First published online April 7, 2006; 10.1104/pp.106.078717
Plant Physiology 141:436-445 (2006)
© 2006 American Society of Plant Biologists
Transcriptomic Footprints Disclose Specificity of Reactive Oxygen Species Signaling in Arabidopsis1,[W]
Ilya Gadjev2,
Sandy Vanderauwera2,
Tsanko S. Gechev,
Christophe Laloi,
Ivan N. Minkov,
Vladimir Shulaev,
Klaus Apel,
Dirk Inzé,
Ron Mittler and
Frank Van Breusegem*
Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, B9052 Gent, Belgium (I.G., S.V., D.I., F.V.B.); Department of Plant Physiology and Plant Molecular Biology, University of Plovdiv, Plovdiv 4000, Bulgaria (I.G., T.S.G., I.N.M.); Department Molecular Biology of Plants, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, NL9751 NN Haren, The Netherlands (T.S.G.); Institute of Plant Sciences, Plant Genetics, Swiss Federal Institute of Technology, CH8092 Zurich, Switzerland (C.L., K.A.); Department of Biochemistry, University of Nevada, Reno, Nevada 89557 (R.M.); and Virginia Bioinformatics Institute, Blacksburg, Virginia 24061 (V.S.)
Reactive oxygen species (ROS) are key players in the regulation of plant development, stress responses, and programmed cell death. Previous studies indicated that depending on the type of ROS (hydrogen peroxide, superoxide, or singlet oxygen) or its subcellular production site (plastidic, cytosolic, peroxisomal, or apoplastic), a different physiological, biochemical, and molecular response is provoked. We used transcriptome data generated from ROS-related microarray experiments to assess the specificity of ROS-driven transcript expression. Data sets obtained by exogenous application of oxidative stress-causing agents (methyl viologen, Alternaria alternata toxin, 3-aminotriazole, and ozone) and from a mutant (fluorescent) and transgenic plants, in which the activity of an individual antioxidant enzyme was perturbed (catalase, cytosolic ascorbate peroxidase, and copper/zinc superoxide dismutase), were compared. In total, the abundance of nearly 26,000 transcripts of Arabidopsis (Arabidopsis thaliana) was monitored in response to different ROS. Overall, 8,056, 5,312, and 3,925 transcripts showed at least a 3-, 4-, or 5-fold change in expression, respectively. In addition to marker transcripts that were specifically regulated by hydrogen peroxide, superoxide, or singlet oxygen, several transcripts were identified as general oxidative stress response markers because their steady-state levels were at least 5-fold elevated in most experiments. We also assessed the expression characteristics of all annotated transcription factors and inferred new candidate regulatory transcripts that could be responsible for orchestrating the specific transcriptomic signatures triggered by different ROS. Our analysis provides a framework that will assist future efforts to address the impact of ROS signals within environmental stress conditions and elucidate the molecular mechanisms of the oxidative stress response in plants.
1 This work was supported by the Research Fund of the Ghent University (Geconcerteerde Onderzoeksacties no. 12051403), by the Institute for the Promotion of Innovation by Science and Technology in Flanders (grant no. 040134), by the Scientific Co-operation between Eastern Europe and Switzerland program and the International Atomic Energy Agency (predoctoral fellowship to I.G.), the North Atlantic Treaty Organization (postdoctoral fellowship [RIG 981271] to T.S.G.).
2 These authors contributed equally to the paper.
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: Frank Van Breusegem (frank.vanbreusegem{at}psb.ugent.be).
[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.106.078717.
* Corresponding author; e-mail frank.vanbreusegem{at}psb.ugent.be; fax 3293313809.
Received February 4, 2006;
returned for revision March 28, 2006;
accepted March 28, 2006.
This article has been cited by other articles:

|
 |

|
 |
 
O. Van Aken, B. Zhang, C. Carrie, V. Uggalla, E. Paynter, E. Giraud, and J. Whelan
Defining the Mitochondrial Stress Response in Arabidopsis thaliana
Mol Plant,
November 1, 2009;
2(6):
1310 - 1324.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Pitzschke, A. Djamei, M. Teige, and H. Hirt
VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression
PNAS,
October 27, 2009;
106(43):
18414 - 18419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Khandal, I. Samol, F. Buhr, S. Pollmann, H. Schmidt, S. Clemens, S. Reinbothe, and C. Reinbothe
Singlet oxygen-dependent translational control in the tigrina-d.12 mutant of barley
PNAS,
August 4, 2009;
106(31):
13112 - 13117.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Encinas-Villarejo, A. M. Maldonado, F. Amil-Ruiz, B. de los Santos, F. Romero, F. Pliego-Alfaro, J. Munoz-Blanco, and J. L. Caballero
Evidence for a positive regulatory role of strawberry (Fragariaxananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance
J. Exp. Bot.,
July 1, 2009;
60(11):
3043 - 3065.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Lehmann, M. Schwarzlander, T. Obata, S. Sirikantaramas, M. Burow, C. E. Olsen, T. Tohge, M. D. Fricker, B. L. Moller, A. R. Fernie, et al.
The Metabolic Response of Arabidopsis Roots to Oxidative Stress is Distinct from that of Heterotrophic Cells in Culture and Highlights a Complex Relationship between the Levels of Transcripts, Metabolites, and Flux
Mol Plant,
May 1, 2009;
2(3):
390 - 406.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Depuydt, S. Trenkamp, A. R. Fernie, S. Elftieh, J.-P. Renou, M. Vuylsteke, M. Holsters, and D. Vereecke
An Integrated Genomics Approach to Define Niche Establishment by Rhodococcus fascians
Plant Physiology,
March 1, 2009;
149(3):
1366 - 1386.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Lepisto, S. Kangasjarvi, E.-M. Luomala, G. Brader, N. Sipari, M. Keranen, M. Keinanen, and E. Rintamaki
Chloroplast NADPH-Thioredoxin Reductase Interacts with Photoperiodic Development in Arabidopsis
Plant Physiology,
March 1, 2009;
149(3):
1261 - 1276.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Pitzschke, A. Djamei, F. Bitton, and H. Hirt
A Major Role of the MEKK1-MKK1/2-MPK4 Pathway in ROS Signalling
Mol Plant,
January 6, 2009;
(2009)
ssn079v1.
[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]
|
 |
|

|
 |

|
 |
 
A. Khandelwal, T. Elvitigala, B. Ghosh, and R. S. Quatrano
Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor
Plant Physiology,
December 1, 2008;
148(4):
2050 - 2058.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Wu, Z. Zhang, H. Zhang, X.-C. Wang, and R. Huang
Transcriptional Modulation of Ethylene Response Factor Protein JERF3 in the Oxidative Stress Response Enhances Tolerance of Tobacco Seedlings to Salt, Drought, and Freezing
Plant Physiology,
December 1, 2008;
148(4):
1953 - 1963.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Grennan
A Transcriptomic Footprint of Reactive Oxygen Species
Plant Physiology,
November 1, 2008;
148(3):
1187 - 1188.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. H.M. Schippers, A. Nunes-Nesi, R. Apetrei, J. Hille, A. R. Fernie, and P. P. Dijkwel
The Arabidopsis onset of leaf death5 Mutation of Quinolinate Synthase Affects Nicotinamide Adenine Dinucleotide Biosynthesis and Causes Early Ageing
PLANT CELL,
October 1, 2008;
20(10):
2909 - 2925.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Triantaphylides, M. Krischke, F. A. Hoeberichts, B. Ksas, G. Gresser, M. Havaux, F. Van Breusegem, and M. J. Mueller
Singlet Oxygen Is the Major Reactive Oxygen Species Involved in Photooxidative Damage to Plants
Plant Physiology,
October 1, 2008;
148(2):
960 - 968.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Fahnenstich, T. E. Scarpeci, E. M. Valle, U.-I. Flugge, and V. G. Maurino
Generation of Hydrogen Peroxide in Chloroplasts of Arabidopsis Overexpressing Glycolate Oxidase as an Inducible System to Study Oxidative Stress
Plant Physiology,
October 1, 2008;
148(2):
719 - 729.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. H.M. Ho, E. Giraud, V. Uggalla, R. Lister, R. Clifton, A. Glen, D. Thirkettle-Watts, O. Van Aken, and J. Whelan
Identification of Regulatory Pathways Controlling Gene Expression of Stress-Responsive Mitochondrial Proteins in Arabidopsis
Plant Physiology,
August 1, 2008;
147(4):
1858 - 1873.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Alos, M. Roca, D. J. Iglesias, M. I. Minguez-Mosquera, C. M. B. Damasceno, T. W. Thannhauser, J. K. C. Rose, M. Talon, and M. Cercos
An Evaluation of the Basis and Consequences of a Stay-Green Mutation in the navel negra Citrus Mutant Using Transcriptomic and Proteomic Profiling and Metabolite Analysis
Plant Physiology,
July 1, 2008;
147(3):
1300 - 1315.
[Abstract]
[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. C. Lopez-Martin, M. Becana, L. C. Romero, and C. Gotor
Knocking Out Cytosolic Cysteine Synthesis Compromises the Antioxidant Capacity of the Cytosol to Maintain Discrete Concentrations of Hydrogen Peroxide in Arabidopsis
Plant Physiology,
June 1, 2008;
147(2):
562 - 572.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. J. Norton, D. E. Lou-Hing, A. A. Meharg, and A. H. Price
Rice-arsenate interactions in hydroponics: whole genome transcriptional analysis
J. Exp. Bot.,
May 2, 2008;
(2008)
ern097v1.
[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]
|
 |
|

|
 |

|
 |
 
S. Lee, Y.-M. Woo, S.-I. Ryu, Y.-D. Shin, W. T. Kim, K. Y. Park, I.-J. Lee, and G. An
Further Characterization of a Rice AGL12 Group MADS-Box Gene, OsMADS26
Plant Physiology,
May 1, 2008;
147(1):
156 - 168.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. A. Paponov, M. Paponov, W. Teale, M. Menges, S. Chakrabortee, J. A.H. Murray, and K. Palme
Comprehensive Transcriptome Analysis of Auxin Responses in Arabidopsis
Mol Plant,
March 1, 2008;
1(2):
321 - 337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
U. Bechtold, O. Richard, A. Zamboni, C. Gapper, M. Geisler, B. Pogson, S. Karpinski, and P. M. Mullineaux
Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis
J. Exp. Bot.,
February 1, 2008;
59(2):
121 - 133.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Queval, J. Hager, B. Gakiere, and G. Noctor
Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts
J. Exp. Bot.,
February 1, 2008;
59(2):
135 - 146.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Xing, W. Jia, and J. Zhang
AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis
J. Exp. Bot.,
August 28, 2007;
(2007)
erm144v1.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. K. Ledford, B. L. Chin, and K. K. Niyogi
Acclimation to Singlet Oxygen Stress in Chlamydomonas reinhardtii
Eukaryot. Cell,
June 1, 2007;
6(6):
919 - 930.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Heiber, E. Stroher, B. Raatz, I. Busse, U. Kahmann, M. W. Bevan, K.-J. Dietz, and M. Baier
The redox imbalanced Mutants of Arabidopsis Differentiate Signaling Pathways for Redox Regulation of Chloroplast Antioxidant Enzymes
Plant Physiology,
April 1, 2007;
143(4):
1774 - 1788.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Baxter, H. Redestig, N. Schauer, D. Repsilber, K. R. Patil, J. Nielsen, J. Selbig, J. Liu, A. R. Fernie, and L. J. Sweetlove
The Metabolic Response of Heterotrophic Arabidopsis Cells to Oxidative Stress
Plant Physiology,
January 1, 2007;
143(1):
312 - 325.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Van Breusegem and J. F. Dat
Reactive Oxygen Species in Plant Cell Death
Plant Physiology,
June 1, 2006;
141(2):
384 - 390.
[Full Text]
[PDF]
|
 |
|
|
|