Mitochondrial composition, function and stress response in plants

Journal of Integrative Plant Biology 2012, 54 (11): 887–906

Invited Expert Review

Mitochondrial Composition, Function and StressResponse in PlantsF

Richard P. Jacoby1,2, Lei Li1,2, Shaobai Huang1,2, Chun Pong Lee3, A. Harvey Millar1,2∗

and Nicolas L. Taylor1,21ARC Centre of Excellence in Plant Energy Biology and 2Centre for Comparative Analysis of Biomolecular Networks (CABiN), MCSBuilding M316, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Western Australia, Australia3Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom∗Corresponding author

E-mail: [email protected] Articles can be viewed online without a subscription.Available online on 10 October 2012 at www.jipb.net and www.wileyonlinelibrary.com/journal/jipbdoi: 10.1111/j.1744-7909.2012.01177.x

A. Harvey Millar

(Corresponding author)

Abstract

The primary function of mitochondria is respiration, wherecatabolism of substrates is coupled to ATP synthesis via oxidativephosphorylation. In plants, mitochondrial composition is relativelycomplex and flexible and has specific pathways to support pho-tosynthetic processes in illuminated leaves. This review beginswith outlining current models of mitochondrial composition in plantcells, with an emphasis upon the assembly of the complexes ofthe classical electron transport chain (ETC). Next, we focus uponthe comparative analysis of mitochondrial function from differenttissue types. A prominent theme in the plant mitochondrial literatureinvolves linking mitochondrial composition to environmental stress

responses, and this review then gives a detailed outline of how oxidative stress impacts upon theplant mitochondrial proteome with particular attention to the role of transition metals. This is followedby an analysis of the signaling capacity of mitochondrial reactive oxygen species, which studies thetranscriptional changes of stress responsive genes as a framework to define specific signals emanatingfrom the mitochondrion. Finally, specific mitochondrial roles during exposure to harsh environments areoutlined, with attention paid to mitochondrial delivery of energy and intermediates, mitochondrial supportfor photosynthesis, and mitochondrial processes operating within root cells that mediate tolerance toanoxia and unfavorable soil chemistries.

Keyword: Plant mitochondria; respiration; oxidative stress; electron transport chain; complex assembly; ROS signaling; carbon.

Jacoby RP, Li L, Huang S, Lee CP, Millar AH, Taylor NL (2012) Mitochondrial composition, function and stress response in plants. J. Integr. PlantBiol. 54(11), 887–906.

Introduction

The ATP needed for cellular maintenance and growth in or-

ganisms comes from respiration. It is the fundamental energy-

conserving process that couples the transfer of potential energy

from the oxidation of reduced organic matter to high-energy

intermediates and heat. In aerobic respiration, which yields

the highest efficiency of conversion to high-energy interme-

diates, mitochondria carry out the final steps to generate the

bulk of the ATP through oxidative phosphorylation driven by

oxidation of organic acids, to release CO2 and reduce O2 to

water. However, mitochondria also play roles in a variety of

important cellular processes associated with carbon, nitrogen,

phosphorus and sulfur metabolism in plants. In photosynthetic

tissues, mitochondria function is indispensable for chloroplast

function. Mitochondria are key agents in how plants respond

C© 2012 Institute of Botany, Chinese Academy of Sciences

888 Journal of Integrative Plant Biology Vol. 54 No. 11 2012

to oxidative stress, and plant mitochondria possess unique

respiratory properties to enable these processes. Understand-

ing the control and regulation of the respiratory processes

is vital to alter the rate of plant biomass production and to

explain plant growth and its variability in different environmental

conditions. An exhaustive analysis of all the elements involved

in these processes is not possible here, but by using specific

examples and recent discoveries we can highlight some key

elements in the structure, mechanism and regulation of this

process. Firstly, we will consider the composition of the key

processes in mitochondrial respiration, our understanding of

the mechanism and regulation of the assembly process that

builds the machinery and the differential steady-states and

roles of these functions in different plant tissue types. Secondly,

we will review our understanding of the regulatory changes

induced by internal factors (signalling processes, redox control

and oxidative stress) and by the environment (salinity, osmotic

stress and nutrient deprivation).

Plant Mitochondrial Composition andAssembly

The functional steps of the respiratory apparatus in plant

mitochondria can be framed as a sequential set of processes,

involving the transport of reduced glycolytic products from

the cytosol into the mitochondrion, and then encompassing

a series of reactions leading to the release of CO2 and

reduction of O2 to water. Firstly, a set of carriers and channels

allow substrates and cofactors from the cytosol to enter the

mitochondria and also facilitate the release of the products

of respiration to the rest of the cell. Next, the tricarboxylic

acid cycle (TCAC) and associated enzymes undertake the

oxidative decarboxylation of organic acids to reduce NAD(P)+

and FAD+ to NAD(P)H and FADH2, respectively, and to drive

substrate level phosphorylation of ADP to ATP. Thirdly, the

classical OXPHOS electron transport chain (ETC) couples the

oxidation of NAD(P)H and FADH2 to the reduction of O2 and

the co-committed translocation of protons used to build an

electrical gradient to drive oxidative phosphorylation. Finally,

non-phosphorylating bypasses of the electron transport chain,

the alternative oxidase and rotenone-insensitive NAD(P)H de-

hydrogenases, can alter the gearing between the TCA cycle

and OXPHOS to facilitate the anaplerotic function of plant

mitochondria for organic acid provision to cellular biosynthetic

pathways without the full TCA cycle. This machinery and

the regulation of pathways to assemble it define the primary

functional composition of mitochondria.

Respiratory metabolite transporters

The two membranes of mitochondria have very different per-

meability properties. The outer membrane allows relatively non-

specific transport of small molecules from the cytosol into the

inter-membrane space (Mannella 1992; Mannella et al. 2001).

The inner membrane contains very selective transporters for

small molecules to the matrix space. This allows a complex set

of inner membrane carrier functions to have a large influence

on the functions of mitochondria (Laloi 1999). Transport across

the outer membrane is largely via the voltage dependent

anion channels (VDAC), that form β-barrel pores for the move-

ment of respiratory substrates and products up to 1000 Da

(Mannella and Tedeschi 1987; Robert et al. 2012). A family of

related mitochondrial inner membrane carriers operate for the

transport of organic acids, amino acids, inorganic phosphate

and nucleotides. Complementation assays have defined the

mitochondrial inorganic phosphate carriers (Hamel et al. 2004),

and adenine di- and tri-nucleotide carriers (Palmieri et al. 2008)

in plants. A general carrier able to transport a variety or both di-

and tricarboxylic acids is likely to carry the bulk of organic acid

traffic (Picault et al. 2002). Basic amino acid carriers have been

identified that transport arginine, ornithine, lysine and histidine

(Catoni et al. 2003a; Hoyos et al. 2003), a succinate-fumarate

carrier has been identified (Catoni et al. 2003b) and the cofactor

NAD+ has a specific carrier in plant mitochondria (Palmieri

et al. 2009).

Tricarboxylic acid cycle

The nine enzymes of the TCAC represent the major carbon

metabolising machinery present in plant mitochondria. Pyru-

vate is directly transported across the inner membrane or

generated in the matrix from malate by the action of malic

enzyme (ME). It is then oxidised by the pyruvate dehydroge-

nase complex (PDC) to form acetyl-CoA. PDC comprises three

enzymes E1 (2-oxo acid dehydrogenase), E2 (acyltransferase)

and E3 (lipoamide dehydrogenase) (Guan et al. 1995; Luethy

et al. 1995). This complex is regulated by phosphorylation of

E1, lowering PDC function in the day and increasing PDC

function at night (Thelen et al. 2000). Citrate synthase (CS)

catalyses the condensation of acetyl CoA with the dicarboxylate

oxaloacetate, yielding citrate and releasing the CoA cofactor

(La Cognata et al. 1996). Over-expression of citrate syn-

thase in Arabidopsis enhances growth under low phosphorous

conditions due to enhanced citrate excretion from the roots

to increase inorganic phosphate availability (Koyama et al.

2000). Citrate is converted to isocitrate via aconitase (ACO),

and isocitrate dehydrogenase (IDH) oxidises isocitrate to form

2-oxoglutarate. 2-oxoglutarate dehydrogenase, succinyl CoA

ligase, succinate dehydrogenase (complex II see below), fu-

marase and malate dehydrogenase compete the cycle by

reforming oxaloacetate. Recent studies of TCA cycle mutants

have shown the wide impact these enzymes have not only in

TCA cycle function but as steps for the anaplerotic delivery

of organic acids for other processes in plant cells such as

Plant Mitochondrial Composition and Stress Responses 889

photosynthetic performance, plant biomass, photorespiration,

nitrogen assimilation and amino acid metabolism, and even

stomatal function. Antisense mutants of malate dehydroge-

nase (MDH) and aconitase in tomato exhibit faster rates of

photosynthetic CO2 assimilation rates and higher ascorbate

levels (Nunes-Nesi et al. 2005). Antisense of fumarase leads

to substantial inhibition of photosynthetic performance and

stomatal function (Nunes-Nesi et al. 2007). Knockdown of

succinate dehydrogenase can alter stomatal aperture, change

nitrogen use efficiency and alter disease signalling (Araujo

et al. 2011; Fuentes et al. 2011; Gleason et al. 2011).

Oxidative phosphorylation (OXPHOS) apparatus

The so-called classical ETC is comprised of four large protein

complexes (I, II, III, IV) that interact with each other via the

Figure 1. Composition and assembly of OX PHOS protein complexes in plant mitochondria.

Numerous investigations have given insights into the composition and assembly of the large, multi-subunit complexes that constitute the

classical electron transport chain (ETC). This figure presents current knowledge of how ETC complex assembly is sequentially organized

through intermediate subcomplexes, and the assembly factors that mediate these processes.

small lipid ubiquinone (UQ) and the small protein cytochrome

c. Electron flow from NADH to oxygen is coupled to proton

translocation out of the matrix, to drive phosphorylation of ADP

to form ATP by the F1FO ATP synthase (Complex V).

Complex I (CI) – NADH-UQ oxidoreductase, catalyses the

oxidation of matrix NADH to reduce ubiquinone (UQ) in the

inner mitochondrial membrane. In plants, 49 subunits can be re-

solved from CI by electrophoretic separations (Heazlewood et

al. 2003a; Klodmann et al. 2010) (Figure 1). Direct comparisons

of CI subunit composition across taxa have revealed diver-

gences between plant CI versus mammalian CI, with eight nu-

clear encoded plant CI subunits being plant-specific, and sev-

eral others being common between plants and non-mammalian

eukaryotes but absent in mammals (Meyer et al. 2008;

Klodmann et al. 2010; Cardol 2011). Studies of mutations of


CI subunits have shown that plants can survive without CI due

to the activity of alternative NAD(P)H dehydrogenases (see

below). Such mutants have a variety of interesting phenotypes

including viral infection tolerance, prolonged hydration under

water-deficient conditions and altered organic and amino acid

concentrations (Dutilleul et al. 2003; Meyer et al. 2009). In

Neurospora crassa, CI assembly analysis using radio-labelled

pulse chase in mutants has revealed that the matrix and mem-

brane arms assemble independently via separate pathways

(Tuschen et al. 1990; Kuffner et al. 1998; Schulte 2001; Videira

and Duarte 2002; Mimaki et al. 2012). By using a combination

of radio-labelled pulse-chase experiments, in vitro mitochon-

drial import and monitoring of tagged CI subunits, several CI

assembly models have also been proposed in human cells

in assembly disturbed systems (Ugalde et al. 2004; Lazarou

et al. 2007; Vogel et al. 2007; Mimaki et al. 2012). In plants,

controlled dissociation of CI using low concentrations of SDS

followed by BN-PAGE and peptide mass spectrometry enabled

the visualisation and compositional analysis of 10 subcom-

plexes between 550 – 85 kDa in size, giving detailed insights

into the internal architecture of CI (Klodmann et al. 2010)

(Figure 1). Using Arabidopsis CI subunit knockout mutants, 200,

400, 450 and 650 kDa membrane arm subcomplexes have

been identified using BN-PAGE and antibodies. It is proposed

that these subcomplexes are assembly intermediates during CI

formation, which accumulate when specific subunits are absent

(Meyer et al. 2011). The first two assembly factors known for

CI, CIA40 and CIA84, were discovered in N. crassa (Kuffner

et al. 1998). Nine assembly factors including NDUFAF2/B17.2,

NDUFAF1/CIA30, C20orf7, C80orf38, NDUFAF4, NDUFAF3,

NUBPL, FOXRED1 and ACAD9 have been found in humans

and deficiency can impair CI assembly and lead to clinical phe-

notypes in patients (Nouws et al. 2012). Little is known about

assembly factors in plants, with only L-galactono-1,4-lactone

dehydrogenase (GLDH) described as a potential assembly

factor in Arabidopsis (Pineau et al. 2008) (Figure 1). Given the

conserved core subunits but divergence of accessory subunits

amongst eukaryotes, it is not yet clear whether the accessory

subunits play different roles in complex I assembly and thus

whether or not the assembly of CI follows the same pathway in

different organisms.

Complex II (CII) – Succinate dehydrogenase, is an enzyme of

both the TCAC and the respiratory ETC. In all organisms, it is

made from four core subunits: a flavoprotein (SDHI), an iron-

sulphur subunit (SDH2) and two membrane anchor subunits

(SDH3 and SDH4). Purification of the complex using BN-PAGE

has revealed the common core subunits, but also four proteins

of unknown function that co-migrate with the complex (Eubel

et al. 2003; Millar et al. 2004a) (Figure 1). In Arabidopsis, all

SDH subunits are encoded in the nuclear genome. Knockout

mutants of the SDH1 gene are embryo lethal (Leon et al. 2007),

but knockdown of SDH1 and SDH2 lead to phenotypes as-

sociated with altered stomatal aperture, altered mitochondrial

ROS production and altered nitrogen use efficiency (Fuentes

et al. 2011; Gleason et al. 2011). Several proteins assisting

CII assembly have been described in yeast and mammalian

cells, but only SDHAF1 and SDHAF2 are considered to be real

assembly factors that directly and specifically aid CII assembly

(Ghezzi et al. 2009; Hao et al. 2009; Rutter et al. 2010). In

Arabidopsis, knockdown of the SDHAF2 homolog lowers SDH

assembly and markedly reduces root growth (Huang et al.

2012) (Figure 1).

Complex III (CIII) – Ubiquinone-cytochrome c oxidoreductase,

contains 10 subunits including the bifunctional core proteins

that act both in CIII function and as the matrix processing

peptidase, removing presequences from imported matrix pro-

teins (Figure 1). Only one subunit of this complex, cytochrome

b, is encoded by the plant mitochondrial genome (Unseld

et al. 1997), with the remaining nine all encoded by the

nuclear genome. In BN-PAGE separations from Arabidopsismitochondria, all of these subunits have been identified and

linked back to a set of mostly single copy genes (Werhahn and

Braun 2002; Meyer et al. 2008). Yeast provides an ideal model

system to study CIII, due to its ability to survive by fermentation

in the absence of the complex, making gene knock-out and

mutagenesis possible (Smith et al. 2012). CIII assembly follows

a modular assembly model including, early core subcomplex,

late core subcomplex and a dimeric CIII states (Smith et al.

2012). There have been 13 assembly factors implicated in

aiding the different stages of CIII assembly in yeast. Two of

these, BCS1L and TTC19, were also found to have functional

homologs in mammalian CIII assembly (Diaz et al. 2011; Smith

et al. 2012). Little is known about CIII assembly or functional

assembly factors in plants.

Complex IV (CIV) – Cytochrome c oxidase, is the terminal

oxidase of the classical ETC. Purification of CIV in plants

originally found only seven or eight subunits (Peiffer et al.

1990), but more recently, a CIV complex containing 14 protein

bands was separated from Arabidopsis (Millar et al. 2004a)

(Figure 1). Eight proteins homologous to known CIV subunits

from other organisms, together with a further six proteins that

may represent plant specific CIV subunits, were identified.

Analysis of human CIV via BN-PAGE separation has revealed

an assembly pathway characterized by the sequential incorpo-

ration of CIV subunits, initiated by subunit 1 and subsequently

progressing through several discrete assembly intermediates

(Barrientos et al. 2009). Studies in yeast have revealed over

40 assembly factors that aid different stages of CIV assembly,

but only a few homologs for these factors have been defined

in humans (Barrientos et al. 2009; Diaz et al. 2011). A plant

homolog of yeast assembly factor COX19 has been studied and


found capable of complementing the yeast cox19 null mutant

and might play a role in the biogenesis of plant cytochrome coxidase to replace damaged forms of the enzyme (Attallah et al.

2007) (Figure 1). However, it seems evident that our knowledge

about the assembly of CIV in plants is still incomplete.

Complex V (CV) – ATP synthase is a membrane-bound F1F0

type H+-ATP synthase that catalyses the terminal step in

oxidative phosphorylation through which ATP is produced. It

is composed of a hydrophilic F1 component which catalyses

ATP formation and protrudes into the matrix and a hydrophobic

F0 component which channels protons through the membrane

while also anchoring the whole complex to the mitochondrial

inner membrane (Senior 1990; Hamasur and Glaser 1992;

Velours and Arselin 2000; Heazlewood et al. 2003b). The

general structure and the core subunits of the enzyme are

highly conserved in both prokaryotic and eukaryotic organisms

(Millar et al. 2011). In plant, most of mitochondrial F1 ATP

synthase subunits are encoded in the nucleus and translated

in the cytosol before being imported into the mitochondria (β,

γ, δ and ε), while most of the F0 subunits are encoded in the

plant mitochondrial genome and translated in the mitochondrial

matrix (a, b, c and A6L) (Jansch et al. 1996; Heazlewood et

al. 2003c; Sabar et al. 2003; Sabar et al. 2005) (Figure 1).

In plants, the F1α subunit is encoded in the mitochondrial

genome in most species. Alterations of mitochondrial-encoded

subunits of the F1F0-ATP synthase are frequently associated

with cytoplasmic male sterility (CMS) in plants, presumably due

to the high ATP demand of floral tissues (Xu et al. 2008). While

knockouts of ATP synthase core subunits are lethal in plants, in-

ducible knockdown with a dexamethasone-inducible promoter

has enabled investigations into the tissue-specific phenotypes

incurred by slowing the rates of mitochondrial ADP:ATP cycling

across a range of developmental stages (Robison et al. 2009).

Induction of the knockdown during germination in the light leads

to seedling lethality. Other phenotypes include the stunting of

dark-grown (etiolated) seedlings, downward curling or wavy-

edged leaf margins of light-grown plants, and ball-shaped

unexpanded flowers (Robison et al. 2009), highlighting the high

energetic demand of key growth stages.

The subunits that form the F1 component are kept in tight

stoichiometry in prokaryotic and eukaryotic organisms through

regulation of the assembly process (Senior 1990; Hamasur

and Glaser 1992; Velours and Arselin 2000; Li et al. 2012).

Models of yeast mitochondrial F1F0 ATP synthase assembly

involve two separate but coordinately regulated pathways,

where two separate subcomplexes are assembled in parallel,

before converging to form functional F1F0 (Rak and Tzagoloff

2009; Rak et al. 2011). Recent research in Arabidopsis using

progressive 15N labeling has measured differential rates of

turnover between different subpopulations of the F1 subcom-

plex. Intriguingly, the same subunits of F1 can exhibit faster or

slower turnover rates depending upon the intra-mitochondrial

localization they are found in, or upon the quaternary structure

of the F1 subcomplex that they constitute. For instance, sub-

units of F1 that were detected within the matrix-localized and

membrane-associated F1 subcomplexes both exhibited faster

turnover rates compared to those same subunits detected

within the intact, membrane-spanning F1F0 complex (Li et al.

2012). The proposed assembly model for plant CV comprises

three steps, the first being the formation of a rapidly turned over

F1 subcomplex in the matrix, then an intermediate stage where

F1 associates with the inner membrane and still turns over at a

fast rate, and then a final unison of F1 with FO to form functional

CV (Li et al. 2012) (Figure 1). This model of CV assembly

was corroborated by in vitro import assays where radiolabelled

CV subunits were incubated with isolated mitochondria, and

assembly intermediates visualised by scintillation counting of

BN-PAGE separations (Li et al. 2012). ATP synthase assembly

factors including Atp10, Atp11, Atp12, Atp22, Atp23 and Fmc1

have been discovered in yeast (Pickova et al. 2005; Osman

et al. 2007). Atp11, Atp12 and Fmc1 mediate the formation of

the F1 subcomplex while Atp10, Atp22 and Atp23 are essential

for the formation of F0 (Pickova et al. 2005; Osman et al. 2007).

Hsp60 and Hsp70 also contribute to efficient CV assembly

(Osman et al. 2007). A phylogenetic analysis of ATP synthase

assembly factors has found Atp11 and Atp12 are preserved

in almost all eukaryotic organisms, including plants, while the

other assembly factors show evidence of divergent evolution

across taxa (Pickova et al. 2005) (Figure 1). However, a detailed

study of the presence and conservation of CV assembly factors

across sequenced plant genomes has not been undertaken to

our knowledge.

Alternative electron transport pathways

In addition to the classical OXPHOS machinery, plant mito-

chondria contain non-phosphorylating respiratory bypasses of

electron transport and of proton-coupled ATP synthesis. These

pathways were first identified by the ability of plant mitochondria

to respire in the presence of cyanide and rotenone, potent

inhibitors of CIV and CI, respectively, and to exhibit natively

uncoupled respiration in the absence of an ADP source.

Alternative oxidase (AOX) – The cyanide-insensitive respi-

ration is catalysed by the alternative oxidase (AOX), a diiron

quinol oxidase that branches from the respiratory chain at UQ

and reduces oxygen to water without proton translocation. AOX

appears to play an antioxidant role in plant mitochondria, is

actively induced by oxidative stress (Van Aken et al. 2009) and

the different genes for the oxidase have been shown to be both

tissue- and development-specific in their expression patterns

(Saisho et al. 2001; Thirkettle-Watts et al. 2003). Knockout of

AOX leads to anthocyanin and ROS accumulation in the leaves


under the combination of high light and drought stress (Giraud

et al. 2008).

Alternative NADH dehydrogenases – These type II NAD(P)H

dehydrogenases are found on both sides of the inner mi-

tochondrial membrane. External or cytosolic NADH and

NADPH can be oxidised via these dehydrogenases which

are insensitive to the CI inhibitor rotenone. These path-

ways operate without the translocation of protons (Finnegan

et al. 2004; Rasmusson et al. 2004). The Arabidopsisgenome contains seven genes encoding these Type II

NAD(P)H dehydrogenases (Michalecka et al. 2003; Moore

et al. 2003), falling into three subgroups: Atnda (1 and 2), Atndb

(1 – 4) and Atndc1. A further complication in Arabidopsis is the

dual localisation of several of the alternative dehydrogenases

in subcellular compartments other than mitochondria (Carrie

et al. 2008).

Uncoupling proteins (UCPs) – UCPs are members of

the mitochondrial carrier family of proteins and have been

the focus of considerable study as pathways for non-

phosphorylating/uncoupled respiration by virtue of their ability

to transport H+ back across the inner membrane, dissipat-

ing the electrical potential built by the ETC. UCPs can be

activated by reactive oxygen species (ROS) and this effect

may indicate an important biochemical control mechanism

for the engagement of this pathway in vivo (Considine et al.

2003). Analysis of knockouts of UCP (AtUCP1) showed that its

absence led to localized oxidative stress but did not impair the

ability of the plant to withstand a wide range of abiotic stresses.

However, knockout of UCP1 limited the photorespiration rate

of plants and reduced the photosynthetic carbon assimilation

rate (Sweetlove et al. 2006). This suggests that the main

role of UCP1 in leaves is to maintain the redox poise of

the mitochondrial ETC to facilitate photosynthesis (Sweetlove

et al. 2006).

Plant Mitochondrial CompositionVariation in Different Tissues

In response to alterations in cellular metabolic and energy

demands, mitochondria often undergo changes in their mor-

phology and respiratory capacity by regulating the composition

and abundance of the protein machinery that has been outlined

above. In this way, mitochondria are dynamically tuned to meet

the specific need for energy in different tissue types or in re-

sponse to the environment. These differences, or heterogeneity

of mitochondria, have been observed through reports of tissue

selective phenotypes of mutants, through evidence of tran-

scriptional programming of mitochondrial functions and through

examples of steady-state differences in organelle composition

and post-translational differentiation of mitochondrial function

in different tissues.

Mutations of nuclear genes encoding mitochondrial proteins

have been reported to yield organ-specific plant phenotypes

in a number of recent reverse-genetics studies. These include

delayed development and flowering by loss of PPR proteins

(de Longevialle et al. 2007; Sosso et al. 2012), altered leaf

morphology and/or photosynthetic capacity by loss of CI, CII

or mitochondrial malate dehydrogenase (Meyer et al. 2009;

Tomaz et al. 2010; Fuentes et al. 2011), and alteration in

root morphology and respiratory rate and inhibition of stomatal

function by loss of fumarase (Nunes-Nesi et al. 2007; van

der Merwe et al. 2009). These observed phenotypes could be

explained by: (i) the inability of mitochondria to meet energy

demands in a particular tissue, and/or (ii) the incompatibility

of a mutation in the mitochondrial proteome that requires the

expression of particular isoforms of proteins, the assembly

of particular complexes, and/or the stoichiometry of different

components in pathways for tissue-specific functions.

A number of nuclear-encoded mitochondrial respiratory com-

ponents have been shown to be co-regulated in various veg-

etative and reproductive organs at the transcriptional level

(Gonzalez et al. 2007; Lee et al. 2011). Promoter analyses

of the co-regulated components have uncovered common site

II motifs in the proximal promoter of these genes that may

direct organ-specific, metabolic, environmental and develop-

mental responses (Welchen and Gonzalez 2005; Gonzalez et

al. 2007). Analysis of broader functional categories of genes

has revealed that components of CI and CV are constitu-

tively expressed, whereas genes encoding for mitochondrial

photorespiratory machinery and heat shock proteins are ex-

pressed selectively across the plant tissues examined (Lee

et al. 2011). While there are a number of examples where

there is a strong correlation between transcript abundance

and protein abundance/activity across the tissues examined,

there are many cases that show otherwise, notably for NAD-

malic enzyme, aldehyde dehydrogenase and thioredoxin re-

ductase (Lee et al. 2012). Therefore, caution has to be taken

when interpreting tissue-specific differences in the activity

of enzymatic steps based on differences in transcript data

alone.

To analyze the specialized role of mitochondria during plant

development, extensive mitochondrial proteomic comparisons

of vegetative (cell culture, root and shoot) and reproductive

(silique, stem and flower) phases of development have been

recently reported in Arabidopsis (Lee et al. 2012). Using dif-

ferential 2-D gel electrophoresis, a total of 83 non-redundant

proteins consisting of components of the TCA cycle and pho-

torespiration as well as enzymes that depend on the supply of

intermediates from these metabolic pathways were identified.

While the abundance of individual subunits in the ETC gen-

erally remains unchanged across the vegetative tissue types


compared, the respiratory capacity alters depending on the

substrate choice and/or availability of the substrate in that

particular tissue/cell type (Lee et al. 2008; Lee et al. 2011).

Determining differences in the abundance of a protein can

allow prediction of the degree of variation in metabolic flux

between different organ/cell types (Johnson et al. 2007). By

mapping these changes on a predesigned scheme of mito-

chondrial metabolism, the specific enzymatic steps which are

regulated due to tissue specialization can be pinpointed (Figure

2). Functional analysis of the vegetative organs/cell reveals

specific differences in the central carbon metabolism e.g. shoot

mitochondria has a specialized role in glycine cleavage via

photorespiration, cell culture mitochondria mainly utilize citrate

from the TCA cycle and peroxisomal β-oxidation to drive the

decarboxylating reactions of the TCA cycle and fuel ATP

formation, while root mitochondria have a higher capacity for

converting 2-oxoglutarate into fumarate for energy production

via CII (Figure 2). Mitochondria from organs in the reproductive

phase tend to have a specialized role in metabolism other than

the TCA cycle, such as the maintenance of mitochondrial redox

Figure 2. Heterogeneity of mitochondrial protein composition in key areas of metabolism.

Mitochondrial metabolism is tuned to perform specialized roles across a range of plant tissues by modulations to protein abundance and

enzyme activity. GDC, Glycine decarboxylase; SHMT, Serine hydroxymethyltransferase; Trx, Thioredoxin; NTR, NADPH thioredoxin reduc-

tase; ARG1, Arginase 1; ARG2, Arginase 2; AlaAT, Alanine aminotransferase; PDC, Pyruvate dehydrogenase; CS, Citrate synthase; ACON,

Aconitase; IDH, Isocitrate dehydrogenase; GDH, Glutamate dehydrogenase; AspAT, Aspartate aminotransferase; OGDC, 2-Oxoglutarate

dehydrogenase; S-CoA, Succinyl-CoA synthetase; SDH, Succinate dehydrogenase; Fum, Fumarase; MDH, Malate dehydrogenase.

environment in flowers, and nitrogen (glutamate) metabolism in

stems. These mitochondrial specializations generally coincide

with the main physiological role of each corresponding tissue

type. For example, the up-regulation of malate dehydrogenase

in the shoot provides evidence for its role in regulating the

redox poise which is crucial for mediating photosynthesis and

respiration in the light (Hanning and Heldt 1993; Raghavendra

and Padmasree 2003; Tomaz et al. 2010).

Most mitochondrial proteomic studies have focus on the

functional impact of tissue-specific nuclear-regulated transcrip-

tional and post-transcriptional events by comparing the to-

tal abundance of a particular protein on the gel. While the

abundance of a protein sometimes correlates with its maximal

catalytic activity, this approximation cannot be applied to all

enzymes, due to differential abundance of isoforms of certain

mitochondrial proteins across tissues, as these differences

in primary amino acid sequence could manifest in altered

kinetics (Lee et al. 2008; Lee et al. 2011; Lee et al. 2012). For

example, isoform 1 (AT4G08900) of arginase appears to be

more highly expressed in vegetative tissue, whereas isoform 2


(AT4G08870) is more abundant in reproductive organs (Lee

et al. 2012). Isoform-specific differences in vegetative and

reproductive development have also been observed when

each of the four voltage-dependent anion channels (VDAC)

isoforms were disrupted (Tateda et al. 2011). Post-translational

events also play a pivotal role in regulating enzyme activity

and thus the flux of a metabolic pathway through modifications

of proteins and the assembly of enzyme complexes. Some

of the protein modifications observed on 2-D gels, especially

truncated products and pI-shifted proteins, have often been

perceived as artefacts introduced during sample preparation.

However, in a recent survey of the mitochondrial proteome

from different organ/cell types (Lee et al. 2012), many proteins

in the TCA cycle, ETC and photorespiration undergo post-

translational modifications in a tissue specific fashion that are

highly reproducible across biological replicates, suggesting that

these changes are not random. The functional implications of

specialized differences in post-translational modifications on

the contribution of mitochondrial metabolism in different tissues

remains to be explored.

Plant Mitochondrial Oxidative Stress andCellular Signalling

Environmental, biotic, abiotic and chemical stresses applied

to plants are well known to induce oxidative stress in plant

cells. These stresses alter plant metabolism, growth and de-

velopment and, at their extremes, can lead to death. Recently,

a number of studies have begun to examine the changes

that occur within plant mitochondria following the induction of

oxidative stress. The accumulation of ROS, ROS induced lipid

peroxidation, changes in metal content, changes in protein

abundance and their interactions in mitochondria following

exposure to external stress, and the role of these changes

in signaling beyond mitochondria, combine to define the impor-

tance of mitochondria as environmental sensors.

Accumulation of ROS in mitochondria

Mitochondria contain two terminal oxidases that reduce oxygen

to water and the entire ETC is known to be a significant source

of ROS under normal conditions. However, under steady state

conditions, this ROS production is dealt with by antioxidant

enzymes and small molecules to limit cellular damage. How-

ever, under some conditions, these defenses are overwhelmed

and ROS accumulate (Figure 3). Superoxide is produced

in mitochondria by peripheral single electron transfers from

reduced components in the ETC to oxygen (Moller 2001).

Classically, the ubiquinone pool and components in CI and

CIII have been implicated, however recently CII has also been

shown to produce significant superoxide (Quinlan et al. 2012).

Measurements suggest that 2–5% of oxygen consumption by

mitochondria is due to single electron superoxide formation,

while the majority of oxygen consumption occurs at the terminal

oxidases by four electron reduction of oxygen to water. The

rate of superoxide production by mitochondria depends on

the concentration of oxygen and on the redox poise of ETC

components. Therefore, ROS production by mitochondria is

low during hypoxic conditions (Noctor et al. 2007), is elevated

when respiration inhibitors block the ETC and cause over-

reduction of earlier ETC components (Maxwell et al. 1999),

and can be altered by environmental factors and chemicals

that alter the rate of these peripheral electron transfer reactions

(Moller 2001; Moller et al. 2007; Noctor et al. 2007). Notably,

nitric oxide is a potent inhibitor of the mitochondrial ETC

and its generation during plant stress may be critical in the

elevation of ROS production from mitochondria in plants (Millar

and Day 1996; Yamasaki et al. 2001; Zottini et al. 2002).

ROS have been shown to have a direct inhibitory effect on

a number of mitochondrial enzymes including components of

the ETC. Most notably H2O2 can inhibit the TCA cycle enzyme

aconitase by modification of its 4Fe-4S cluster (Verniquet et al.

1991).

ROS induced lipid peroxidation in mitochondria

Lipid peroxidation in a mitochondrial context refers to free

radical autoxidation of polyunsaturated fatty acids of membrane

lipids such as linoleic acid, linolenic acid, arachidonic acid

and hexadecatrienoic acid to yield various cytotoxic aldehydes,

alkenals and hydroxyalkenals. The interaction of the hydroxyl

radicle (OH �) with polyunsaturated fatty acids initiates lipid

peroxidation that by a sequential series of reactions leads to

a number of toxic lipid peroxidation end products (LPEP) by

a non-enzymatic, metal ion enhanced process (Noordermeer

et al. 2000) (Figure 3). Probably the most cytotoxic and studied

LPEP is 4-hydroxy-2-nonenal (HNE). HNE is potentially able

to undergo a number of reactions with proteins, phospho-

lipids and nucleic acids. It has been shown to accumulate in

plants during the oxidative burst (Deighton et al. 1999), biotic

stresses (Montillet et al. 2002) and during exposure to chemical

stresses (Winger et al. 2005). HNE has been shown to inhibit

the activities of mitochondrial pyruvate dehydrogenase, 2-

oxoglutarate dehydrogenase and glycine decarboxylase via the

modification of the lipoic acid residues found on the E2 subunits

of these enzymes (Taylor et al. 2002). This modification by

HNE results in the formation of HNE-Michael adducts, which

no longer allow the normal function of the essential E2 catalytic

subunit. Further research has also identified a wider range

of proteins that are damaged or inhibited by HNE. In some

cases lipoic acid moieties are not involved and HNE acts

directly by covalent modification of amino acid residues such

as Cys, Lys, His, Ser and Tyr (Esterbauer et al. 1991). The


Figure 3. Proposed scheme of the interaction of ROS, proteins, metals and lipid peroxidation end products in plant mitochondria

exposed to stresses.

When a plant is exposed to environmental stress this must be sensed either by a receptor on the cell wall/plasma membrane or directly

inside the cell. This is then likely signalled to the nucleus and the mitochondria. Inside the organelles an accumulation of ROS can occur

when antioxidants and antioxidant proteins (AP) are overwhelmed and this leads to the production of lipid peroxidation end products (LPEP),

damaged proteins (DP), unfolded proteins (UP) and release of transition metals (TM). The accumulated ROS can directly inhibit proteins,

while accumulated LPEP can modify proteins with lipoic acid cofactors (ML) directly amino acid (ML). Accumulated transition metals can

facilitate metal catalyzed oxidation leading to the formation or carbonyl groups (CB). The organelles may also signal the accumulation of ROS

to the nucleus. Either the external sensing of stress or organellar signalling of ROS leads to the production of new proteins by the nucleus,

including replacement proteins sHSPs, proteases and antioxidant proteins (AP). These are then involved in the refolding of unfolded proteins

(UP) or the degradation of damaged proteins (DP). AP, Antioxidant proteins; CB, Carbonyl modified amino acids; DP, Damaged proteins;

LPEP, Lipid peroxidation end-products; MA, Michael adducts formation on amino acids by LPEP; ML, Michael adducts formation on lipoic

acid by LPEP; sHSP, Small heat shock proteins; TM, Transition metals; UP, Unfolded proteins.

alternative oxidase (AOX) and NAD-malic enzyme are inhibited

by HNE (Winger et al. 2005), and it has been proposed in both

enzymes that modification of a critical cysteine residue near

the active site might be responsible (Millar and Leaver 2000;

Winger et al. 2005). The likely pathways for the detoxification

of lipid peroxidation end-products such as HNE are yet to

be elucidated in plants, but it is likely to involve glutathione-

s-transferase (GST) conjugation of modified peptides and

may also involve aldehyde dehydrogenases and/or aldose

reductases.


Metallome changes during oxidative stress

Plant mitochondria contain the transition metals Fe, Cu, Zn and

Mn as well as trace levels of Co and Mo (Tan et al. 2010). The

redox cycling metals Cu and Fe tend to be concentrated to

the integral membrane proteome likely due to the abundance

of Cu- and Fe-containing ETC components and account for

approximately 75% of the mitochondrial metallome (Tan et al.

2010). Treatment of cultured cells with chemicals known to

induce oxidative stress induce a reduction of peripheral mem-

brane Fe and integral membrane Cu content, suggesting dam-

age to membrane-associated ferro-proteins and membrane-

embedded cupro-proteins (Tan et al. 2010). Significant losses

have also been seen for soluble fraction Fe, Cu and Mn

suggesting damage to metallo-matrix proteins and release of

Fe, Cu and Mn. These labile transition metals, in particular

redox active copper and iron ions, typically react with hydrogen

peroxide in Fenton type reactions to catalyze the formation

of OH �. In addition, other redox-cycling reactions within the

mitochondria exist and they are capable of eliciting metal-

catalyzed oxidation (MCO) (Figure 3). Metal-catalyzed oxidation

of proteins results in the oxidation of susceptible amino acids

such as arginine, lysine, proline and histidine (Stadtman 1993),

among a plethora of other poorly characterized consequences.

One of the major by-products of MCO of proteins is the

irreversible formation of carbonyl derivatives. These carbonyls

are highly reactive and may cause protein aggregation if the

damaged proteins are not degraded. These reactive carbonyls

are often studied as markers of oxidative stress in both plants

and animals. However, the impacts of protein carbonylation in

plants at a subcellular level remains poorly understood.

Proteome changes during oxidative stress

A number of studies have revealed global changes in protein

abundance of mitochondrial proteins following conditions that

induce oxidative stress in a wide range of plant species (Sweet-

love et al. 2002; Taylor et al. 2005; Chen et al. 2009; Taylor

et al. 2009; Jacoby et al. 2010; Huang et al. 2011; Komatsu

et al. 2011; Hossain et al. 2012; Tan et al. 2012). Recently it has

also been shown that the large respiratory subunits of the ETC

also coordinate protein changes to alter respiration in response

to oxidative stress conditions (Tan et al. 2012). In addition to

these changes are changes in proteins responding to ROS

and the damage they cause. For example the mitochondrion

is protected by a number of antioxidant enzymes that detoxify

ROS and many have been observed to vary in abundance dur-

ing oxidative stress including: Mn-superoxide dismutase (Jiang

et al. 2007), ascorbate peroxidase (Dooki et al. 2006) mon-

odehydroascorbate reductase (Sarry et al. 2006), glutathione

peroxidase (Jiang et al. 2007) and peroxiredoxins (Sweetlove

et al. 2002; Sarry et al. 2006). The importance of these organel-

lar antioxidant defense mechanisms in plant stress tolerance

has been highlighted by transgenic manipulation of the expres-

sion of these antioxidant enzymes (Allen et al. 1997). Changes

in abundance of GST proteins are detected in almost every

stress proteome study, sometimes accompanied by aldehyde

dehydrogenases (Cui et al. 2005; Ndimba et al. 2005; Sarry

et al. 2006), both of which may be involved in the detoxification

of lipid-peroxidation end-products. Many metalloproteins have

been shown to change in abundance following exposure to

stress including Mn-SOD (Jiang et al. 2007), the Fe-S center

containing CIII UCR1 (Tan et al. 2012), CI 75 kDa subunit

(Taylor et al. 2005) and the copper interacting CI subunit B16

(Tan et al. 2012). In addition to these direct protein changes,

other proteins have been observed to increase in abundance

including mitochondrial class I and mitochondrial class II small

heat shock proteins (sHsps) (Siddique et al. 2008) (Figure 3).

It is generally accepted that sHsps alleviate the deleterious

effects of stresses by preventing protein denaturation and

aggregation, as well as facilitating the correct refolding of

denatured proteins. Similarly increases in constitutive ser-

ine protease activity can be induced by oxidative stress in

mitochondria (Sweetlove et al. 2002) although the specific

Clp and FtsH serine proteases responsible for this remain

unresolved. Mitochondria also contain Lon metalloproteases

(Sarria et al. 1998; Rigas et al. 2009) and together with

the serine proteases it seems likely that these proteins are

responsible for the degradation of oxidatively damaged proteins

(Figure 3).

Regulation of downstream gene expression such asGSTs and HSPs

Due to the complexity of the interconnected ROS signalling

network that operates within plant cells (Mittler et al. 2004), it is

difficult to attribute specific cellular responses to mtROS signals

alone (Møller and Sweetlove 2011). However, by analysing the

gene expression patterns elicited by respiratory inhibitors and

the transcriptional anomalies exhibited by plants carrying muta-

tions to mitochondrial genes, it appears that the expression pat-

terns of certain gene clusters could be key indicators of mtROS

signals. Here we briefly outline how the molecular signatures

generated by mtROS signals could potentially be deduced

by analysing transcriptional upregulation within subsets of the

glutathione-s-transferases (GSTs) and heat shock proteins

(HSPs). In maize, expression patterns of gstIII and gstI genes

were similar between NCS4 (mitochondrial ribosome mutant

affecting translation) and NCS6 (CIV mutant) compared to their

respective wild type (Karpova et al. 2002). However, both gstIIIand gstI were increased in the NCS2 (CI mutant) (Karpova et al.

2002). Therefore, dysfunction of CI (NCS2), but not dysfunction

of either CIV (NCS6) or mitochondrial translation (NCS4),

induces these GSTs. Interestingly, treatment with exogenous


H2O2 can also induce expression of gstIII and gstI genes in

maize leaves (Karpova et al. 2002), perhaps suggesting that

the NCS2 mutation (CI) exerts its signaling effect via H2O2

signals derived from mitochondrion, whereas the NCS4 (ribo-

some) and NCS6 (CIV) mutations communicate mitochondrial

dysfunction via a different route. These mechanisms of ROS

signaling could be conserved between species, as mutations to

CI in Arabidopsis induce accumulation of ROS (Lee et al. 2002;

Meyer et al. 2009), and higher expression levels of GSTF3

and GSTF6 transcripts (Meyer et al. 2009). The activity of the

Arabidopsis GSTF8 promoter has been defined as a marker for

defense response during the early stages of stress exposure

(Sappl et al. 2009), and recently, a forward genetics approach

that employed GSTF8 promoter activity to define mutants with

altered stress responses identified a novel CII mutant, dsr1(Gleason et al. 2011). Analysis of GSTF8 promoter activity

upon application of exogenous chemicals revealed that the

dsr1 mutant could not mediate GSTF8 promoter activity in

response to salicylic acid (SA), despite this treatment eliciting

strong GSTF8 promoter activity in a wild type background.

However, external supply of H2O2 recovered the induction

of GSTF8 promoter activity in dsr1. These results suggest

a stress signaling model whereby upstream SA signals are

converted into mtROS signals via H2O2 production at CII. This

signal is then transmitted to the nucleus to elicit downstream

responses such as induction of a certain subset of GST

transcripts.

Numerous studies have measured increased expression of

genes encoding heat shock proteins upon disruption of the ETC

via genetic mutation or treatment with respiratory inhibitors. For

example, higher abundance of HSP transcripts was observed

in Arabidopsis CI mutant lines (Meyer et al. 2009), in cultured

Arabidopsis cells treated with CI inhibitors (Garmier et al. 2008),

and in maize NCS mutants including NCS2 (CI), NCS4 (riboso-

mal translation) and NCS6 (CIV) (Kuzmin et al. 2004). Further

dissection of the triggers that can elicit higher expression of

sHSP22A suggest that its promoter activation depends upon

a decrease in the potential difference across the mitochondrial

inner membrane, independent of Ca2+ signals (Kuzmin et al.

2004). A study in C. elegans suggests that the induction of

mitochondrial heat shock proteins is regulated by the prote-

olytic cleaving of specific mitochondrial proteins to generate

messenger peptides which are exported to the nucleus, with

the divergent amino acid sequences across a range of dif-

ferent messenger peptides providing the specificity required

to elicit the subsequent induction of a specific set of genes

(Haynes et al. 2010; Moller and Sweetlove 2011). This offers a

tempting explanation for the link between sHSP22A induction

and lower potential difference across the mitochondrial inner

membrane in maize (Kuzmin et al. 2004), as the depolarization

of mitochondrial membrane potential could permit the export of

signaling peptides. It can be posited that different mitochondrial

stress signals can activate divergent pathways of mitochondrial

retrograde signaling, as within the aforementioned suite of

maize mutants, there are significant overlaps amongst HSP

gene family expression but divergent transcriptional responses

within the set of GSTs, with higher expression of GSTI and

GSTIII only being elicited by CI mutation. Molecular models

of specific mitochondrial retrograde signaling pathways are

maturing and detailed analysis of expression patterns within

and between sets of stress responsive genes can further our

understanding of the molecular signaling processes communi-

cated by mtROS. This opportunity is particularly timely as well

characterised suites of ETC mutants are now available across

a range of species.

Plant Mitochondrial Roles in HarshEnvironments

Insights into how the respiratory roles of mitochondria in cells

operate under harsh environmental conditions encountered

by intact plants have been derived by analyzing phenotypes

across a wide range of physical scales (Figure 4). Ecosystem

studies have shown that plant respiration rates were a major

factor underpinning slower rates of forest and crop productivity

across Europe during a 2003 heatwave, with prolonged heat

and drought temporarily switching certain European forests

into sources of atmospheric carbon, rather than sinks (Ciais

et al. 2005). At an individual plant level, physiological studies

have defined that respiratory rates are a key determinant of

growth reductions under a range of stresses such as extreme

temperatures, drought and salinity (Atkin et al. 2005; Atkin

and Macherel 2009; Jacoby et al. 2011). The most powerful

theoretical framework analysing these responses is the process

of carbon balance, where growth rate is positioned as the

sum total of carbon captured via photosynthesis minus carbon

expended by respiration (McCree 1986; Amthor 2000). Tissue-

level experiments have shown that some stresses, such as

temperature, can induce rapid changes to respiratory rates

of excised tissue, probably mediated through thermal effects

on the kinetics of the ETC (Kurimoto et al. 2004; Armstrong

et al. 2006), whereas exposing excised tissue to external

NaCl has little impact on respiratory rates in the short term,

probably because salinity exerts its effects on respiration

rates through alterations to substrate provision and cellular

energetic demand (Flowers 1972). Oxygen uptake rates of

isolated mitochondria exposed to harsh conditions in vitro have

defined the routes of mitochondrial electron transport that can

withstand high concentrations of toxic substances such as

NaCl, lipid peroxidation products and cadmium (Miller et al.

1973; Hamilton and Heckathorn 2001; Winger et al. 2007),

while analyses of ETC biochemistry in mitochondria isolated

from plants exposed to harsh stresses have repeatedly shown


Figure 4. Plant mitochondrial roles in harsh environments.

The left of this figure presents a schematic outline of three major mitochondrial processes that mediate plant growth and survival during stress.

First is mitochondrial support for photosynthesis (green), second is the mitochondrial delivery of energy and intermediates (brown), and third

are mitochondrial contributions to root cell homeostasis and transport processes (yellow). The right of this figure shows that mitochondrial

processes such as respiration, metabolism and signaling can be analysed across a wide range of physical scales, demonstrating that

mitochondrial stress responses are relevant to a broad range of researchers.

that the alternative respiratory pathways display increased

activities in response to a wide range of stresses (McDonald

2008). In terms of individual enzymes, activity assays have

shown that certain components of key metabolic pathways

are sensitive to cellular products of stress, such as hydrogen

peroxide, metal cations and HNE (Verniquet et al. 1991; Millar

and Leaver 2000; Tan et al. 2010), so metabolic flexibility

must be required to reshuffle TCA cycle flux around these

blockages during environmental stress (Sweetlove et al. 2010).

Recently, these characterisations of mitochondrial function are

being complemented by high-throughput ‘omics studies that

define the specific mitochondrial transcripts and proteins which

underpin these tolerance strategies in commercially important

crop species to provide mechanistic targets in respiration

for crop improvement (Abe et al. 2002; Taylor et al. 2005;

Jacoby et al. 2010). These can be considered in three main

areas related to mitochondrial delivery of energy and inter-

mediates, mitochondrial support for photosynthesis, and mito-

chondrial contributions to root cell homeostasis and transport

processes.

Cell survival under stress fuelled by mitochondrialprovision of carbon skeletons, ATP and reducingequivalents

Experiments have described a number of cellular responses

that mediate tolerance mechanisms in stress treated plants,

such as altered rates of protein turnover, rebalancing of cellular

metabolite pools, altered abundance of ROS species and

changes in the redox ratios within pools of reducing equiva-

lents. Each of these phenomena can be linked to mitochondrial

processes through alterations to central metabolic pathways,

or by their demand for fast rates of ADP:ATP cycling medi-

ated by respiratory oxidative phosphorylation (Figure 4). For


instance, plants display differential rates of protein turnover

relative to unstressed controls in response to a wide range

of stresses such as drought, osmotic stress and heat stress

(Dungey and Davies 1982; Zagdanska 1995; Huang et al.

2012), and it has been well established that this protein quality

control network incurs a significant energetic cost, as ATP is

hydrolysed to fuel the refolding and degradation of damaged

proteins, and also the synthesis of new replacement proteins

(Moller et al. 2007). Although the plastidic ETC produces a

large amount of cellular ATP in illuminated leaves, this is all

consumed by the process of photosynthetic carbon reduction;

therefore, mitochondrial electron transport provides the ATP

during day and night in both roots and shoots for all other

cellular operations. As a consequence, robust mitochondrial

function in all tissues is crucial to plant survival under stress

conditions. Another molecular signature of harsh environmen-

tal conditions is the accumulation of high concentrations of

particular metabolites, such as proline, glycine betaine (GB)

and GABA (Hare et al. 1998). At a molecular level, these

molecules can stabilize proteins, scavenge ROS, and serve as

alternative energy sources when classical metabolic pathways

are substrate-limited or biochemically-inhibited (Arakawa and

Timasheff 1985; Verslues and Sharp 1999; Chen and Dickman

2005). The mitochondrial role in regulation of proline and GABA

concentrations comes through the abundance and activity of

catabolic proteins such as ProDH, P5CDH and GABA-T that

are located in the mitochondrial matrix (Miller et al. 2009;

Renault et al. 2010), while a mitochondrial role in regulating

cellular concentrations of GB comes through the provision of

photorespiratory serine by the reactions of GDC and SHMT

in mitochondria (Bhuiyan et al. 2007). Further links between

mitochondrial function and cellular metabolic status come

through the provision of 2-OG via the TCA cycle, as 2-OG

is a precursor for many N-containing metabolites in plant cells,

and exposure to abiotic stress can alter the rate of TCA cycle

flux (Baxter et al. 2007; Sweetlove et al. 2010). Increased

ROS abundance is a convergence point for a wide range of

stress treatments, and stress treated plants commonly exhibit

shifts in the redox poise of ascorbate and glutathione to more

oxidized states following stress treatments (Foyer and Noctor

2011). Mitochondrial regulation of these phenomena has been

illustrated by transgenic studies showing that manipulation of

mitochondrial enzymes can alter whole-plant redox balance

and stress tolerance (Dutilleul et al. 2003; Morgan et al. 2008;

Tomaz et al. 2010).

Mitochondria support for photosynthesis duringenvironmental challenge

Photosynthetic carbon capture is a coordinated process that

requires mutual cooperation between organelles, and mito-

chondrial functions are particularly important in sustaining

photosynthesis under high light. It is now widely accepted that

fast photosynthetic rates and the avoidance of photoinhibition

are dependent upon mitochondrial function being configured

to rapidly transfer electrons from NADH into water through the

non-phosphorylating bypasses of the classical ETC (Millar et al.

2011) (Figure 4). This framework is supported by several lines of

evidence, such as measurements showing that the abundance

and activity of this particular set of mitochondrial enzymes

are induced by high light (Noguchi and Yoshida 2008), while

toxic inhibition of the mitochondrial ETC leads to decreased

photosynthetic rates (Saradadevi and Raghavendra 1992),

and compellingly evidence from knockouts of genes encoding

mitochondrial proteins that result in lower photosynthetic rates

and acute sensitivity to high light coupled to drought (Sweetlove

et al. 2006; Giraud et al. 2008). Rates of plant growth are

largely determined by the balance between photosynthesis and

respiration, with more productive, fast-growing plants generally

allocating a smaller fraction of their daily fixed carbon to

respiratory CO2 production. This reserves a larger fraction of

fixed carbon to allocate into synthesising new tissue, which

is primarily constructed by the accumulation of carbohydrates

(Poorter et al. 1990; De Block and Van Lijsebettens 2011).

However, there appears to be a limit to the productivity

increases that can be acquired through slower respiratory

rates, with canola experiments showing that plants selected for

slightly slower respiration rates displaying increased biomass

production, but plants where respiration rates had fallen below

a certain threshold displayed dramatically slower growth rates

probably because cellular energy supply cannot match baseline

demand (Hauben et al. 2009). Although this study did not

investigate a stress condition, the results identify an important

limitation in strategies that aim to enhance biomass accumula-

tion through selecting for uniformly lower respiration rates, as

slow respiration would likely be a disadvantage during transient

stressful periods which require increased rates of mitochondrial

energy production to fuel energetically costly cellular defense

processes. Respiratory elasticity is likely to be the most useful

trait, enabling slow respiration rates to promote growth during

optimal conditions, but faster respiration rates to fuel defense

during transient stress periods.

Root-specific mitochondrial processes mediatingtolerance to unfavourable soil conditions

Oxidative phosphorylation in mitochondria is the main source

of ATP in root tissue, and mitochondrial processes are also

involved in the tolerance of plants to root-specific stresses, such

as low oxygen and toxic soil conditions (Figure 4). Root tissue

is prone to dramatic fluctuations in cellular oxygen concentra-

tions, owing to the low solubility of oxygen in water coupled

with hydrological flood-drain cycles imposed by variations in

rainfall or soil drainage, in both rainfed and irrigated agricultural


systems. Under low oxygen, mitochondrial metabolism shifts

away from the classical TCA cycle and ETC, towards other

mitochondrial processes such as amino acid metabolism (Millar

et al. 2004b; Taylor et al. 2010). Mitochondrial ROS defenses

such as MnSOD accumulate under anoxia, presumably in

anticipation of the forthcoming ROS burst that will occur upon

re-oxygenation (Millar et al. 2004b; Shingaki-Wells et al. 2011).

Large areas of the earth’s surface are covered by soils with

chemical properties that are sub-optimal for plant growth, due

to high concentrations of salts or heavy metals, insufficient

bioavailability of essential nutrients like iron, phosphate, sul-

phur and nitrogen, as well as unfavourably acidic or alkali

pH. The perception of heavy metal toxicity has been shown

to involve mitochondrial ROS signals (Garnier et al. 2006), and

the key role of mitochondrial ROS defenses within root cells has

been pinpointed by the dramatic root growth reductions elicited

by exposing mitochondrial peroxiredoxin mutants to high cad-

mium concentrations (Finkemeier et al. 2005). Exudation of

TCA cycle intermediates have been linked to iron absorption

from soils where neutral pHs render the iron insoluble, as these

acidic metabolites acidify the soil, thus solubilising sequestered

iron to increase bioavailability (Vigani 2012). Conversely, alu-

minium toxicity can be alleviated by exudation of citrate and

isocitrate, as these TCA cycle intermediates have chelating

properties that decrease bioavailability of the toxic Al3+ ion

(Ma et al. 2001; Fujii et al. 2012). Sodium exclusion is a

well defined mechanism of plant NaCl tolerance, and strong

links between the degree of sodium exclusion and the rate

of root respiration have been demonstrated by the collapse

of sodium exclusion following anoxia treatment of roots (Drew

and Lauchli 1985). Radioisotope tracer studies have shown that

rates of root respiration in saline media are positively correlated

to sodium exclusion capacity between rice varieties (Malagoli

et al. 2008), further illustrating this relationship.

Future Perspectives

As the powerhouses of eukaryotic cells, mitochondria rep-

resent an ancient but flexible factory in cells that enable cell

function, growth and division through energy metabolism.

While our knowledge of how plant mitochondria work is

rapidly increasing, much is still being extrapolated from

yeast and mammalian systems without direct evidence in

plants. Detailed insights into the assembly of mitochon-

drial machinery, the signalling by mitochondrial of oxidative

stress and the regulation of respiratory rate are still needed

in order to maximise respiration for plant protection in harsh

environments and to minimize respiratory losses to enhance

plant yields.

Acknowledgements

This work was supported by the Australian Research Council(ARC) ARC Centre of Excellence for Plant Energy Biology(CE0561495). RPJ is supported by a Grains Research andDevelopment Corporation (GRDC) PhD scholarship, LL wasfunded by Scholarship International Research Fees (SIRF),University International Stipend (UIS) and a Top Up Scholarshipfor UIS. AHM is supported by the Australian Research Council(ARC) as an ARC Future Fellow.

Received 30 Jul. 2012 Accepted 2 Oct. 2012

References

Abe F, Saito K, Miura K, Toriyama K (2002) A single nucleotide

polymorphism in the alternative oxidase gene among rice varieties

differing in low temperature tolerance. FEBS Lett. 527, 181–185.

Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to

study antioxidant defenses. Free Radic. Biol. Med. 23, 473–479.

Amthor JS (2000) The McCree-de Wit-Penning de Vries-Thornley

respiration paradigms: 30 years later. Ann. Bot. 86, 1–20.

Arakawa T, Timasheff SN (1985) The stabilization of proteins by

osmolytes. Biophys. J. 47, 411–414.

Araujo WL, Nunes-Nesi A, Osorio S, Usadel B, Fuentes D, Nagy R,

Balbo I, Lehmann M, Studart-Witkowski C, Tohge T, Martinoia

E, Jordana X, DaMatta FM, Fernie AR (2011) Antisense inhibition

of the iron-sulphur subunit of succinate dehydrogenase enhances

photosynthesis and growth in tomato via an organic acid-mediated

effect on stomatal aperture. Plant Cell 23, 600–627.

Armstrong AF, Logan DC, Tobin AK, O’Toole P, Atkin OK (2006)

Heterogeneity of plant mitochondrial responses underpinning respi-

ratory acclimation to the cold in Arabidopsis thaliana leaves. Plant

Cell Environ. 29, 940–949.

Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) The hot and

the cold: Unravelling the variable response of plant respiration to

temperature. Funct. Plant Biol. 32, 87–105.

Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in

orchestrating drought tolerance. Ann. Bot. 103, 581–597.

Attallah CV, Welchen E, Pujol C, Bonnard G, Gonzalez DH (2007)

Characterization of Arabidopsis thaliana genes encoding functional

homologues of the yeast metal chaperone Cox19p, involved in

cytochrome c oxidase biogenesis. Plant Mol. Biol. 65, 343–355.

Barrientos A, Gouget K, Horn D, Soto IC, Fontanesi F (2009)

Suppression mechanisms of COX assembly defects in yeast and

human: Insights into the COX assembly process. Biochim. Biophys.

Acta 1793, 97–107.

Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, Nielsen

J, Selbig J, Liu J, Fernie AR, Sweetlove LJ (2007) The metabolic

response of heterotrophic Arabidopsis cells to oxidative stress. Plant

Physiol. 143, 312–325.


Bhuiyan NH, Hamada A, Yamada N, Rai V, Hibino T, Takabe T

(2007) Regulation of betaine synthesis by precursor supply and

choline monooxygenase expression in Amaranthus tricolor . J. Exp.

Bot. 58, 4203–4212.

Cardol P (2011) Mitochondrial NADH:ubiquinone oxidoreductase

(complex I) in eukaryotes: A highly conserved subunit composition

highlighted by mining of protein databases. Biochim. Biophys. Acta

1807, 1390–1397.

Carrie C, Murcha MW, Kuehn K, Duncan O, Barthet M, Smith

PM, Eubel H, Meyer E, Day DA, Millar AH, Whelan J (2008)

Type II NAD(P)H dehydrogenases are targeted to mitochondria and

chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett.

582, 3073–3079.

Catoni E, Desimone M, Hilpert M, Wipf D, Kunze R, Schneider A,

Flugge UI, Schumacher K, Frommer WB (2003a) Expression

pattern of a nuclear encoded mitochondrial arginine- ornithine

translocator gene from Arabidopsis. BMC Plant Biol. 3, 1.

Catoni E, Schwab R, Hilpert M, Desimone M, Schwacke R, Flugge

UI, Schumacher K, Frommer WB (2003b) Identification of an

Arabidopsis mitochondrial succinate-fumarate translocator. FEBS

Lett. 534, 87–92.

Chen CB, Dickman MB (2005) Proline suppresses apoptosis in the

fungal pathogen Colletotrichum trifolii. Proc. Natl. Acad. Sci. USA

102, 3459–3464.

Chen X, Wang Y, Li J, Jiang A, Cheng Y, Zhang W (2009) Mitochon-

drial proteome during salt stress-induced programmed cell death in

rice. Plant Physiol. Biochem. 47, 407–415.

Ciais P, Reichstein M, Viovy N, Granier A, Ogee J, Allard V, Aubinet

M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De

Noblet N, Friend AD, Friedlingstein P, Grunwald T, Heinesch B,

Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci

G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal

S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T,

Valentini R (2005) Europe-wide reduction in primary productivity

caused by the heat and drought in 2003. Nature 437, 529–533.

Considine MJ, Goodman M, Echtay KS, Laloi M, Whelan J, Brand

MD, Sweetlove LJ (2003) Superoxide stimulates a proton leak

in potato mitochondria that is related to the activity of uncoupling

protein. J. Biol. Chem. 278, 22298–22302.

Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic

analysis of cold stress response in rice seedlings. Proteomics 5,

3162–3172.

De Block M, Van Lijsebettens M (2011) Energy efficiency and energy

homeostasis as genetic and epigenetic components of plant perfor-

mance and crop productivity. Curr. Opin. Plant Biol. 14, 275–282.

de Longevialle AoF, Meyer EH, Andres C, Taylor NL, Lurin C, Millar

AH, Small ID (2007) The pentatricopeptide repeat gene OTP43

is required for trans-splicing of the mitochondrial nad1 Intron 1 in

Arabidopsis thaliana. Plant Cell 19, 3256–3265.

Deighton N, Muckenschnabel I, Goodman BA, Williamson B (1999)

Lipid peroxidation and the oxidative burst associated with infection

of Capsicum annuum by Botrytis cinerea. Plant J. 20, 485–492.

Diaz F, Kotarsky H, Fellman V, Moraes CT (2011) Mitochondrial dis-

orders caused by mutations in respiratory chain assembly factors.

Sem. Fetal Neonatal. Med. 16, 197–204.

Dooki AD, Mayer-Posner FJ, Askari H, Zaiee AA, Salekdeh GH

(2006) Proteomic responses of rice young panicles to salinity.

Proteomics 6, 6498–6507.

Drew MC, Lauchli A (1985) Oxygen dependent exclusion of sodium

ions from shoots by roots of Zea mays (cv Pioneer 3906) in relation

to salinity damage. Plant Physiol. 79, 171–176.

Dungey NO, Davies DD (1982) Protein turnover in isolated barley

leaf segments and the effects of stress. J. Exp. Bot. 33, 12–

20.

Dutilleul C, Garmier M, Noctor G, Mathieu C, Chetrit P, Foyer

CH, de Paepe R (2003) Leaf mitochondria modulate whole cell

redox homeostasis, set antioxidant capacity, and determine stress

resistance through altered signaling and diurnal regulation. Plant

Cell 15, 1212–1226.

Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochem-

istry of 4-hydroxynonenal, malonaldehyde and related aldehydes.

Free Rad. Biol. Med. 11, 81–128.

Eubel H, Jansch L, Braun HP (2003) New insights into the respiratory

chain of plant mitochondria. Supercomplexes and a unique compo-

sition of complex II. Plant Physiol. 133, 274–286.

Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweet-

love LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F

is essential for redox homeostasis and root growth of Arabidopsis

thaliana under stress. J. Biol. Chem. 280, 12168–12180.

Finnegan P, Soole KL, Umbach AL (2004) Alternative mitochondrial

electron transport proteins in higher plants. In: Day DA, Millar AH,

Whelan J, eds. Plant Mitochondria: From Genome to Function –

Advances in Photosynthesis and Respiration. Springer. pp. 163–

230.

Flowers TJ (1972) Salt tolerance in Suaeda maritima – Effect of

sodium chloride on growth, respiration, and soluble enzymes in a

comparative study with Pisum sativum. J. Exp. Bot. 23, 310.

Foyer CH, Noctor G (2011) Ascorbate and glutathione: The heart of

the redox hub. Plant Physiol. 155, 2–18.

Fuentes D, Meneses M, Nunes-Nesi A, Araujo W, Tapia R, Gomez

I, Holuigue L, Gutierrez RA, Fernie AR, Jordana X (2011) A

deficiency in the flavoprotein of Arabidopsis mitochondrial complex

II results in elevated photosynthesis and better growth in nitrogen-

limiting conditions. Plant Physiol. 10.1104/pp.1111.183939.

Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi

H, Sato K, Nakazono M, Ma JF (2012) Acquisition of aluminium

tolerance by modification of a single gene in barley. Nat. Commun.

3, 713.

Garmier M, Carroll AJ, Delannoy E, Vallet C, Day DA, Small ID,

Millar AH (2008) Complex I dysfunction redirects cellular and

mitochondrial metabolism in Arabidopsis. Plant Physiol. 148, 1324–

1341.

Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva

R, Montillet JL (2006) Cadmium affects tobacco cells by a series


of three waves of reactive oxygen species that contribute to cyto-

toxicity. Plant Cell Environ. 29, 1956–1969.

Ghezzi D, Goffrini P, Uziel G, Horvath R, Klopstock T, Lochmuller

H, D’Adamo P, Gasparini P, Strom TM, Prokisch H, Invernizzi

F, Ferrero I, Zeviani M (2009) SDHAF1, encoding a LYR complex-

II specific assembly factor, is mutated in SDH-defective infantile

leukoencephalopathy. Nature Genet. 41, 654–656.

Giraud E, Ho LHM, Clifton R, Carroll A, Estavillo G, Tan YF, Howell

KA, Ivanova A, Pogson BJ, Millar AH, Whelan J (2008) The

absence of alternative oxidase1a in Arabidopsis results in acute

sensitivity to combined light and drought stress. Plant Physiol. 147,

595–610.

Gleason C, Huang S, Thatcher LF, Foley RC, Anderson CR, Carroll

AJ, Millar AH, Singh KB (2011) Mitochondrial complex II has a

key role in mitochondrial-derived reactive oxygen species influence

on plant stress gene regulation and defense. Proc. Natl. Acad. Sci.

USA 108, 10768–10773.

Gonzalez DH, Welchen E, Attallah CV, Comelli RN, Mufarrege

EF (2007) Transcriptional coordination of the biogenesis of the

oxidative phosphorylation machinery in plants. Plant J. 51, 105–

116.

Guan Y, Rawsthorne S, Scofield G, Shaw P, Doonan J (1995)

Cloning and characterization of a dihydrolipoamide acetyltrans-

ferase (E2) subunit of the pyruvate dehydrogenase complex from

Arabidopsis thaliana. J. Biol. Chem. 270, 5412–5417.

Hamasur B, Glaser E (1992) Plant mitochondrial F0F1 ATP synthase.

Identification of the individual subunits and properties of the purified

spinach leaf mitochondrial ATP synthase. Eur. J. Biochem. 205,

409–416.

Hamel P, Saint-Georges Y, de Pinto B, Lachacinski N, Altamura

N, Dujardin G (2004) Redundancy in the function of mitochondrial

phosphate transport in Saccharomyces cerevisiae and Arabidopsis

thaliana. Mol. Microbiol. 51, 307–317.

Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptations to

NaCl. Complex I is protected by anti-oxidants and small heat shock

proteins, whereas complex II is protected by proline and betaine.

Plant Physiol. 126, 1266–1274.

Hanning I, Heldt HW (1993) On the function of mitochondrial

metabolism during photosynthesis in spinach (Spinacia oleracea

L.) leaves (Partitioning between respiration and export of redox

equivalents and precursors for nitrate assimilation products). Plant

Physiol. 103, 1147–1154.

Hao HX, Khalimonchuk O, Schraders M, Dephoure N, Bayley JP,

Kunst H, Devilee P, Cremers CW, Schiffman JD, Bentz BG,

Gygi SP, Winge DR, Kremer H, Rutter J (2009) SDH5, a gene

required for flavination of succinate dehydrogenase, is mutated in

paraganglioma. Science 325, 1139–1142.

Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of

osmolyte accumulation during stress. Plant Cell Environ. 21, 535–

553.

Hauben M, Haesendonckx B, Standaert E, Van Der Kelen K, Azmi

A, Akpo H, Van Breusegem F, Guisez Y, Bots M, Lambert B,

Laga B, De Block M (2009) Energy use efficiency is characterized

by an epigenetic component that can be directed through artificial

selection to increase yield. Proc. Natl. Acad. Sci. USA 106, 20109–

20114.

Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D (2010) The matrix

peptide exporter HAF-1 signals a mitochondrial UPR by activating

the transcription factor ZC376.7 in C. elegans. Mol. Cell 37, 529–

540.

Heazlewood JL, Howell KA, Millar AH (2003a) Mitochondrial complex

I from Arabidopsis and rice: Orthologs of mammalian and fungal

components coupled with plant-specific subunits. Biochim. Biophys.

Acta 1604, 159–169.

Heazlewood JL, Howell KA, Whelan J, Millar AH (2003b) Towards

an analysis of the rice mitochondrial proteome. Plant Physiol. 132,

230–242.

Heazlewood JL, Whelan J, Millar AH (2003c) The products of the

mitochondrial orf25 and orfB genes are FO components in the plant

F1FO ATP synthase. FEBS Lett. 540, 201–205.

Hossain Z, Nouri MZ, Komatsu S (2012) Plant cell organelle pro-

teomics in response to abiotic stress. J. Proteome Res. 11, 37–48.

Hoyos ME, Palmieri L, Wertin T, Arrigoni R, Polacco JC, Palmieri

F (2003) Identification of a mitochondrial transporter for basic

amino acids in Arabidopsis thaliana by functional reconstitution into

liposomes and complementation in yeast. Plant J. 33, 1027–1035.

Huang BR, Rachmilevitch S, Xu JC (2012) Root carbon and protein

metabolism associated with heat tolerance. J. Exp. Bot. 63, 3455–

3465.

Huang S, Millar AH, Taylor NL (2011) The plant mitochondrial pro-

teome composition and stress response: Conservation and diver-

gence between monocots and dicots. In: Kempken F, ed. Advances

in Plant Biology. Springer, New York. pp. 533.

Huang S, Taylor NL, Stroher E, Fenske R, Millar AH (2012) Succinate

dehydrogenase assembly factor 2 is needed for assembly and

activity of mitochondrial complex II and for normal root elongation

in Arabidopsis. Plant J. (in press).

Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial pro-

teomes provide new links between antioxidant defense and plant

salinity tolerance. J. Prot. Res. 9, 6595–6604.

Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial

respiration in salinity tolerance. Trends Plant Sci. 16, 614–623.

Jansch L, Kruft V, Schmitz UK, Braun HP (1996) New insights into

the composition, molecular mass and stoichiometry of the protein

complexes of plant mitochondria. Plant J. 9, 357–368.

Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative pro-

teomic analysis of NaCl stress-responsive proteins in Arabidopsis

roots. J. Exp. Bot. 58, 3591–3607.

Johnson DT, Harris RA, French S, Blair PV, You J, Bemis KG, Wang

M, Balaban RS (2007) Tissue heterogeneity of the mammalian

mitochondrial proteome. Am. J. Physiol. 292, C689–C697.

Karpova OV, Kuzmin EV, Elthon TE, Newton KJ (2002) Differential

expression of alternative oxidase genes in maize mitochondrial

mutants. Plant Cell 14, 3271–3284.


Klodmann J, Sunderhaus S, Nimtz M, Jansch L, Braun HP (2010)

Internal architecture of mitochondrial complex I from Arabidopsis

thaliana. Plant Cell 22, 797–810.

Komatsu S, Yamamoto A, Nakamura T, Nouri MZ, Nanjo Y,

Nishizawa K, Furukawa K (2011) Comprehensive analysis of

mitochondria in roots and hypocotyls of soybean under flooding

stress using proteomics and metabolomics techniques. J. Prot. Res.

10, 3993–4004.

Koyama H, Kawamura A, Kihara T, Hara T, Takita E, Shibata D

(2000) Overexpression of mitochondrial citrate synthase in Ara-

bidopsis thaliana improved growth on a phosphorus-limited soil.

Plant Cell Physiol. 41, 1030–1037.

Kuffner R, Rohr A, Schmiede A, Krull C, Schulte U (1998) Involve-

ment of two novel chaperones in the assembly of mitochondrial

NADH:Ubiquinone oxidoreductase (complex I). J. Mol. Biol. 283,

409–417.

Kurimoto K, Day DA, Lambers H, Noguchi K (2004) Effect of

respiratory homeostasis on plant growth in cultivars of wheat and

rice. Plant Cell Environ. 27, 853–862.

Kuzmin EV, Karpova OV, Elthon TE, Newton KJ (2004) Mitochondrial

respiratory deficiencies signal pu-regulation of genes for heat shock

proteins. J. Biol. Chem. 279, 20672–20677.

La Cognata U, Landschutze V, Willmitzer L, Muller-Rober B (1996)

Structure and expression of mitochondrial citrate synthases from

higher plants. Plant Cell Physiol. 37, 1022–1029.

Laloi M (1999) Plant mitochondrial carriers: An overview. Cell Mol. Life

Sci. 56, 918–944.

Lazarou M, McKenzie M, Ohtake A, Thorburn DR, Ryan MT (2007)

Analysis of the assembly profiles for mitochondrial- and nuclear-

DNA-encoded subunits into complex I. Mol. Cell Biol. 27, 4228–

4237.

Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I

defect impairs cold-regulated nuclear gene expression. Plant Cell

14, 1235–1251.

Lee CP, Eubel H, O’Toole N, Millar A (2011) Combining proteomics

of root and shoot mitochondria and transcript analysis to define

constitutive and variable components in plant mitochondria. Phyto-

chemistry 72, 1092–1108.

Lee CP, Eubel H, O’Toole N, Millar AH (2008) Heterogeneity of the

mitochondrial proteome for photosynthetic and non-photosynthetic

Arabidopsis metabolism. Mol. Cell Proteomics 7, 1297–1316.

Lee CP, Eubel H, Solheim C, Millar AH (2012) Mitochondrial proteome

heterogeneity between tissues from the vegetative and reproductive

stages of Arabidopsis thaliana development. J. Prot. Res. 11, 3326–

3343.

Leon G, Holuigue L, Jordana X (2007) Mitochondrial complex II

Is essential for gametophyte development in Arabidopsis. Plant

Physiol. 143, 1534–1546.

Li L, Carrie C, Nelson C, Whelan J, Millar AH (2012) Accumulation of

newly synthesised F1 in vivo in Arabidopsis mitochondria provides

evidence for modular assembly of the plant F1Fo ATP synthase. J.

Biol. Chem. 287, 25749–25757.

Luethy MH, Miernyk JA, Randall DD (1995) The mitochondrial pyru-

vate dehydrogenase complex: Nucleotide and deduced amino-acid

sequences of a cDNA encoding the Arabidopsis thaliana E1 alpha-

subunit. Gene 164, 251–254.

Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and

the complexing role of organic acids. Trends Plant Sci. 6, 273–278.

Malagoli P, Britto DT, Schulze LM, Kronzucker HJ (2008) Futile

Na+ cycling at the root plasma membrane in rice (Oryza sativa L.):

Kinetics, energetics, and relationship to salinity tolerance. J. Exp.

Bot. 59, 4109–4117.

Mannella CA (1992) The ‘ins’ and ‘outs’ of mitochondrial membrane

channels. Trends Biochem. Sci. 17, 315–320.

Mannella CA, Pfeiffer DR, Bradshaw PC, Moraru II, Slepchenko

B, Loew LM, Hsieh CE, Buttle K, Marko M (2001) Topology

of the mitochondrial inner membrane: Dynamics and bioenergetic

implications. IUBMB Life 52, 93–100.

Mannella CA, Tedeschi H (1987) Importance of the mitochondrial outer

membrane channel as a model biological channel. J. Bioenerg.

Biomembr. 19, 305–308.

Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase

lowers mitochondrial reactive oxygen production in plant cells. Proc.

Natl. Acad. Sci. USA 96, 8271–8276.

McCree KJ (1986) Whole-plant carbon balance during osmotic ad-

justment to drought and salinity stress. Aust. J. Plant Physiol. 13,

33–43.

McDonald AE (2008) Alternative oxidase: An inter-kingdom perspec-

tive on the function and regulation of this broadly distributed

‘cyanide-resistant’ terminal oxidase. Funct. Plant Biol. 35, 535–

552.

Meyer EH, Solheim C, Tanz SK, Bonnard G, Millar AH (2011) Insights

into the composition and assembly of the membrane arm of plant

complex I through analysis of subcomplexes in Arabidopsis mutant

lines. J. Biol. Chem. 286, 26081–26092.

Meyer EH, Taylor NL, Millar AH (2008) Resolving and identifying

protein components of plant mitochondrial respiratory complexes

using three dimensions of gel electrophoresis. J. Prot. Res. 7, 786–

794.

Meyer EH, Tomaz T, Carroll AJ, Estavillo G, Delannoy E, Tanz SK,

Small ID, Pogson BJ, Millar AH (2009) Remodeled respiration in

ndufs4 with low phosphorylation efficiency suppresses Arabidopsis

germination and growth and alters control of metabolism at night.


Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson

U, Brennicke A, Binder S, Rasmusson AG (2003) Arabidopsis

genes encoding mitochondrial type II NAD(P)H dehydrogenases

have different evolutionary origin and show distinct responses to

light. Plant Physiol. 133, 642–652.

Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase

but not the alternative oxidase of plant mitochondria. FEBS Lett.

398, 155–158.

Millar AH, Eubel H, Jansch L, Kruft V, Heazlewood JL, Braun

HP (2004a) Mitochondrial cytochrome c oxidase and succinate


dehydrogenase complexes contain plant specific subunits. Plant

Mol. Biol. 56, 77–90.

Millar AH, Leaver CJ (2000) The cytotoxic lipid peroxidation product,

4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydro-

genases in the matrix of plant mitochondria. FEBS Lett. 481, 117–

121.

Millar AH, Trend AE, Heazlewood JL (2004b) Changes in the mi-

tochondrial proteome during the anoxia to air transition in rice

focus around cytochrome-containing respiratory complexes. J. Biol.

Chem. 279, 39471–39478.

Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and

regulation of mitochondrial respiration in plants. Ann. Rev. Plant

Biol. 62, 79–104.

Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A (2009)

Unraveling delta(1)-pyrroline-5-carboxylate-proline cycle in plants

by uncoupled expression of proline oxidation enzymes. J. Biol.

Chem. 284, 26482–26492.

Miller RJ, Bittell JE, Koeppe DE (1973) Effect of cadmium on elec-

tron transport and energy transfer reactions in corn mitochondria.

Physiol. Plant. 28, 166–171.

Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT (2012)

Understanding mitochondrial complex I assembly in health and

disease. Biochim. Biophys. Acta 1817, 851–862.

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004)

Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–

498.

Moller IM (2001) Plant mitochondria and oxidative stress: Electron

transport, NADPH turnover, and metabolism of reactive oxygen

species. Ann. Rev. Plant Physiol. Plant Mol. Biol. 52, 561–

591.

Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to

cellular components in plants. Ann. Rev. Plant Biol. 58, 459–481.

Møller IM, Sweetlove LJ (2011) ROS signalling – specificity is required.

Trends Plant Sci. 15, 370–374.

Montillet J-L, Agnel J-P, Ponchet M, Vailleau F, Roby D, Trianta-

phylides C (2002) Lipoxygenase-mediated production of fatty acid

hydroperoxides is a specific signature of the hypersensitive reaction

in plants. Plant Physiol. Biochem. 40, 633–639.

Moore CS, Cook-Johnson R, Rudhe C, Whelan J, Day DA, Wiskich

JT, Soole KL (2003) Identification of AtNDI1, an internal non-

phosphorylating NAD(P)H dehydrogenase in Arabidopsis thaliana

mitochondria. Plant Physiol. 133, 1968–1978.

Morgan MJ, Lehmann M, Schwarzlander M, Baxter CJ, Sienkiewicz-

Porzucek A, Williams TCR, Schauer N, Fernie AR, Fricker MD,

Ratcliffe RG, Sweetlove LJ, Finkemeier I (2008) Decrease in

manganese superoxide dismutase leads to reduced root growth

and affects tricarboxylic acid cycle flux and mitochondrial redox

homeostasis. Plant Physiol. 147, 101–114.

Ndimba BK, Chivasa S, Simon WJ, Slabas AR (2005) Identification of

Arabidopsis salt and osmotic stress responsive proteins using two-

dimensional difference gel electrophoresis and mass spectrometry.

Proteomics 5, 4185–4196.

Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology

and homeostasis in plants. Trends Plant Sci. 12, 125–134.

Noguchi K, Yoshida K (2008) Interaction between photosynthesis and

respiration in illuminated leaves. Mitochondrion 8, 87–99.

Noordermeer MA, Feussner I, Kolbe A, Veldink GA, Vliegen-

thart JFG (2000) Oxygenation of (3Z)-alkenals to 4-hydroxy-(2E)-

alkenals in plant extracts: A nonenzymatic process. Biochem.

Biophys. Res. Comm. 277, 112–116.

Nouws J, Nijtmans LG, Smeitink JA, Vogel RO (2012) Assembly

factors as a new class of disease genes for mitochondrial complex

I deficiency: Cause, pathology and treatment options. Brain 135,

12–22.

Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A,

Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR

(2007) Deficiency of mitochondrial fumarase activity in tomato plants

impairs photosynthesis via an effect on stomatal function. Plant J.

50, 1093–1106.

Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AM, Loureiro ME,

Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photo-

synthetic performance and growth as a consequence of decreasing

mitochondrial malate dehydrogenase activity in transgenic tomato

plants. Plant Physiol. 137, 611–622.

Osman C, Wilmes C, Tatsuta T, Langer T (2007) Prohibitins interact

genetically with Atp23, a novel processing peptidase and chaperone

for the F1Fo-ATP synthase. Mol. Biol. Cell 18, 627–635.

Palmieri F, Rieder B, Ventrella A, Blanco E, Do PT, Nunes-Nesi

A, Trauth AU, Fiermonte G, Tjaden J, Agrimi G, Kirchberger

S, Paradies E, Fernie AR, Neuhaus HE (2009) Molecular iden-

tification and functional characterization of Arabidopsis thaliana

mitochondrial and chloroplastic NAD+ carrier proteins. J. Biol.

Chem. 284, 31249–31259.

Palmieri L, Santoro A, Carrari F, Blanco E, Nunes-Nesi A, Arrigoni

R, Genchi F, Fernie AR, Palmieri F (2008) Identification and char-

acterization of ADNT1, a novel mitochondrial adenine nucleotide

transporter from Arabidopsis. Plant Physiol. 148, 1797–1808.

Peiffer WE, Ingle RT, Ferguson-Miller S (1990) Structurally unique

plant cytochrome c oxidase isolated from wheat germ, a rich

source of plant mitochondrial enzymes. Biochemistry 29, 8696–

8701.

Picault N, Palmieri L, Pisano I, Hodges M, Palmieri F (2002) Identifi-

cation of a novel transporter for dicarboxylates and tricarboxylates in

plant mitochondria. Bacterial expression, reconstitution, functional

characterization, and tissue distribution. J. Biol. Chem. 277, 24204–

24211.

Pickova A, Potocky M, Houstek J (2005) Assembly factors of F1FO-

ATP synthase across genomes. Proteins 59, 393–402.

Pineau B, Layoune O, Danon A, De Paepe R (2008) L-galactono-1,4-

lactone dehydrogenase is required for the accumulation of plant

respiratory complex I. J. Biol. Chem. 283, 32500–32505.

Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen

economy of 24 wild species differing in relative growth rate. Plant

Physiol. 94, 621–627.


Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA,

Brand MD (2012) Mitochondrial complex II can generate reactive

oxygen species at high rates in both the forward and reverse

reactions. J. Biol. Chem. 10.1074/jbc.M1112.374629.

Raghavendra AS, Padmasree K (2003) Beneficial interactions of

mitochondrial metabolism with photosynthetic carbon assimilation.

Trends Plant Sci. 8, 546–553.

Rak M, Gokova S, Tzagoloff A (2011) Modular assembly of yeast

mitochondrial ATP synthase. EMBO J. 30, 920–930.

Rak M, Tzagoloff A (2009) F1-dependent translation of mitochondrially

encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc.

Natl. Acad. Sci. USA 106, 18509–18514.

Rasmusson AG, Soole KL, Elthon TE (2004) Alternative NAD(P)H

dehydrogenases of plant mitochondria. Ann. Rev. Plant Biol. 55,

23–39.

Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau

A, Deleu C (2010) The Arabidopsis pop2–1 mutant reveals the

involvement of GABA transaminase in salt stress tolerance. BMC

Plant Biol. 10, 20.

Rigas S, Daras G, Laxa M, Marathias N, Fasseas C, Sweetlove LJ,

Hatzopoulos P (2009) Role of Lon1 protease in post-germinative

growth and maintenance of mitochondrial function in Arabidopsis

thaliana. New Phytol. 181, 588–600.

Robert N, d’Erfurth I, Marmagne A, Erhardt M, Allot M, Boivin K,

Gissot L, Monachello D, Michaud M, Duchene AM, Barbier-

Brygoo H, Marechal-Drouard L, Ephritikhine G, Filleur S (2012)

Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a

dual localization in the cell but show a distinct role in mitochondria.

Plant Mol. Biol. 78, 431–446.

Robison MM, Ling X, Smid MP, Zarei A, Wolyn DJ (2009) Anti-

sense expression of mitochondrial ATP synthase subunits OSCP

(ATP5) and gamma (ATP3) alters leaf morphology, metabolism

and gene expression in Arabidopsis. Plant Cell Physiol. 50, 1840–

1850.

Rutter J, Winge DR, Schiffman JD (2010) Succinate dehydrogenase

– Assembly, regulation and role in human disease. Mitochondrion

10, 393–401.

Sabar M, Balk J, Leaver CJ (2005) Histochemical staining and

quantification of plant mitochondrial respiratory chain complexes

using blue-native polyacrylamide gel electrophoresis. Plant J. 44,

893–901.

Sabar M, Gagliardi D, Balk J, Leaver CJ (2003) ORFB is a subunit of

F(1)F(O)-ATP synthase: Insight into the basis of cytoplasmic male

sterility in sunflower. EMBO Rep. 4, 1–6.

Saisho D, Nakazono M, Lee K, Tsutsumi N, Akita S, Hirai A

(2001) The gene for alternative oxidase-2 (AOX2) from Arabidopsis

thaliana consists of five exons unlike other AOX genes and is

transcribed at an early stage during germination. Genes Genet.

Syst. 76, 89–97.

Sappl PG, Carroll AJ, Clifton R, Lister R, Whelan J, Millar AH,

Singh KB (2009) The Arabidopsis glutathione transferase gene

family displays complex stress regulation and co-silencing multiple

genes results in altered metabolic sensitivity to oxidative stress.

Plant J. 58, 53–68.

Saradadevi K, Raghavendra AS (1992) Dark respiration protects

photosynthesis against photoinhibtion in mesophyll protoplasts of

pea (Pisum sativum). Plant Physiol. 99, 1232–1237.

Sarria R, Lyznik A, Vallejos CE, Mackenzie SA (1998) A cytoplasmic

male sterility-associated mitochondrial peptide in common bean is

post-translationally regulated. Plant Cell 10, 1217–1228.

Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V,

Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin

C, Ezan E, Garin J, Bourguignon J (2006) The early responses

of Arabidopsis thaliana cells to cadmium exposure explored by

protein and metabolite profiling analyses. Proteomics 6, 2180–

2198.

Schulte U (2001) Biogenesis of respiratory complex I. J. Bioenerg.

Biomembr. 33, 205–212.

Senior AE (1990) The proton-translocating ATPase of Escherichia coli.

Ann. Rev. Biophys. Biophys. Chem. 19, 7–41.

Shingaki-Wells RN, Huang SB, Taylor NL, Carroll AJ, Zhou WX,

Millar AH (2011) Differential molecular responses of rice and wheat

coleoptiles to anoxia reveal novel metabolic adaptations in amino

acid metabolism for tissue tolerance. Plant Physiol. 156, 1706–

1724.

Siddique M, Gernhard S, von Koskull-Doring P, Vierling E, Scharf

KD (2008) The plant sHSP superfamily: Five new members in

Arabidopsis thaliana with unexpected properties. Cell Stress Chap-

erones 13, 183–197.

Smith PM, Fox JL, Winge DR (2012) Biogenesis of the cytochrome

bc(1) complex and role of assembly factors. Biochim. Biophys. Acta

1817, 276–286.

Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier

P, Dauzat M, Heurtevin L, Guyon V, Takenaka M, Rogowsky

PM (2012) PPR2263, a DYW-subgroup pentatricopeptide repeat

protein, is required for mitochondrial nad5 and cob transcript editing,

mitochondrion biogenesis, and maize growth. Plant Cell 24, 676–

691.

Stadtman ER (1993) Oxidation of free amino acids and amino acid

residues in proteins by radiolysis and by metal-catalyzed reactions.

Annu. Rev. Biochem. 62, 797–821.

Sweetlove LJ, Beard KFM, Nunes-Nesi A, Fernie AR, Ratcliffe RG

(2010) Not just a circle: Flux modes in the plant TCA cycle. Trends

Plant Sci. 15, 462–470.

Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA,

Leaver CJ, Millar AH (2002) The impact of oxidative stress on

Arabidopsis mitochondria. Plant J. 32, 891–904.

Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor

NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial

uncoupling protein is required for efficient photosynthesis. Proc.

Natl. Acad. Sci. USA 103, 19587–19592.

Tan YF, Millar AH, Taylor NL (2012) Components of mitochondrial

oxidative phosphorylation vary in abundance following exposure to

cold and chemical stresses. J. Prot. Res. 11, 3860–3879.


Tan YF, O’Toole N, Taylor NL, Millar AH (2010) Divalent metal ions

in plant mitochondria and their role in interactions with proteins

and oxidative stress-induced damage to respiratory function. Plant

Physiol. 152, 747–761.

Tateda C, Watanabe K, Kusano T, Takahashi Y (2011) Molecular and

genetic characterization of the gene family encoding the voltage-

dependent anion channel in Arabidopsis. J. Exp. Bot. 62, 4773–

4785.

Taylor NL, Day DA, Millar AH (2002) Environmental stress causes

oxidative damage to plant mitochondria leading to inhibition of

glycine decarboxylase. J. Biol. Chem. 277, 42663–42668.

Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential im-

pact of environmental stresses on the pea mitochondrial proteome.

Mol. Cell Proteomics 4, 1122–1133.

Taylor NL, Howell KA, Heazlewood JL, Tan TYW, Narsai R, Huang

SB, Whelan J, Millar AH (2010) Analysis of the rice mitochondrial

carrier family reveals anaerobic accumulation of a basic amino acid

carrier involved in arginine metabolism during seed germination.


Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmen-

tal stress induced changes in the Arabidopsis thaliana chloroplast,

mitochondria and peroxisome proteomes. J. Proteomics 72, 367–

378.

Thelen JJ, Miernyk JA, Randall DD (2000) Pyruvate dehydrogenase

kinase from Arabidopsis thaliana: A protein histidine kinase that

phosphorylates serine residues. Biochem. J. 349, 195–201.

Thirkettle-Watts D, McCabe TC, Clifton R, Moore C, Finnegan

PM, Day DA, Whelan J (2003) Analysis of the alternative

oxidase promoters from soybean. Plant Physiol. 133, 1158–

1169.

Tomaz T, Bagard M, Pracharoenwattana I, Linden P, Lee CP,

Carroll AJ, Stroher E, Smith SM, Gardestrom P, Millar AH

(2010) Mitochondrial malate dehydrogenase lowers leaf respiration

and alters photorespiration and plant growth in Arabidopsis. Plant

Physiol. 154, 1143–1157.

Tuschen G, Sackmann U, Nehls U, Haiker H, Buse G, Weiss

H (1990) Assembly of NADH: Ubiquinone reductase (complex I)

in Neurospora mitochondria. Independent pathways of nuclear-

encoded and mitochondrially encoded subunits. J. Mol. Biol. 213,

845–857.

Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J,

Nijtmans L (2004) Human mitochondrial complex I assembles

through the combination of evolutionary conserved modules: A

framework to interpret complex I deficiencies. Hum. Mol. Genet.

13, 2461–2472.

Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mi-

tochondrial genome of Arabidopsis thaliana contains 57 genes in

366,924 nucleotides. Nature Genet. 15, 57–61.

Van Aken O, Giraud E, Clifton R, Whelan J (2009) Alternative

oxidase: A target and regulator of stress responses. Physiol. Plant.

137, 354–361.

van der Merwe MJ, Osorio S, Moritz T, Nunes-Nesi A, Fernie AR

(2009) Decreased mitochondrial activities of malate dehydrogenase

and fumarase in tomato lead to altered root growth and architecture

via diverse mechanisms. Plant Physiol. 149, 653–669.

Velours J, Arselin G (2000) The saccharomyces cerevisiae ATP

synthase. J. Bioenerg. Biomembr. 32, 383–390.

Verniquet F, Gaillard J, Neuburger M, Douce R (1991) Rapid inac-

tivation of plant aconitase by hydrogen peroxide. Biochem. J. 276,

643–648.

Verslues PE, Sharp RE (1999) Proline accumulation in maize (Zea

mays L.) primary roots at low water potentials. II. Metabolic source

of increased proline deposition in the elongation zone. Plant Physiol.

119, 1349–1360.

Videira A, Duarte M (2002) From NADH to ubiquinone in Neurospora

mitochondria. Biochim. Biophys. Acta 1555, 187–191.

Vigani G (2012) Discovering the role of mitochondria in the iron

deficiency-induced metabolic responses of plants. J. Plant Physiol.

169, 1–11.

Vogel RO, van den Brand MA, Rodenburg RJ, van den Heuvel LP,

Tsuneoka M, Smeitink JA, Nijtmans LG (2007) Investigation of

the complex I assembly chaperones B17.2L and NDUFAF1 in a

cohort of CI deficient patients. Mol. Gen. Met. 91, 176–182.

Welchen E, Gonzalez DH (2005) Differential expression of the Ara-

bidopsis cytochrome c genes Cytc-1 and Cytc-2. Evidence for the

involvement of TCP-domain protein-binding elements in anther- and

meristem-specific expression of the Cytc-1 gene. Plant Physiol.139,

88–100.

Werhahn W, Braun HP (2002) Biochemical dissection of the mitochon-

drial proteome from Arabidopsis thaliana by three-dimensional gel

electrophoresis. Electrophoresis 23, 640–646.

Winger AM, Millar AH, Day DA (2005) Sensitivity of plant mitochondrial

terminal oxidases to the lipid peroxidation product 4-hydroxy-2-

nonenal (HNE). Biochem. J. 387, 865–870.

Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH (2007)

The cytotoxic lipid peroxidation product 4-hydroxy-2-nonenal co-

valently modifies a selective range of proteins linked to respira-

tory function in plant mitochondria. J. Biol. Chem. 282, 37436–

37447.

Xu P, Yang Y, Zhang Z, Chen W, Zhang C, Zhang L, Zou S,

Ma Z (2008) Expression of the nuclear gene TaF(A)d is under

mitochondrial retrograde regulation in anthers of male sterile wheat

plants with timopheevii cytoplasm. J. Exp. Bot. 59, 1375–1381.

Yamasaki H, Shimoji H, Ohshiro Y, Sakihama Y (2001) Inhibitory

effects of nitric oxide on oxidative phosphorylation in plant mito-

chondria. Nitric Oxide 5, 261–270.

Zagdanska B (1995) Respiratory energy demand for protein turnover

and ion transport in wheat leaves upon water deficit. Physiol. Plant.

95, 428–436.

Zottini M, Formentin E, Scattolin M, Carimi F, Lo Schiavo F, Terzi M

(2002) Nitric oxide affects plant mitochondrial functionality in vivo.

FEBS Lett. 515, 75–78.

(Co-Editor: Jianping Hu)

Mitochondrial composition, function and stress response in plants

Documents

Transcript of Mitochondrial composition, function and stress response in plants