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The signaling role of a mitochondrial superoxide burst during stress - PubMed

The signaling role of a mitochondrial superoxide burst during stress

Marina Cvetkovska et al. Plant Signal Behav. 2013 Jan.

Abstract

Plant mitochondria are proposed to act as signaling organelles in the orchestration of defense responses to biotic stress and acclimation responses to abiotic stress. However, the primary signal(s) being generated by mitochondria and then interpreted by the cell are largely unknown. Recently, we showed that mitochondria generate a sustained burst of superoxide (O 2(-)) during particular plant-pathogen interactions. This O 2(-) burst appears to be controlled by mitochondrial components that influence rates of O 2(-) generation and scavenging within the organelle. The O 2(-) burst appears to influence downstream processes such as the hypersensitive response, indicating that it could represent an important mitochondrial signal in support of plant stress responses. The findings generate many interesting questions regarding the upstream factors required to generate the O 2(-) burst, the mitochondrial events that occur in support of and in parallel with this burst and the downstream events that respond to this burst.

Keywords: alternative oxidase; biotic stress; manganese superoxide dismutase; mitochondrial electron transport chain; nitric oxide; organelle signaling; salicylic acid; superoxide burst.

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Figures

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Figure 1. The plant mitochondrial ETC includes two terminal oxidases able to catalyze the 4-electron reduction of O2 to H2O, the usual cyt oxidase (complex IV) and AOX. Electron transport from the ubiquinone pool (Q) to complex IV is coupled to the generation of a membrane potential that is subsequently dissipated by ATP synthase (complex V) to produce ATP. However, electron flow from Q to AOX is non-energy conserving. When the ability of an ETC component to transport electrons is reduced and/or membrane potential is high, electron transport can slow, leading to an over-reduction of the ETC. Under these conditions, single electron leak to O2 or nitrite increases, producing O2- and NO, respectively. In plants, the specific sites and mechanisms of O2- and NO generation are not yet well understood. See text for further details. I, II, III, IV, V: complexes I to V.

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Figure 2. The impact of two incompatible pv’s of P. syringae on the mitochondria of tobacco leaf mesophyll cells. (A) Infection with the HR-inducing pv maculicola results in an early and persistent burst of O2- in the mitochondrial matrix that may have a signaling role in support of the HR. (B) Infection with pv phaseolicola, that causes induction of plant defenses but not including the HR, lacks a matrix O2- burst. The differential effect of the two pv’s is supported by a coordinated response of the major ETC mechanism to avoid O2- generation (AOX) and the sole enzymatic means to scavenge matrix O2- (MnSOD). In response to pv phaseolicola, AOX is strongly induced and MnSOD activity remains high, while in response to pv maculicola MnSOD activity declines and AOX remains low. As a result, the two bacterial pv’s each generate distinct mitochondrial ROS signatures that may impact defense responses and cell fate.

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Figure 3. Simple cartoon of a plant cell and mitochondrion. This figure is meant to highlight some key questions regarding the upstream factors required to generate a mitochondrial O2- burst, the mitochondrial events that occur in support of or in parallel with this burst, and the downstream events that may be responsive to this burst. See text for further discussion of these aspects. PM, plasma membrane; OMM, outer mitochondrial membrane; IMS, intermembrane space; IMM, inner mitochondrial membrane.

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