Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling

Abstract

ROS are known to be important signaling molecules in plants (Van Breusegem et al., 2001; Neill et al, 2002; Laloi et al., 2004). ROS levels, antioxidant levels, and redox status are balanced by plant cells, including within mitochondria. Each is important for plant health. Perturbations of this balance are likely detected and the plant responds accordingly. Responses to changes in ROS levels include alteration of expression of nuclear genes encoding enzymes that function to regain homeostasis by producing antioxidant compounds and protective and repair enzymes. Currently, little is known about how increased mtROS production is conveyed to the nucleus. Because ROS are involved in many distinct aspects of plant responses to stresses, there must be distinct detection mechanisms that differentiate identity, levels, and perhaps even sources of ROS. Mitochondrial ROS must fit into this scheme. Evaluation of the current literature leads us to conclude that the outcome of various mitochondrial perturbations may not be easily predicted due to the variety of potential mitochondrial responses, including mtROS production, as well as other signals and changes that may be arising elsewhere in the cell simultaneously. These responses may occur sequentially under some stresses and lead to a predictable outcome. For example, a stress may disrupt the mtETC causing mtROS production of a sufficient level to initiate permeability transition pore opening, cytochrome c release, and PCD. On the other hand, slightly different treatments or the same treatments in different plant species may cause mitochondria to respond with parallel events, such as simultaneously signaling for changes in nuclear gene expression to regain homeostasis and initiation of PCD, with the actual outcome decided by yet other inputs. Identification of components of the various signaling pathways will likely help clarify this complex picture. In the most extreme case of high mtROS production, when cells sense a severe threat, mitochondria likely initiate PCD. Although plants employ this important option to "cut their losses" in situations such as pathogen attack, such an extreme outcome should be under tight control. Increased mtROS can cause critical shifts in cell redox status because antioxidant systems ultimately require electrons from redox pairs such as NADP/NADPH, which connect many aspects of metabolism. Major challenges will be to determine the roles of mtROS and the potential consequences of altered mtROS levels, such as production of other reactive molecules and shifts in redox balance, in plant developmental processes and stress responses. © 2006 American Society of Plant Biologists.