Trends in Plant Science
Volume 9, Issue 10, October 2004, Pages 490-498
Journal home page for Trends in Plant Science

Abiotic stress series
Reactive oxygen gene network of plants

https://doi.org/10.1016/j.tplants.2004.08.009Get rights and content

Reactive oxygen species (ROS) control many different processes in plants. However, being toxic molecules, they are also capable of injuring cells. How this conflict is resolved in plants is largely unknown. Nonetheless, it is clear that the steady-state level of ROS in cells needs to be tightly regulated. In Arabidopsis, a network of at least 152 genes is involved in managing the level of ROS. This network is highly dynamic and redundant, and encodes ROS-scavenging and ROS-producing proteins. Although recent studies have unraveled some of the key players in the network, many questions related to its mode of regulation, its protective roles and its modulation of signaling networks that control growth, development and stress response remain unanswered.

Section snippets

Modulation of ROS signaling by the reactive oxygen gene network of plants

Whereas Ca2+ signaling is predominantly controlled in plants by storage and release, ROS signaling is controlled by production and scavenging (Figure 1). Different developmental or environmental signals feed into the ROS signaling network and perturb ROS homeostasis in a compartment-specific or even cell-specific manner. Perturbed ROS levels are perceived by different proteins, enzymes or receptors and modulate different developmental, metabolic and defense pathways. ROS can be generated by

Production of ROS in plants

Organelles with a highly oxidizing metabolic activity or with an intense rate of electron flow, such as chloroplasts, mitochondria and microbodies, are a major source of ROS production in plant cells. Together with an extensive battery of oxidases, the plant cell is well armed for bountiful yet flexible ROS production. In chloroplasts, the primary sources of ROS production are the Mehler reaction and the antenna pigments [2]. Production of ROS by these sources is enhanced in plants by

Enzymatic components of the ROS-scavenging pathways of plants

Major ROS-scavenging enzymes of plants include superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX) and peroxiredoxin (PrxR) (Table 1). Together with the antioxidants ascorbic acid and glutathione [35], these enzymes provide cells with highly efficient machinery for detoxifying O2 and H2O2. The balance between SODs and the different H2O2-scavenging enzymes in cells is considered to be crucial in determining the steady-state level of O2 and H2O2.

Cellular localization and coordination of the ROS-scavenging pathways of plants

The various scavenging enzymes encoded by the ROS network can be found in almost every subcellular compartment (Figure 2). In addition, usually more than one enzymatic scavenging activity per a particular ROS can be found in each of the different compartments (e.g. GPXs, PrxRs and APXs in the cytosol and chloroplast, and APXs and CATs in peroxisomes; Figure 2). When the relative function of the different enzymes in the different cellular compartments is considered, it is important to remember

Gene annotation and expression of the ROS network in Arabidopsis

Table 1 and the table in the supplementary material (available in the on-line version) summarize all known ROS-scavenging genes and NADPH oxidases in Arabidopsis. Expression data for the different genes in three different knockout or antisense lines (Apx1, CSD2 and Cat2) and in plants subjected to different abiotic stresses (e.g. drought, salt, cold or high light) are also included. Although data were assembled from different experiments and should only be considered from a qualitative point of

Key components of the reactive oxygen gene network identified by reverse genetics

Recent studies of knockout and antisense lines for Cat2, Apx1, chlAOX, mitAOX, CSD2, 2-cysteine PrxR and various NADPH oxidases have revealed a strong link between ROS and processes such as growth, development, stomatal responses and biotic and abiotic stress responses 7, 8, 50, 52, 57, 59, 60, 61, 62. These findings demonstrate the complex nature of the ROS gene network in plants and its modulation of key biological processes. Although mutants for all the proteins listed above are viable,

ROS signal transduction pathway of plants

Recent studies in Arabidopsis have uncovered some of the key components involved in the ROS signal transduction pathway of plants. Although the receptors for ROS are unknown at present, it has been suggested that plant cells sense ROS via at least three different mechanisms (Figure 3): (i) unidentified receptor proteins; (ii) redox-sensitive transcription factors, such as NPR1 or HSFs; and (iii) direct inhibition of phosphatases by ROS 6, 13, 20, 64.

Downstream signaling events associated with

Acknowledgements

We thank Ivan Baxter and Jeffery Harper for sharing unpublished work. This work was supported by funding from The National Science Foundation (NSF-0431327) and a grant from the Research Fund of the Ghent University (Geconcerteerde Onderzoeksacties no. 12051403).

References (80)

  • D.R. Walters

    Polyamines and plant disease

    Phytochemistry

    (2003)
  • M. Tognolli

    Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana

    Gene

    (2002)
  • C. Pignocchi et al.

    Apoplastic ascorbate metabolism and its role in the regulation of cell signalling

    Curr. Opin. Plant Biol.

    (2003)
  • F.J. Corpas

    Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells

    Trends Plant Sci.

    (2001)
  • L. Rizhsky

    The water–water cycle is essential for chloroplast protection in the absence of stress

    J. Biol. Chem.

    (2003)
  • L. Rizhsky

    The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis

    J. Biol. Chem.

    (2004)
  • H. Knight et al.

    Abiotic stress signalling pathways: specificity and cross-talk

    Trends Plant Sci.

    (2001)
  • C. Bowler et al.

    The role of calcium and activated oxygens as signals for controlling cross-tolerance

    Trends Plant Sci.

    (2000)
  • B. Halliwell et al.

    Free Radicals in Biology and Medicine

    (1989)
  • Asada, K. and Takahashi, M. (1987) Production and scavenging of active oxygen in photosynthesis. In Photoinhibition...
  • Y. Kovtun

    Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants

    Proc. Natl. Acad. Sci. U. S. A.

    (2000)
  • Z-M. Pei

    Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells

    Nature

    (2000)
  • M.A. Torres

    Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response

    Proc. Natl. Acad. Sci. U. S. A.

    (2002)
  • J. Foreman

    Reactive oxygen species produced by NADPH oxidase regulate plant cell growth

    Nature

    (2003)
  • J.M. Kwak

    NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis

    EMBO J.

    (2003)
  • K. Jiang

    Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment

    Development

    (2003)
  • J. Dat

    Dual action of the active oxygen species during plant stress responses

    Cell. Mol. Life Sci.

    (2000)
  • C.H. Foyer

    The contribution of photosynthetic oxygen metabolism to oxidative stress in plants

  • I.M. Møller

    Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (2001)
  • C. Lamb et al.

    The oxidative burst in plant disease resistance

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1997)
  • K. Apel et al.

    Reactive oxygen species: metabolism, oxidative stress, and signal transduction

    Annu. Rev. Plant Biol.

    (2004)
  • R. Tenhaken

    Function of the oxidative burst in hypersensitive disease resistance

    Proc. Natl. Acad. Sci. U. S. A.

    (1995)
  • A.C. Allan et al.

    Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells

    Plant Cell

    (1997)
  • R. Pellinen

    Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells

    Plant J.

    (1999)
  • H-J. Park

    Physiological mechanisms of a sub-systemic oxidative burst triggered by elicitor-induced local oxidative burst in potato tuber slices

    Plant Cell Physiol.

    (1998)
  • J.F. Dat

    Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco

    Plant J.

    (2003)
  • T. Lara-Ortíz

    Reactive oxygen species generated by microbial NADPH oxidase NoxA regulated sexual development in Aspergillus nidulans

    Mol. Microbiol.

    (2003)
  • T. Keller

    A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs

    Plant Cell

    (1998)
  • M.A. Torres

    Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox)

    Plant J.

    (1998)
  • Q.J. Groom

    rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene

    Plant J.

    (1996)
  • Cited by (4533)

    View all citing articles on Scopus
    View full text