Decreasing electron flux through the cytochrome and/or alternative respiratory pathways triggers common and distinct cellular responses dependent on growth conditions.

Kristina Kühn,Catherine Colas Des Francs Small,Estelle Giraud,Simon R Law,Parwinder Kaur,Szymon Kubiszewski-Jakubiak,Guangkun Yin,Owen Duncan,Reena Narsai,Etienne Meyer,Yan Wang,James Whelan

doi:10.1104/pp.114.249946

Abstract

Diverse signaling pathways are activated by perturbation of mitochondrial function under different growth conditions.Mitochondria have emerged as an important organelle for sensing and coping with stress in addition to being the sites of important metabolic pathways. Here, responses to moderate light and drought stress were examined in different Arabidopsis (Arabidopsis thaliana) mutant plants lacking a functional alternative oxidase (alternative oxidase1a [aox1a]), those with reduced cytochrome electron transport chain capacity (T3/T7 bacteriophage-type RNA polymerase, mitochondrial, and plastidial [rpoTmp]), and double mutants impaired in both pathways (aox1a:rpoTmp). Under conditions considered optimal for growth, transcriptomes of aox1a and rpoTmp were distinct. Under adverse growth conditions, however, transcriptome changes in aox1a and rpoTmp displayed a highly significant overlap and were indicative of a common mitochondrial stress response and down-regulation of photosynthesis. This suggests that the role of mitochondria to support photosynthesis is provided through either the alternative pathway or the cytochrome pathway, and when either pathway is inhibited, such as under environmental stress, a common, dramatic, and succinct mitochondrial signal is activated to alter energy metabolism in both organelles. aox1a:rpoTmp double mutants grown under optimal conditions showed dramatic reductions in biomass production compared with aox1a and rpoTmp and a transcriptome that was distinct from aox1a or rpoTmp. Transcript data indicating activation of mitochondrial biogenesis in aox1a:rpoTmp were supported by a proteomic analysis of over 200 proteins. Under optimal conditions, aox1a:rpoTmp plants seemed to switch on many of the typical mitochondrial stress regulators. Under adverse conditions, aox1a:rpoTmp turned off these responses and displayed a biotic stress response. Taken together, these results highlight the diverse signaling pathways activated by the perturbation of mitochondrial function under different growth conditions.

Highlights

Diverse signaling pathways are activated by perturbation of mitochondrial function under different growth conditions
To investigate the effects of limitation of electron flow through the alternative or cytochrome mitochondrial electron transport chain under normal and stress conditions, mutants lacking the alternative oxidase (AOX) or mutants with dramatically decreased complex I and IV levels were investigated. aox1a mutants lack a functional AOX1a protein (At3g22370), whereas rpoTmp mutants are defective in the dual-targeted mitochondrial and plastidial RNA polymerase (At5g15700). rpoTmp plants display specific defects in transcript abundance of mitochondrial-located genes that cause a reduction in the accumulation of complexes I and IV, and rpoTmp mitochondria show only approximately 15% of the complex IV capacity measured for the wild type (Kühn et al, 2009)
To gain an understanding of the effects that the aox1a and rpoTmp mutations have on respiratory capacity and investigate possible compensatory effects through other pathways of electron transfer, respiratory capacity was analyzed in mitochondria isolated from mutant lines or wildtype (Columbia-0 [Col-0]) plants grown under normal growth conditions (Fig. 1A)

Summary

Introduction

Diverse signaling pathways are activated by perturbation of mitochondrial function under different growth conditions. Transcriptome changes in aox1a and rpoTmp displayed a highly significant overlap and were indicative of a common mitochondrial stress response and downregulation of photosynthesis. This suggests that the role of mitochondria to support photosynthesis is provided through either the alternative pathway or the cytochrome pathway, and when either pathway is inhibited, such as under environmental stress, a common, dramatic, and succinct mitochondrial signal is activated to alter energy metabolism in both organelles. Aox1a:rpoTmp turned off these responses and displayed a biotic stress response Taken together, these results highlight the diverse signaling pathways activated by the perturbation of mitochondrial function under different growth conditions. More detailed studies on the role of AOX in tobacco and Arabidopsis (Arabidopsis thaliana) showed that it suppresses the production of ROS (see studies outlined above) and, by its activity, it mediates or determines signals coming from mitochondria (Arnholdt-Schmitt et al, 2006; Clifton et al, 2006; Vanlerberghe et al, 2009)

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