Elsevier

Mitochondrion

Volume 7, Issue 3, May 2007, Pages 177-194
Mitochondrion

Review
Mitochondrial retrograde regulation in plants

https://doi.org/10.1016/j.mito.2007.01.002Get rights and content

Abstract

Plant cells must react to a variety of adverse environmental conditions that they may experience on a regular basis. Part of this response centers around (1) ROS as damaging molecules and signaling molecules; (2) redox status, which can be influenced by ROS production; and (3) availability of metabolites. All of these are also likely to interface with changes in hormone levels [Desikan, R., Hancock, J., Neill, S., 2005. Reactive oxygen species as signalling molecules. In: Smirnoff, N. (ed.), Antioxidants and reactive oxygen species in plants. Blackwell Pub. Ltd., Oxford, pp. 169–196; Kwak, J.M., Nguyen, V., Schroeder, J.I., 2006. The role of reactive oxygen species in hormonal responses. Plant Physiol. 141, 323–329]. Each of these areas can be strongly influenced by changes in mitochondrial function. Such changes trigger altered nuclear gene expression by a poorly understood process of mitochondrial retrograde regulation (MRR), which is likely composed of several distinct signaling pathways. Much of what is known about plant MRR centers around the response to a dysfunctional mtETC and subsequent induction of genes encoding proteins involved in recovery of mitochondrial functions, such as AOX and alternative NAD(P)H dehydrogenases, and genes encoding enzymes aimed at regaining ROS level/redox homeostasis, such as glutathione transferases, catalases, ascorbate peroxidases and superoxide dismutases. However, as evidence of new and interesting targets of MRR emerge, this picture is likely to change and the complexity and importance of MRR in plant responses to stresses and the decision for cells to either recover or switch into programmed cell death mode is likely to become more apparent.

Introduction

Abiotic stresses, biotic stresses, or mutations can alter the functioning of organelles. In response, organelles can direct changes in nuclear gene expression. The alteration of nuclear gene expression directed by organelles through organelle-to-nucleus signaling is referred to as retrograde communication, retrograde signaling, retrograde stress signaling or retrograde regulation (Butow and Avadhani, 2004, Liao and Butow, 1993, Patil and Walter, 2001, Rhoads and Vanlerberghe, 2004, Rodermel, 2001, Surpin et al., 2002). In the case of plant mitochondria-to-nucleus signaling, we refer to it as mitochondrial retrograde regulation (MRR). Signaling due to changes in mitochondrial function could link to metabolic signaling pathways or general reactive oxygen species (ROS) signaling pathways and trigger gene expression responses, but these would still be mitochondria-directed responses. Mounting evidence indicates that retrograde regulation is an important regulatory/response mechanism for plants, animals and fungi. This is a new but rapidly expanding area of biology. Relatively little attention has been given to retrograde regulation in plants especially to MRR.

In animals, mitochondrial dysfunction, and the MRR that likely results, is now thought to be an important factor in many human diseases (Butow and Avadhani, 2004, Lane, 2006, Weissig et al., 2004). Mitochondrial dysfunction, and in some cases MRR, has been connected to Alzheimer’s disease (Moreira et al., 2006, Parihar and Brewer, 2007), Parkinson’s disease (Beal, 2005, Kwong et al., 2006), Huntington’s disease (Beal, 2005, Kwong et al., 2006, Marx, 2005), bipolar disorder (Iwamoto et al., 2005, Kato, 2005), schizophrenia (Ben-Shachar and Laifenfeld, 2004, Iwamoto et al., 2005), type 2 diabetes (Guo et al., 2005, Lowell and Shulman, 2005), cancer ( Butow and Avadhani, 2004, Singh et al., 2005), and aging (Beal, 2005, Butow and Avadhani, 2004). MRR is a relatively new angle on the importance of mitochondria in diseases (Biswas et al., 2005, Butow and Avadhani, 2004, Singh et al., 2005).

Although some target genes are in common among MRR pathways, there seem to be several distinct MRR signaling pathways in animals (Butow and Avadhani, 2004).

MRR in yeast has been well studied. The yeast Saccharomyces cerevisiae responds to mitochondrial dysfunction by altering nitrogen and carbon metabolism (Butow and Avadhani, 2004). Respiratory deficient cells shift metabolism in an attempt to maintain glutamate levels by restoring levels of TCA cycle intermediates. Gene induction involves regulation by RTG transcription factors in many of the best studied cases (Butow and Avadhani, 2004, Poyton and McEwen, 1996, Sekito et al., 2000), but at least two other MRR signaling pathways are present in S. cerevisiae (Devaux et al., 2002, Guaragnella and Butow, 2003).

Plants contain two energy-producing organelles: chloroplasts, which convert sunlight to chemical energy in the form of ATP and stored energy in the form of carbon compounds such as sugars and lipids, and mitochondria, which convert stored energy to ATP. Both organelles are able to communicate with the nucleus. Chloroplastic retrograde regulation pathways are, to date, the best studied retrograde signaling pathways in plants. Potential pathways have been identified for signaling in response to photomorphogenesis (Surpin et al., 2002), altered function during chloroplast biogenesis (Barr et al., 2004), and redox poise (Rodermel, 2001). In this review, we focus on our current understanding of MRR in plants, which has been revealed primarily in instances of mitochondrial dysfunction. Mitochondrial dysfunction caused by mutations in plants often results in male sterility, in an embryo lethal phenotype, or in chlorotic plants that do not survive to maturity (Newton et al., 2004). In addition, mitochondrial dysfunction in plants can be caused by abiotic and biotic stresses. Although relatively little is known about the specific cellular consequences of mitochondrial dysfunction in plants, there is growing evidence that the responses of mitochondria to biotic and abiotic stresses contribute significantly to overall plant stress responses. The molecular mechanisms used by retrograde signaling pathways have just begun to be defined; a few components have been identified in some cases. Mitochondria likely play vital roles in stress responses by contributing to altered nuclear gene expression. A great deal of flexibility in responses to stresses is especially important for plants because they are sessile and these changes in nuclear gene expression likely contribute to this flexibility. The responses of mitochondria to stresses, including the specific target genes of MRR in individual stress responses, may determine the fate of plant cells, resulting in either recovery or cell death (Fig. 1).

Section snippets

MRR from chemical disruption of mitochondrial function and in mitochondrial mutants

In plants, some fungi, some animals, and some protozoans the mitochondrial electron transport chain (mtETC) consists of two, partially overlapping respiratory pathways: the cytochrome respiratory pathway which has cytochrome oxidase (COX) as the terminal oxidase and the alternative respiratory pathway, which has alternative oxidase (AOX) as the terminal oxidase (Finnegan et al., 2004, Mackenzie and McIntosh, 1999, McDonald and Vanlerberghe, 2004, Siedow, 1995, Siedow and Umbach, 1995,

MRR in response to abiotic stresses

Plant mitochondria may function as general sensors of stresses and initiate cellular responses to specific stresses, or, at least contribute to the overall response to a given stress (Fig. 1; Jones, 2000). This may include both responses to abiotic stresses and biotic stresses.

MRR in response to biotic stresses

Although the precise roles have not yet been elucidated, there is evidence for the importance of plant mitochondria during pathogen attack, including the involvement of MRR. Increased respiration during pathogen attack has been documented (Baker et al., 2000, Baker et al., 2001). This may be due to the need for increased energy during infection, but it may also result in increased mtROS production resulting from an inhibition of respiration caused by the pathogen during the infection. Again,

ROS are involved in plant MRR associated with mtETC disruption

It is clear that a dramatically increased cellular ROS level is a common feature of abiotic and biotic plant stresses and that an increased cellular ROS level causes altered nuclear gene expression (Inzé and Van Montagu, 1995, Jones, 2000, Kubo et al., 1999, Kuzniak and Urbanek, 2000, Taylor et al., 2002, Vranová et al., 2002). However, the precise roles of ROS in plant stress responses and the role(s), if any, of ROS in all types of MRR are not clear. ROS are both potential damaging compounds

MRR and the choice between recovery and programmed cell death

Apoptosis is a form of PCD that has defined cell morphological changes and, in animals, can clearly be directed by mitochondria (Green and Reed, 1998). Recently it was shown that mammalian cells responding to mitochondrial dysfunction with MRR are more resistant to apoptosis due to induced expression of anti-apoptotic proteins, suggesting that these events are directly connected in animals (Biswas et al., 2005). Several studies indicate that mitochondria can direct at least some forms of PCD in

Multiple MRR pathways in plants

Compelling evidence suggests that multiple types of mitochondrial signaling pathways exist in plants (Djajanegara et al., 2002, Gray and McIntosh, 1998, Karpova et al., 2002, Kuzmin et al., 2004, Zarkovic et al., 2005). These include the observation that citrate addition (which is assumed to affect mitochondrial function) induces AOX gene expression in both suspension-cultured tobacco cells and suspension-cultured soybean cells, but does not cause detectable increases in ROS (Djajanegara et

Summary

Plant cells must react to a variety of adverse environmental conditions that they may experience on a regular basis. Part of this response centers around (1) ROS as damaging molecules and signaling molecules; (2) redox status, which can be influenced by ROS production; (3) energy status; and (4) availability of metabolites. All of these are also likely to interface with changes in hormone levels (Desikan et al., 2005, Kwak et al., 2006). Each of these areas can be strongly influenced by changes

Acknowledgements

We thank Dr. Ann L. Umbach for helpful discussions and critical reading of this manuscript and Samuel J. White for help with manuscript preparation.

References (201)

  • N. Guaragnella et al.

    ATO3 encoding a putative outward ammonium transporter is an RTG-independent retrograde responsive gene regulated by GCN4 and the Ssy1-Ptr3-Ssy5 amino acid sensor system

    J. Biol. Chem.

    (2003)
  • L.J. Guo et al.

    Mitochondrial genome polymorphisms associated with type-2 diabetes or obesity

    Mitochondrion

    (2005)
  • D. Inzé et al.

    Oxidative stress in plants

    Curr. Opin. Biotech.

    (1995)
  • A. Jones

    Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?

    Trends Plant Sci.

    (2000)
  • T. Kato

    Mitochondrial dysfunction in bipolar disorder: from 31P-magnetic resonance spectroscopic findings to their molecular mechanisms

    Int. Rev. Neurobiol.

    (2005)
  • T. Kumagai et al.

    4-hydroxy-2-nonenal, the end product of lipid peroxidation, is a specific inducer of cyclooxygenase-2 gene expression

    Biochem. Biophys. Res. Commun.

    (2000)
  • E.V. Kuzmin et al.

    Mitochondrial respiratory deficiencies signal up-regulation of genes for heat shock proteins

    J. Biol. Chem.

    (2004)
  • X. Liao et al.

    RTG1 and RTG2: two yeast genes required for a novel path of communication from mitochondria to the nucleus

    Cell

    (1993)
  • G.P. Miles et al.

    RNA interference-based (RNAi) suppression of AtMPK6, an Arabidopsis mitogen-activated protein kinase, results in hypersensitivity to ozone and misregulation of AtMPK3

    Environ. Pollut.

    (2005)
  • R. Ahlfors et al.

    Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure

    Plant J.

    (2004)
  • L.E. Anderson et al.

    Three enzymes of carbon metabolism, or their antigenic analogs, in pea nuclei

    Plant Physiol.

    (1995)
  • J. Bailey-Serres et al.

    Sensing and signalling in response to oxygen deprivation in plants and other organisms

    Ann. Bot.

    (2005)
  • J. Balk et al.

    The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release

    Plant Cell

    (2001)
  • J. Barr et al.

    The GHOST terminal oxidase regulates developmental programming in tomato fruit

    Plant Cell Environ.

    (2004)
  • U. Basu et al.

    Transgenic Brassica napus plants overexpressing aluminum-induced mitochondrial manganese superoxide dismutase cDNA are resistant to aluminum

    Plant Cell Environ.

    (2001)
  • M.F. Beal

    Mitochondria take center stage in aging and neurodegeneration

    Ann. Neurol.

    (2005)
  • S. Bourque et al.

    The elicitor cryptogein blocks glucose transport in tobacco cells

    Plant Physiol.

    (2002)
  • A. Boveris et al.

    Production of superoxide radicals and hydrogen peroxide in mitochondria

  • C. Branco-Price et al.

    Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation

    Ann. Bot.

    (2005)
  • W.W.P. Chang et al.

    Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry

    Plant Physiol.

    (2000)
  • R. Chapman et al.

    Intracellular signaling from the endoplasmic reticulum to the nucleus

    Annu. Rev. Cell Dev. Biol.

    (1998)
  • W. Chen et al.

    The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element

    Plant J.

    (1999)
  • W. Chen et al.

    Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses

    Plant Cell

    (2002)
  • S.H. Cheng et al.

    Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family

    Plant Physiol.

    (2002)
  • H.J. Chung et al.

    Arabidopsis alcohol dehydrogenase expression in both shoots and roots is conditioned by root growth environment

    Plant Physiol.

    (1999)
  • R. Clifton et al.

    Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana

    Plant Mol. Biol.

    (2005)
  • S.M. Coelho et al.

    Spatiotemporal patterning of reactive oxygen production and Ca2+ wave propagation in Fucus rhizoid cells

    Plant Cell

    (2002)
  • M.J. Curtis et al.

    The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death

    Plant J.

    (2002)
  • J. Dat et al.

    Dual action of the active oxygen species during plant stress responses

    Cell Mol. Life Sci.

    (2000)
  • E. Daugas et al.

    Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis

    FASEB J.

    (2000)
  • M.C. de Pinto et al.

    Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells

    Plant Physiol.

    (2002)
  • R. Desikan et al.

    Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures

    Biochem. J.

    (1998)
  • R. Desikan et al.

    Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMAPK4 and AtMAPK6

    Plant Physiol.

    (2001)
  • R. Desikan et al.

    Reactive oxygen species as signalling molecules

  • I. Djajanegara et al.

    Regulation of alternative oxidase gene expression in soybean

    Plant Mol. Biol.

    (2002)
  • D. Dojcinovic et al.

    Identification of regions of the Arabidopsis AtAOX1a promoter important for developmental and mitochondrial retrograde regulation of expression

    Plant Mol. Biol.

    (2005)
  • M.C. Drew

    Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1997)
  • C. Dutilleul et al.

    Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation

    Plant Cell

    (2003)
  • C. Dutilleul et al.

    Mitochondria-driven changes in leaf NAD status exert a crucial influence in the cantrol of nitrate assimilation and the integration of carbon and nitrogen metabolism

    Plant Physiol.

    (2005)
  • J.M. Escoubas et al.

    Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool

    Proc. Natl. Acad. Sci. USA

    (1995)
  • Cited by (233)

    • Cyanide resistant respiration and the alternative oxidase pathway: A journey from plants to mammals

      2022, Biochimica et Biophysica Acta - Bioenergetics
      Citation Excerpt :

      In plants, AOX also confers metabolic plasticity, enabling organisms to adapt to various biotic and abiotic stress factors such as drought, salinity, osmotic stress, nutrient deprivation, infection by pathogens or extreme conditions of light and temperature: many of which have been linked to ROS [112–126]. AOX also influences fungal biology in ways linked to ROS, in many cases with effects on pathogenicity [126–132]. How broadly AOX protects animals endowed with it against similar stress conditions remains an open question.

    View all citing articles on Scopus
    View full text