
Steven J. Neill,
Zhangcheng Tang and
Weiming Cai*
Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Graduate School of the Chinese Academy of Sciences, Shanghai 200032, China (X.H., Z.T., W.C.); and Centre for Research in Plant Science, University of the West of England, Bristol BS16 1QY, United Kingdom (S.J.N.)
Plant roots are gravitropic, detecting and responding to changes in orientation via differential growth that results in bending and reestablishment of downward growth. Recent data support the basics of the Cholodny-Went hypothesis, indicating that differential growth is due to redistribution of auxin to the lower sides of gravistimulated roots, but little is known regarding the molecular details of such effects. Here, we investigate auxin and gravity signal transduction by demonstrating that the endogenous signaling molecules nitric oxide (NO) and cGMP mediate responses to gravistimulation in primary roots of soybean (Glycine max). Horizontal orientation of soybean roots caused the accumulation of both NO and cGMP in the primary root tip. Fluorescence confocal microcopy revealed that the accumulation of NO was asymmetric, with NO concentrating in the lower side of the root. Removal of NO with an NO scavenger or inhibition of NO synthesis via NO synthase inhibitors or an inhibitor of nitrate reductase reduced both NO accumulation and gravitropic bending, indicating that NO synthesis was required for the gravitropic responses and that both NO synthase and nitrate reductase may contribute to the synthesis of the NO required. Auxin induced NO accumulation in root protoplasts and asymmetric NO accumulation in root tips. Gravistimulation, NO, and auxin also induced the accumulation of cGMP, a response inhibited by removal of NO or by inhibitors of guanylyl cyclase, compounds that also reduced gravitropic bending. Asymmetric NO accumulation and gravitropic bending were both inhibited by an auxin transport inhibitor, and the inhibition of bending was overcome by treatment with NO or 8-bromo-cGMP, a cell-permeable analog of cGMP. These data indicate that auxin-induced NO and cGMP mediate gravitropic curvature in soybean roots.
1 This work was supported by the Chinese Academy of Sciences (grant no. KSCX2SW322), the Shanghai Institute of Plant Physiology and Ecology, and the National Natural Sciences Foundation of China (grant no. 39770199). Collaboration between the United Kingdom and China was supported by The Royal Society and The Biotechnology and Biological Sciences Research Council.
2 Present address: Department of Botany and Plant Sciences, University of California, Riverside, CA 92521.
[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.104.054494.
* Corresponding author; e-mail wmcai{at}iris.sipp.ac.cn; fax 862154924015.
Received October 8, 2004;
returned for revision December 16, 2004;
accepted December 20, 2004.
Related articles in Plant Physiol.:
- On the Inside
- Peter V. Minorsky
Plant Physiol. 2005 137: 586-587.
[Full Text]
This article has been cited by other articles:

|
 |

|
 |
 
S. A. Reichler, J. Torres, A. L. Rivera, V. A. Cintolesi, G. Clark, and S. J. Roux
Intersection of two signalling pathways: extracellular nucleotides regulate pollen germination and pollen tube growth via nitric oxide
J. Exp. Bot.,
May 1, 2009;
60(7):
2129 - 2138.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kasprowicz, A. Szuba, D. Volkmann, F. Baluska, and P. Wojtaszek
Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices
J. Exp. Bot.,
April 1, 2009;
60(6):
1605 - 1617.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S.-J. Wu and J.-Y. Wu
Extracellular ATP-induced NO production and its dependence on membrane Ca2+ flux in Salvia miltiorrhiza hairy roots
J. Exp. Bot.,
October 1, 2008;
59(14):
4007 - 4016.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Xuan, F.-Y. Zhu, S. Xu, B.-K. Huang, T.-F. Ling, J.-Y. Qi, M.-B. Ye, and W.-B. Shen
The Heme Oxygenase/Carbon Monoxide System Is Involved in the Auxin-Induced Cucumber Adventitious Rooting Process
Plant Physiology,
October 1, 2008;
148(2):
881 - 893.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Besson-Bard, S. Griveau, F. Bedioui, and D. Wendehenne
Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses
J. Exp. Bot.,
September 1, 2008;
59(12):
3407 - 3414.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. B. Kirkham
Horizontal Root Growth: Water Uptake and Stomatal Resistance under Microgravity
Vadose Zone J.,
August 13, 2008;
7(3):
1125 - 1131.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Flores, C. D. Todd, A. Tovar-Mendez, P. K. Dhanoa, N. Correa-Aragunde, M. E. Hoyos, D. M. Brownfield, R. T. Mullen, L. Lamattina, and J. C. Polacco
Arginase-Negative Mutants of Arabidopsis Exhibit Increased Nitric Oxide Signaling in Root Development
Plant Physiology,
August 1, 2008;
147(4):
1936 - 1946.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Prado, R. Colaco, N. Moreno, A. C. Silva, and J. A. Feijo
Targeting of Pollen Tubes to Ovules Is Dependent on Nitric Oxide (NO) Signaling
Mol Plant,
July 1, 2008;
1(4):
703 - 714.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Lanteri, A. M. Laxalt, and L. Lamattina
Nitric Oxide Triggers Phosphatidic Acid Accumulation via Phospholipase D during Auxin-Induced Adventitious Root Formation in Cucumber
Plant Physiology,
May 1, 2008;
147(1):
188 - 198.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Vitecek, V. Reinohl, and R. L. Jones
Measuring NO Production by Plant Tissues and Suspension Cultured Cells
Mol Plant,
March 1, 2008;
1(2):
270 - 284.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Courtois, A. Besson, J. Dahan, S. Bourque, G. Dobrowolska, A. Pugin, and D. Wendehenne
Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases
J. Exp. Bot.,
February 1, 2008;
59(2):
155 - 163.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Neill, J. Bright, R. Desikan, J. Hancock, J. Harrison, and I. Wilson
Nitric oxide evolution and perception
J. Exp. Bot.,
January 1, 2008;
59(1):
25 - 35.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Wu, I. Steinebrunner, Y. Sun, T. Butterfield, J. Torres, D. Arnold, A. Gonzalez, F. Jacob, S. Reichler, and S. J. Roux
Apyrases (Nucleoside Triphosphate-Diphosphohydrolases) Play a Key Role in Growth Control in Arabidopsis
Plant Physiology,
June 1, 2007;
144(2):
961 - 975.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Salmi, K. E. Morris, S. J. Roux, and D. M. Porterfield
Nitric Oxide and cGMP Signaling in Calcium-Dependent Development of Cell Polarity in Ceratopteris richardii
Plant Physiology,
May 1, 2007;
144(1):
94 - 104.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Liu, R. Wu, Q. Wan, G. Xie, and Y. Bi
Glucose-6-Phosphate Dehydrogenase Plays a Pivotal Role in Nitric Oxide-Involved Defense Against Oxidative Stress Under Salt Stress in Red Kidney Bean Roots
Plant Cell Physiol.,
March 1, 2007;
48(3):
511 - 522.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Stohr and S. Stremlau
Formation and possible roles of nitric oxide in plant roots
J. Exp. Bot.,
February 1, 2006;
57(3):
463 - 470.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Perazzolli, M. C. Romero-Puertas, and M. Delledonne
Modulation of nitric oxide bioactivity by plant haemoglobins
J. Exp. Bot.,
February 1, 2006;
57(3):
479 - 488.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Grun, C. Lindermayr, S. Sell, and J. Durner
Nitric oxide and gene regulation in plants
J. Exp. Bot.,
February 1, 2006;
57(3):
507 - 516.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|