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

Abstract

ORCID IDs: 0000-0001-5369-7911 (S.W.); 0000-0003-4024-968X (O.V.A.); 0000-0003-0796-8308 (M.S.).Cells of complex organisms typically rely on mitochondria for energy provision. The amount of energy required to sustain cellular activity can vary strongly depending on external conditions. Vice versa, constraints on respiratory activity due to metabolic status or stress insult require mitochondrial signaling to coordinate cellular physiology with the function of the organelle. In this update, we review recent insights into plant mitochondrial energy signaling in the light of their significance to stress acclimation. First, we focus on the characteristic adjustments of the nuclear transcriptome that occur after pharmacological inhibition of the mitochondrial electron transport chain as the output of mitochondrial retrograde signaling. Second, we discuss the proteins that have recently been identified as regulators of the transcript responses and the emerging picture of their action as a signaling network. We then pose the question of how well our current models of inducing mitochondrial dysfunction relate to conditions that plants face naturally. We reason that low-oxygen stress shows striking similarities with electron transport inhibitors with respect to their impact on mitochondrial energy physiology upstream, as well as the cellular transcriptomic response. Finally, we highlight and discuss changes in mitochondrial physiology that are common to both stimuli as candidates for upstream signals. The aim of this update is to better define the physiological context in which mitochondrial signaling operates to provide new directions for future research. RESPONSES TO MITOCHONDRIAL ENERGY SIGNALING AT THE TRANSCRIPT LEVEL

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

“…In contrast, anterograde (= nucleus to organelle) signals mainly regulate biogenesis of the organelles as well as maintenance, for example, in repair processes during stress situations. This topic is further discussed in another review of this special issue focusing on mitochondrial retrograde signals (Wagner et al, 2018). The finding that bZIP63 is a direct regulator of ETFQO and thereby affects mitochondrial electron transport (Pedrotti et al, 2018) and the identification of several differentially phosphorylated proteins in chloroplasts and mitochondria in AKIN10/11 mutants (Nukarinen et al, 2016) prompted us to screen further for target genes of those TFs, which have been identified as SnRK1 targets.…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…The importance of mitochondrial energy and redox state in signaling when O 2 is limiting is comprehensively discussed by Wagner et al (2018). Their analysis complements the review by Schmidt et al (2018) that highlights integration of responses to O 2 deficiency, including consequences of mitochondrial electron transport inhibition and ROS release.…”

“…Updates in this issue consider how O 2 deficiency is managed through integrated signaling and response networks that reconfigure gene expression and metabolism and promote changes in anatomy or morphology that enhance aeration. These involve both direct and indirect sensing of changes in cellular O 2 homeostasis, with the latter involving the mitochondrion and both anterograde and retrograde signaling (Schmidt et al, 2018;Wagner et al, 2018). The low O 2 levels intrinsic to some developmental zones, such as meristems, also guide developmental processes in consort with light and carbon availability, as described for seasonal progressions in axillary buds (Signorelli et al, 2018).…”

“…The latter catalyze the first step in ERF-VII turnover through oxidation of an evolutionarily conserved N-terminal Cys to a Cys-sulfonic acid residue (White et al, 2017). Nitric oxide also is important in the conditional regulation of ERF-VII abundance (Giuntoli and Perata, 2018;Sasidharan et al, 2018;Wagner et al, 2018).…”

Oxygen Sensing and Integrative Stress Signaling in Plants

“…Indeed, roles for these diverse signals in mitochondrial retrograde responses have been established and are discussed by Wagner et al (2018) in this Focus Issue. The role of mitochondrial retrograde signals in hypoxia has been partly investigated; for example, mitochondrial ROS signals were shown to impact on anoxia tolerance (Chang et al, 2012).…”