Reactive oxygen species and hormonal control of cell death

https://doi.org/10.1016/S1360-1385(03)00135-3Get rights and content

Abstract

The accumulation of reactive oxygen species (ROS) is involved in regulating cell death. Pathogen- and ozone-induced processes have become important models for the study of cell death regulation by ROS. Hydrogen peroxide and superoxide have emerged as the two key ROS and recent studies have addressed their sources and control of their production. ROS signals interact directly or indirectly with several other signaling pathways, such as nitric oxide, and the stress hormones salicylic acid, jasmonic acid and ethylene. The interaction and balance of these pathways determines whether the cell lives or dies.

Section snippets

Ozone as a model of cell death regulation

In contrast to stratospheric O3, which protects plants from harmful ultraviolet radiation, tropospheric O3 is a potent toxin [9]. In sensitive plants, O3 causes the formation of lesions that have many characteristics in common with the HR. These include induction of an oxidative burst, deposition of autofluorescent phenolic compounds, pathogenesis-related (PR) protein expression and both micro- and macro-scale cell death and the associated local and systemic-induced pathogen resistance 6, 7, 10

Oxidative burst

The oxidative burst is a common response to virtually every biotic and abiotic stress [16] including the HR and the O3 response. For example, in the O3-sensitive Bel-W3 tobacco and the O3-sensitive Arabidopsis accession Cvi-0, and in the rcd1 and jar1 mutants, a biphasic O3-induced oxidative burst and prolonged ROS accumulation result in the activation of cell death 13, 17, 18. When tobacco, seven tomato cultivars, 12 Arabidopsis accessions, two Rumex and one Malva species were assayed for ROS

Hormonal regulation of ROS-dependent cell death

A picture of the integral role of plant hormones in the regulation of ROS-dependent cell death is now emerging. To facilitate their initial characterization, hormone signal transduction pathways have necessarily been conceptualized as linear and independent. However, as more details of these signaling pathways have become available, so their interconnected nature has become increasingly evident. The three hormones ethylene, salicylic acid and jasmonic acid are of particular importance in

Oxidative cell death cycle

The extent of HR and O3-lesion propagation seems to be under hormonal control, with different hormones and their interactions regulating ROS production and the competence of the cell to perceive and react to ROS signals (Box 1). Regulation of the ROS-dependent cell death in the oxidative cell death cycle has been proposed based on work with plants undergoing HR [46] and later modified based on O3-induced oxidative cell death [13]. In this model (Fig. 1), which is further supported by the

Conclusions and future challenges

Powerful genetic strategies driven by the use of Arabidopsis have resulted in the elucidation of many hormone and other signaling pathways in plants. As illustrated by the studies reviewed here, the application of this knowledge and, in particular, the use of signaling mutants have allowed the delineation of signals involved in cell death regulation. Similarly, genetic approaches involving mutants have been key in identifying novel plant pathways, such as the MAP kinase cascades (Box 2)

Acknowledgements

We acknowledge the financial support from the Academy of Finland (Finnish Center of Excellence program 2000–05) and EU (FAIR/Tomstress; QLK5-Establish). K.O. is a recipient of a post doctoral fellowship from the Academy of Finland.

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      Most of the ROS are formed in the reaction center (PS Ⅰ and PS Ⅱ) on the thylakoid, thus causing direct damage to the thylakoid structure (Asada, 2006; Knauert and Knauer, 2008). Excess ROS exceeds the scavenging capacity of the antioxidant system, causing damage to photosynthesis-related organelles (Overmyer et al., 2003) and disrupt the membrane structure of the thylakoid membrane (Deng et al., 2019), which is one of the main reasons for halting photosynthesis. It has also been found that ROS itself has an inhibitory effect on photosynthesis (Apel and Hirt, 2004).

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