Oxidative Stress and Acclimation Mechanisms in Plants

One of the most crucial functions of plant cells is their ability to respond to fluctuations in their environment. Understanding the connections between a plant's initial responses and the downstream events that constitute successful adjustment to its altered environment is one of the next grand challenges of plant biology. Oxidative stress from environmental sources and developmental transitions such as seed maturation involves the formation of reactive oxygen species (ROS) in plant cells. The redox-modulated changes that follow are central events in cellular responses. Thiol redox regulation (Figure 1) partially mediated through the redox state of the glutathione pool (GSH/GSSG), regulation of the glutathione biosynthetic pathway, and ROS themselves are each thought to have important roles as environmental sensors and/or modulators of global patterns of gene expression in development and defense. Exposure of green tissue to potentially damaging light intensities involves redox sensing molecular events throughout the plant, originating at the plastoquinone (PQ) pool in the thylakoid membrane. Major defense genes whose expression is affected by the redox state of the PQ pool include both cytosolic and chloroplast ascorbate peroxidases (APX) ( Karpinska et al. 2000 ). The superoxide dismutase (SOD) gene families appear to be specialized in function with respect to subcellular location and other as yet unknown factors (Alscher et al. 2002). In the case of peroxisomes, the imposition of oxidative stress gives rise to organelle proliferation, thus adding another layer of complexity to stress responses (Lopez-Huertas et al. 2000). Defense mechanisms involving molecular chaperones and methionine sulfoxide reductase are becoming recognized as important players in resistance to oxidative stress throughout the cell. Figure 1. Thiol redox control and stress defense Intracellular origins of ROS and their multiple damaging effects Any circumstance in which cellular redox homeostasis is disrupted can lead to oxidative stress or the generation of ROS (Asada 1994). Production of ROS during environmental stress is one of the main causes for decreases in productivity, injury, and death that accompany these stresses in plants. ROS are produced in both unstressed and stressed cells, and in various locations (Halliwell and Gutteridge 1989) (Figure 2). They are generated endogenously during certain developmental transitions such as seed maturation and as a result of normal, unstressed, photosynthetic and respiratory metabolism. An initial oxyradical product, the superoxide radical (O2-.), upon further reaction within the cell, can form more ROS such as hydroxyl radicals and singlet oxygen. Superoxide is a charged molecule and cannot cross biological membranes. Subcellular compartmentation of defense mechanisms is, therefore, crucial for efficient removal of superoxide anions at their sites of generation throughout the cell. Hydrogen peroxide, on the other hand, which is formed as a result of SOD action, is capable of diffusing across membranes and is thought to fulfil a signaling function in defense responses (Mullineaux et al. 2000). Figure 2. Reactive oxygen species (ROS) arise throughout the cell. ROS play an important role in endonuclease activation and consequent DNA damage (Hagar et al. 1996). In the presence of metal ions such as Fe or Cu(II), hydroxyl radicals are formed very rapidly. Hydroxyl radicals can cause damage to all classes of biologically important macromolecules, especially nucleic acids. Hydroxyl radicals can also modify proteins so as to make them more susceptible to proteolytic attack. There is evidently considerable specificity associated with this degradative process since proteins have widely differing susceptibilities to attack by ROS (Davies 1987). Once damaged, proteins can be broken down further by specific endopeptidases such as the one found bound to the thylakoid membrane (Casano et al. 1994). A multicatalytic proteinase complex has been demonstrated in plant systems, with the capacity to selectively break down oxidatively damaged proteins (Van Nocker et al. 1996)