Plant Physiology Preview Published on June 7, 2007; 10.1104/pp.107.101436
OPEN ACCESS ARTICLE
Received April 23, 2007
Accepted May 21, 2007
Double Mutants Deficient in Cytosolic and Thylakoid Ascorbate Peroxidase Reveal a Complex Mode of Interaction between Reactive Oxygen Species, Plant Development and Response to Abiotic Stresses
Gad Miller , Nobuhiro Suzuki , Ludmila Rizhsky , Alicia Hegie , Shai Koussevitzky , and Ron Mittler. *
Department of Biochemistry and Molecular Biology, University of Nevada, Mail Stop 200, Reno NV 89557; Department of Genetics, Development and Cell Biology, Iowa State University, Room 353 Bessey Hall, Ames, Iowa 50011; Department of Plant Sciences, Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel
* Corresponding author; email: ronm{at}unr.edu.
Reactive oxygen species (ROS) play a key signaling role in plants, and are controlled in cells by a complex network of ROS metabolizing enzymes found in several different cellular compartments. To study how different ROS signals, generated in different cellular compartments, are integrated in cells, we generated a double mutant lacking thylakoid ascorbate peroxidase (tylapx) and cytosolic ascorbate peroxidase 1 (apx1). Our analysis suggests that two different signals are generated in plants lacking cytosolic APX1 or tylAPX. The lack of a chloroplastic H2O2-removal enzyme triggers a specific signal in cells that results in enhanced tolerance to heat stress, whereas the lack of a cytosolic H2O2-removal enzyme triggers a different signal that results in stunted growth and enhanced sensitivity to oxidative stress. When the two signals are co-activated in cells (i.e., tylapx/apx1), a new response is detected suggesting that the integration of the two different signals results in a new signal that manifests in late flowering, low protein oxidation during light stress, and enhanced accumulation of anthocyanins. Our results demonstrate a high degree of plasticity in ROS signaling in Arabidopsis and suggest the existence of redundant pathways for ROS protection that compensate for the lack of classical ROS-removal enzymes such as cytosolic and chloroplastic APXs. Further investigation of the enhanced heat tolerance in plants lacking tylAPX, using mutant deficient in chloroplast-to-nuclei retrograde signaling, suggest the existence of a chloroplast-generated stress signal that enhances basal thermotolerance in plants.
This article has been cited by other articles:

|
 |

|
 |
 
M. Hernandez, N. Fernandez-Garcia, P. Diaz-Vivancos, and E. Olmos
A different role for hydrogen peroxide and the antioxidative system under short and long salt stress in Brassica oleracea roots
J. Exp. Bot.,
November 11, 2009;
(2009)
erp321v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. J. Im, M. Ji, A. Lee, R. Killens, A. M. Grunden, and W. F. Boss
Expression of Pyrococcus furiosus Superoxide Reductase in Arabidopsis Enhances Heat Tolerance
Plant Physiology,
October 1, 2009;
151(2):
893 - 904.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tunc-Ozdemir, G. Miller, L. Song, J. Kim, A. Sodek, S. Koussevitzky, A. N. Misra, R. Mittler, and D. Shintani
Thiamin Confers Enhanced Tolerance to Oxidative Stress in Arabidopsis
Plant Physiology,
September 1, 2009;
151(1):
421 - 432.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-J. Song and M. Matsuoka
Bar the windows: an optimized strategy to survive drought and salt adversities
Genes & Dev.,
August 1, 2009;
23(15):
1709 - 1713.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-Y. Huang, D.-Y. Chao, J.-P. Gao, M.-Z. Zhu, M. Shi, and H.-X. Lin
A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control
Genes & Dev.,
August 1, 2009;
23(15):
1805 - 1817.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. O. Kotchoni, K. E. Larrimore, M. Mukherjee, C. F. Kempinski, and C. Barth
Alterations in the Endogenous Ascorbic Acid Content Affect Flowering Time in Arabidopsis
Plant Physiology,
February 1, 2009;
149(2):
803 - 815.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Xue, X. Li, W. Zhu, C. Wu, G. Yang, and C. Zheng
Cotton metallothionein GhMT3a, a reactive oxygen species scavenger, increased tolerance against abiotic stress in transgenic tobacco and yeast
J. Exp. Bot.,
January 1, 2009;
60(1):
339 - 349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Myouga, C. Hosoda, T. Umezawa, H. Iizumi, T. Kuromori, R. Motohashi, Y. Shono, N. Nagata, M. Ikeuchi, and K. Shinozaki
A Heterocomplex of Iron Superoxide Dismutases Defends Chloroplast Nucleoids against Oxidative Stress and Is Essential for Chloroplast Development in Arabidopsis
PLANT CELL,
November 1, 2008;
20(11):
3148 - 3162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Luhua, S. Ciftci-Yilmaz, J. Harper, J. Cushman, and R. Mittler
Enhanced Tolerance to Oxidative Stress in Transgenic Arabidopsis Plants Expressing Proteins of Unknown Function
Plant Physiology,
September 1, 2008;
148(1):
280 - 292.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Van Breusegem, J. Bailey-Serres, and R. Mittler
Unraveling the Tapestry of Networks Involving Reactive Oxygen Species in Plants
Plant Physiology,
July 1, 2008;
147(3):
978 - 984.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Giraud, L. H.M. Ho, R. Clifton, A. Carroll, G. Estavillo, Y.-F. Tan, K. A. Howell, A. Ivanova, B. J. Pogson, A. H. Millar, et al.
The Absence of ALTERNATIVE OXIDASE1a in Arabidopsis Results in Acute Sensitivity to Combined Light and Drought Stress
Plant Physiology,
June 1, 2008;
147(2):
595 - 610.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Morgan, M. Lehmann, M. Schwarzlander, C. J. Baxter, A. Sienkiewicz-Porzucek, T. C.R. Williams, N. Schauer, A. R. Fernie, M. D. Fricker, R. G. Ratcliffe, et al.
Decrease in Manganese Superoxide Dismutase Leads to Reduced Root Growth and Affects Tricarboxylic Acid Cycle Flux and Mitochondrial Redox Homeostasis
Plant Physiology,
May 1, 2008;
147(1):
101 - 114.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|