Mitochondrial Energy and Redox Signaling in Plants

Abstract

Significance: For a plant to grow and develop, energy and appropriate building blocks are a fundamental requirement. Mitochondrial respiration is a vital source for both. The delicate redox processes that make up respiration are affected by the plant's changing environment. Therefore, mitochondrial regulation is critically important to maintain cellular homeostasis. This involves sensing signals from changes in mitochondrial physiology, transducing this information, and mounting tailored responses, by either adjusting mitochondrial and cellular functions directly or reprogramming gene expression. Recent Advances: Retrograde (RTG) signaling, by which mitochondrial signals control nuclear gene expression, has been a field of very active research in recent years. Nevertheless, no mitochondrial RTG-signaling pathway is yet understood in plants. This review summarizes recent advances toward elucidating redox processes and other bioenergetic factors as a part of RTG signaling of plant mitochondria. Critical Issues: Novel insights into mitochondrial physiology and redoxregulation provide a framework of upstream signaling. On the other end, downstream responses to modified mitochondrial function have become available, including transcriptomic data and mitochondrial phenotypes, revealing processes in the plant that are under mitochondrial control. Future Directions: Drawing parallels to chloroplast signaling and mitochondrial signaling in animal systems allows to bridge gaps in the current understanding and to deduce promising directions for future research. It is proposed that targeted usage of new technical approaches, such as quantitative in vivo imaging, will provide novel leverage to the dissection of plant mitochondrial signaling.

Immobilized Subpopulations of Leaf Epidermal Mitochondria Mediate PENETRATION2-Dependent Pathogen Entry Control in Arabidopsis

“…In particular, exemplary studies have emphasized the importance of salicylic acid-triggered mitochondrial ROS production (Gleason et al, 2011), controlled mitochondrial protein import (Huang et al, 2013), and mitochondrial retrograde signaling control (Vellosillo et al, 2013) in defense against microbial pathogens. These finding are supported by recent Arabidopsis transcriptome meta-analyses suggesting that upregulation of defense gene expression might be under mitochondrial retrograde control (Schwarzländer et al, 2012) and that transcripts of alternative respiration, representing marker genes for retrograde signaling, are specifically induced by Bgh attack (Schwarzländer and Finkemeier, 2013). Consequently, it is not surprising that microbial pathogens evolved effector molecules that target mitochondria in order to manipulate their functionality (Block et al, 2010).…”

“…Using Arabidopsis lines expressing the mitochondrial redox sensor mtroGFP2, we were able to show here that mitochondria immobilized at plant-microbe interaction sites exhibit a redox shift toward oxidation as a likely consequence of localized generation of ROS. Regardless of whether mitochondria are the prime source of ROS, or a target for oxidative damage, or whether perturbation of mitochondrial function and dynamics is the cause or consequence of the observed elevated oxidation status, it is important to note that mitochondrial ROS can trigger retrograde signaling and hypersensitive cell death in plants (Schwarzländer and Finkemeier, 2013;Ng et al, 2014). Thus, it is tempting to speculate that the original evolutionary function of the mitochondrial subpopulation observed in this study was to contribute to pathogen-induced retrograde signaling to the nucleus and transcriptional reprogramming.…”

“…Thus, it is possible that the recruitment of plant mitochondria to interaction sites with invading microbes may also supply ATP for energy-dependent transport and secretion at the plasma membrane. Moreover, as the respiratory machinery is very sensitive to changing redox conditions, mitochondria are also known to function as sensors for cellular functional imbalance (Schwarzländer and Finkemeier, 2013;Ng et al, 2014). Thus, changes in the mitochondrial redox status can induce signaling events leading to direct effects on mitochondrial function and dynamics and to adaptations in gene expression via retrograde signaling between mitochondria and the nucleus.…”

Transcriptomic Analysis of the Role of Carboxylic Acids in Metabolite Signaling in Arabidopsis Leaves

“…Perturbation of mitochondrial function often leads to an oxidative inhibition of the mitochondrial aconitase, which is followed by a rise in cellular citrate levels (Vanlerberghe and McIntosh, 1994;Morgan et al, 2008;Lehmann et al, 2009;Gupta et al, 2012). Mitochondrial citrate was discussed as a possible mediator of mitochondrial retrograde signals in plants as well as in yeast cells, but an in-depth transcriptome study was lacking so far (Vanlerberghe and McIntosh, 1994;Mackenzie and McIntosh, 1999;McCammon et al, 2003;Clifton et al, 2005;Schwarzländer and Finkemeier, 2013). Vanlerberghe and McIntosh (1996) already reported that the AOX1 transcript level responded to increased levels of citrate that were supplied externally or were increased internally through the inhibition of aconitase using monofluroacetate.…”

The Membrane-Bound NAC Transcription Factor ANAC013 Functions in Mitochondrial Retrograde Regulation of the Oxidative Stress Response in Arabidopsis

“…In addition to their damaging effects, mtROS probably act as MRR-triggering signaling molecules (Vanlerberghe et al, 2002;Rhoads et al, 2006). Calcium originating from the mitochondria might also be an MRR signal (Subbaiah et al, 1998), as seen in mammalian cells (Butow and Avadhani, 2004), as well as changes in mitochondrial redox status and metabolites (Schwarzländer and Finkemeier, 2013).…”