Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species

Abstract

Previously, we showed that inoculation of tobacco with Pseudomonas syringae incompatible pv. maculicola results in a rapid and persistent burst of superoxide (O2 -) from mitochondria, no change in amount of mitochondrial alternative oxidase (AOX) and induction of the hypersensitive response (HR). However, inoculation with incompatible pv. phaseolicola resulted in increased AOX, no O2 -burst and no HR. Here, we show that in transgenic plants unable to induce AOX in response to pv. phaseolicola, there is now a strong mitochondrial O2 -burst, similar to that normally seen only with pv. maculicola. This interaction did not however result in a HR. This indicates that AOX amount is a key determinant of the mitochondrial O2 -burst but also that the burst itself is not sufficient to induce the HR. Surprisingly, the O2 -burst normally seen towards pv. maculicola is delayed in plants lacking AOX. This delay is associated with a delayed HR, suggesting that the burst does promote the HR. A O2 -burst can also be induced by the complex III inhibitor antimycin A (AA), but is again delayed in plants lacking AOX. The similar mitochondrial response induced by pv. maculicola and AA suggests that electron transport is a target during HR-inducing biotic interactions.

Mitochondrial Energy Signaling and Its Role in the Low-Oxygen Stress Response of Plants

“…Like AA, these inhibitors stop electron flow down the respiratory chain, albeit at different steps with different physiological outcomes. The concerted action of transcriptionally elevated alternative electron transport components has been interpreted as an inducible safety valve to counterbalance ROS production independent of adenosine phosphorylation status (Vanlerberghe and McIntosh, 1992;Maxwell et al, 1999;Cvetkovska and Vanlerberghe, 2013). In the third section of this article, we will discuss how AA treatment compares with more physiological stimuli that induce the plant MRR.…”

“…Hence, natural conditions that lead to an increase in mtROS production may also activate the identified signaling responses. Indeed, several biotic and abiotic stresses have been associated with mtROS production (Rhoads et al, 2006;Yao and Greenberg, 2006;Chang et al, 2012;Cvetkovska and Vanlerberghe, 2013) as well as with the induction of AOX1a and other retrograde marker transcripts (Van Aken and Whelan, 2012). Yet, the link between mtROS and induction of signaling remains correlative, which is partly due to the difficulty to trigger increased mtROS production without causing gross perturbation of respiratory physiology.…”

Early events induced by the toxin deoxynivalenol lead to programmed cell death in Nicotiana tabacum cells

“…It is assumed that plants can induce mitochondrial AOX activity to prevent ROS overgeneration by lowering the ubiquinone reduction level [60,61], thus reducing redox stress and ROS accumulation [62]. An early superoxide burst in the mitochondrial matrix preceding the HR has been reported to be due to a coordinated response of AOX [63,64]. Consistently, downregulation of AOX level, either via inhibitors or via transgenic approaches, has been reported to cause an increase in ROS production [65] and stimulate PCD [66], while overexpression of Aox1 has been shown to decrease PCD [42].…”

Reactive oxygen species and stress signaling in plants

“…Основными сайтами утечки электронов у растений, как и у живот-ных, считаются комплексы I и III [15]. В изоли-рованных митохондриях генерация АФК (H 2 O 2 или О 2…”

“…•- [15]. У растений взаимосвязь между транспор-том электронов, окислительным фосфорилиро-ванием и генерацией АФК более сложная, чем у животных в связи с наличием альтернативной оксидазы, катализирующей окисление убихино-на и восстановление молекулярного кислорода до воды.…”