The signaling role of a mitochondrial superoxide burst during stress

Cvetkovska, Marina; Alber, Nicole A.; Vanlerberghe, Greg C.

doi:10.4161/psb.22749

Cited by 27 publications

(14 citation statements)

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“…). These findings may be significant in the context of mitochondria acting as signalling organelles, because both ROS and NO are often implicated as the signals being generated (Bleier & Dröse ; Chang et al ; Cvetkovska et al ; De Clercq et al ; Gleason et al ; Hebelstrup & Møller ; Jardim‐Messeder et al ; Ng et al ; Schwarzländer & Finkemeier ; Umbach et al ; Van Aken & Van Breusegem ; Wu et al ). In this respect, Complex III may be a key signal generator of ROS and/or NO, while AOX appears well positioned to act as a key signal regulator .…”

Section: Resultsmentioning

confidence: 97%

The occurrence and control of nitric oxide generation by the plant mitochondrial electron transport chain

Alber

Sivanesan

Vanlerberghe

2017

Plant Cell & Environment

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The plant mitochondrial electron transport chain (ETC) is bifurcated such that electrons from ubiquinol are passed to oxygen via the usual cytochrome path or through alternative oxidase (AOX). We previously showed that knockdown of AOX in transgenic tobacco increased leaf concentrations of nitric oxide (NO), implying that an activity capable of generating NO had been effected. Here, we identify the potential source of this NO. Treatment of leaves with antimycin A (AA, Q -site inhibitor of Complex III) increased NO amount more than treatment with myxothiazol (Myxo, Q -site inhibitor) despite both being equally effective at inhibiting respiration. Comparison of nitrate-grown wild-type with AOX knockdown and overexpression plants showed a negative correlation between AOX amount and NO amount following AA. Further, Myxo fully negated the ability of AA to increase NO amount. With ammonium-grown plants, neither AA nor Myxo strongly increased NO amount in any plant line. When these leaves were supplied with nitrite alongside the AA or Myxo, then the inhibitor effects across lines mirrored that of nitrate-grown plants. Hence the ETC, likely the Q-cycle of Complex III generates NO from nitrite, and AOX reduces this activity by acting as a non-energy-conserving electron sink upstream of Complex III.

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Section: Resultsmentioning

confidence: 97%

The occurrence and control of nitric oxide generation by the plant mitochondrial electron transport chain

Alber

Sivanesan

Vanlerberghe

2017

Plant Cell & Environment

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“…ROS are also produced in the mitochondria, for example by complex III at the outer side of the inner mitochondrial membrane (Cvetkovska et al, 2013, Ng et al, 2014, Huang et al, 2016). Such ROS are implicated in mitochondrial retrograde signaling.…”

Section: Introductionmentioning

confidence: 99%

RCD1 Coordinates Chloroplastic and Mitochondrial Electron Transfer through Interaction with ANAC Transcription Factors in Arabidopsis

Shapiguzov

Vainonen

Hunter

et al. 2018

Preprint

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43Signaling from chloroplasts and mitochondria, both dependent on reactive oxygen 44 species (ROS), merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 45 (RCD1). ROS produced in the chloroplasts affect the abundance, thiol redox state and 46 oligomerization of RCD1. RCD1 directly interacts in vivo with ANAC013 and ANAC017 47 transcription factors, which are the mediators of the ROS-related mitochondrial complex 48 III retrograde signa and suppresses activity of ANAC013 and ANAC017. Inactivation of 49 RCD1 leads to increased expression of ANAC013 and ANAC017-regulated genes 50 belonging to the mitochondrial dysfunction stimulon (MDS), including genes for 51 mitochondrial alternative oxidases (AOXs). Accumulating AOXs and other MDS gene 52 products alter electron transfer pathways in the chloroplasts, leading to diminished 53 production of chloroplastic ROS and increased protection of photosynthetic apparatus 54 from ROS damage. RCD1-dependent regulation affects chloroplastic and mitochondrial 55 retrograde signaling including chloroplast signaling by 3'-phosphoadenosine 5'-56 phosphate (PAP). Sensitivity of RCD1 to organellar ROS provides feedback control of 57 nuclear gene expression. 58 157 Nishiyama et al., 2011).To reveal the significance of RCD1 in responses to PSI-produced 158 chloroplastic ROS, rosettes of Arabidopsis were pre-treated overnight in darkness with 159 MV and exposed to light. After the dark period, the plants displayed unchanged PSII 160 photochemical yield (Fv/Fm). Subsequent exposure to three hours of light resulted in 161 decrease of Fv/Fm in wild type (Col-0) (Fig. 1A), but not in the rcd1 mutant. Moreover, 162 tolerance of rcd1 was evident under various concentrations of MV (Fig. 1B). The 163 superoxide anion is an unstable compound that is enzymatically reduced to the more 164 long-lived H2O2. Chloroplastic production of H2O2 in the presence of MV in the light was 165 assessed by staining plants with 3,3′-diaminobenzidine (DAB). After pre-treatment with 166 MV, higher H2O2 accumulation was evident in both Col-0 and rcd1 (Fig. S1A). Subsequent 167 incubation of these plants under light led to a time-dependent increase in the H2O2 168accumulation in Col-0, but not in rcd1. 169 In several MV-tolerant mutants the resistance is based on restricted access of MV to 170 chloroplasts (Hawkes 2014). However, in rcd1 pretreatment with MV led to initial increase 171 in H2O2 production similar to that in the wild type ( Fig. S1A), suggesting that resistance 172 of rcd1 was not due to restricted delivery of MV to PSI. In order to test this directly, 173 oxidation of PSI was assessed by in vivo spectroscopy using DUAL-PAM. Leaves were 174 adapted to far-red light, which is more efficiently used by PSI than PSII. Under these 175 conditions PSI is producing electrons at a faster rate than it is supplied by electrons 176 coming from PSII, and hence the PSI reaction center P700 becomes oxidized. Then a 177 flash of orange light was provided that is efficiently absorbed by PSII. Electrons generated...

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“…This in turn will reduce the probability of the single electron leak from the ETC that can generate superoxide and nitric oxide (Møller 2001, Poyton et al 2009). Since ROS and reactive nitrogen species can act as signaling molecules, it is possible that AOX has a role in defining such signaling from the mitochondrion (Giraud et al 2008, Van Aken et al 2009, Vanlerberghe et al 2009, Cvetkovska et al 2013.…”

Section: Introductionmentioning

confidence: 99%

A lack of mitochondrial alternative oxidase compromises capacity to recover from severe drought stress

Wang

Vanlerberghe

2013

Physiologia Plantarum

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Alternative oxidase (AOX) constitutes a nonenergy conserving branch of the mitochondrial electron transport chain. AOX activity may be important to avoid reactive oxygen species (ROS) generation by the chain, particularly during abiotic stress. We compared leaf AOX1a transcript and AOX protein amounts in wild-type (WT) Nicotiana tabacum plants experiencing mild to severe drought. Mild to moderate drought resulted in a progressive and modest increase in AOX amount, accompanied by a progressive increased expression of different ROS-scavenging components. Under these conditions, transgenic plants with suppressed AOX amount, due to an RNA interference construct, were not compromised in their ability to manage ROS load and prevent cellular damage. Severe drought stress, particularly when combined with increased irradiance, strongly increased AOX amount in WT tobacco and this coincided with an increase in total respiration and, despite further induction of ROS-scavenging systems, some evidence of cellular damage. Under these severe conditions, plants lacking AOX suffered more cellular damage than WT and, at the most severe stage, were found to downregulate rather than upregulate the transcript level of several important ROS-scavenging components. At this stage, WT plants could still recover rapidly after rewatering, but the recoverability of AOX knockdown plants was strongly compromised.

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The signaling role of a mitochondrial superoxide burst during stress

Cited by 27 publications

References 50 publications

The occurrence and control of nitric oxide generation by the plant mitochondrial electron transport chain

The occurrence and control of nitric oxide generation by the plant mitochondrial electron transport chain

RCD1 Coordinates Chloroplastic and Mitochondrial Electron Transfer through Interaction with ANAC Transcription Factors in Arabidopsis

A lack of mitochondrial alternative oxidase compromises capacity to recover from severe drought stress

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