1 running title - plant physiology€¦ · 13.06.2016 · 138 al., 2012; youle and van der blick,...

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Running title: 1

FTSH4 as a mitochondrial quality control protein 2

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Corresponding authors: 5

Hanna Janska 6

Faculty of Biotechnology, University of Wroclaw 7

F. Joliot-Curie 14A, 50-383 Wroclaw, Poland 8

Tel. + 48 71 375 62 49, Fax + 48 71 375 62 34 9

E-mail address: [email protected] 10

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Christiane Funk 12

Dept. of Chemistry, Umeå University 13

901 87 Umeå, Sweden 14

Tel. + 46 90 786 7633, Fax + 46 90 786 7655 15

E-mail address: [email protected] 16

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Plant Physiology Preview. Published on June 13, 2016, as DOI:10.1104/pp.16.00370

Copyright 2016 by the American Society of Plant Biologists

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Title: Lack of FTSH4 protease affects protein carbonylation, mitochondrial 27

morphology and phospholipid content in mitochondria of Arabidopsis: new insights 28

into a complex interplay 29

Authors: Elwira Smakowska1*, Renata Skibior-Blaszczyk1*, Malgorzata Czarna1, 30

Marta Kolodziejczak1, Malgorzata Kwasniak-Owczarek1, Katarzyna Parys1, 31

Christiane Funk2a, Hanna Janska1a 32

1Faculty of Biotechnology, University of Wroclaw, F. Joliot-Curie 14A, 50-383 33

Wroclaw, Poland 34

2Department of Chemistry, Umeå University, 901 87 Umeå, Sweden. 35

aCorresponding authors 36

* These authors contributed equally to this work 37

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Summary Sentence: FTSH4 protease controls a proper cardiolipin content in the 39

mitochondrial membrane and in consequence prevents oxidative stress. 40

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Author contributions 42

HJ, CF designed the research. ES, RS, MC, MK, MKO, KP performed the 43

experiments. HJ, ES, MC, RS, MK, MKO, KP analyzed the data. HJ wrote the article 44

with input of all co-authors. 45

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This work was supported by Grants 2011/03/N/NZ2/00221 and 47

2013/11/N/NZ3/00061 from the National Science Centre, Poland, as well as by the 48

Swedish Energy Agency (2012-005889) and Umeå University. The contribution of 49

MKO was supported by the START scholarship granted by Foundation for Polish 50

Science and scholarship for outstanding young scientists from the Polish Minister of 51

Science and Higher Education. 52

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The Proteomics Facility of the Chemical Biological Centre of Umeå University 54

provided the facilities for performing the 2D-DIGE experiment and the MALDI-TOF 55

mass spectrometry analyses. 56

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Corresponding authors: 58

[email protected] 59

[email protected] 60

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ABSTRACT 92

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FTSH4 is one of the inner membrane-embedded ATP-dependent 94

metalloproteases in mitochondria of Arabidopsis thaliana. In mutants impaired to 95

express FTSH4 carbonylated proteins accumulated and leaf morphology was altered 96

when grown under short-day photoperiod, at 22°C, and long-day photoperiod, at 97

30°C. To provide better insight into the function of FTSH4 we compared the 98

mitochondrial proteomes and oxyproteomes of two ftsh4 mutants and wild type plants 99

grown under conditions inducing the phenotypic alterations. Numerous proteins from 100

various submitochondrial compartments were observed to be carbonylated in the 101

ftsh4 mutants indicating a widespread oxidative stress. One of the reasons for the 102

accumulation of carbonylated proteins in ftsh4 was limited ATP-dependent proteolytic 103

capacity of ftsh4 mitochondria, arising from insufficient ATP amount, probably as a 104

result of an impaired oxidative phosphorylation (OXPHOS), especially complex V. In 105

ftsh4 we further observed giant, spherical mitochondria co-existing among normal 106

ones. Both effects, the increased number of abnormal mitochondria as well as the 107

decreased stability/activity of the OXPHOS complexes was probably caused by the 108

lower amount of the mitochondrial membrane phospholipid cardiolipin. We postulate 109

that the reduced cardiolipin content in ftsh4 mitochondria leads to perturbations 110

within the OXPHOS complexes generating more reactive oxygen species, less ATP 111

and to deregulation of mitochondrial dynamics causing in consequence the 112

accumulation of oxidative damage. 113

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INTRODUCTION 126

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Mitochondria play an important role in cellular metabolism and cell longevity 128

with the most notable function in the generation of ATP through oxidative 129

phosphorylation. During oxidative phosphorylation (OXPHOS) under unfavorable 130

conditions, reactive oxygen species (ROS) are generated, which might lead to 131

oxidative damages (Moller, 2001). To avoid accumulation of non-functional proteins, 132

particularly the formation of insoluble, harmful protein aggregates, mitochondria have 133

evolved a hierarchically structured quality control (QC) system (Tatsuta and Langer, 134

2008; Baker et al., 2011; Fischer et al., 2012). The QC system links molecular, 135

organellar and cellular levels, and includes: i) a protease/chaperone system (Voos, 136

2013), ii) mitochondrial fission and fusion processes (Twig et al., 2008; Osellame et 137

al., 2012; Youle and van der Blick, 2012, Elgass et al., 2013), and - in case the first 138

two actions fail, iii) initiation of the intrinsic cell death program (Fischer et al., 2012, 139

Gaspard and McMaster, 2015). It ensures the persistence of a healthy mitochondrial 140

population and ultimately survival of the organism, especially during stress conditions 141

(Baker et al., 2014). 142

A conserved intra-mitochondrial network of chaperones and proteases that 143

maintain protein homeostasis (Tatsuta and Langer, 2007; Baker et al., 2011) 144

constitutes the first level of the QC system. Key proteolytic enzymes are ATP-145

dependent proteases, which combine both proteolytic and chaperone-like activities 146

(Voos, 2013). Typically, mitochondria contain three types of ATP-dependent 147

proteases: Lon, Clp, and FtsH (Janska et al., 2010). The two first protease families 148

are classified as serine proteases, whereas FtsH proteases have a catalytic site 149

characteristic for metalloproteases. 150

FtsH proteases, also termed as AAA proteases (ATPases Associated with 151

diverse cellular Activities), form oligomeric complexes in the mitochondrial inner 152

membrane with catalytic domains facing the intermembrane space (i-AAA) or matrix 153

side (m-AAA). Only one i-AAA protease is present in yeast (Yme1) and human 154

(YMEL1), while plant mitochondria contain two i-AAA proteases: FTSH4 and FTSH11 155

(Urantowka et al., 2005). Interestingly, different from human YMEL1, Arabidopsis 156

FTSH4 protease does not complement the yeast homolog, suggesting its plant 157

specific function (Urantowka et al., 2005). Yeast i-AAA protease was reported to act 158

as quality control enzyme and to degrade unassembled inner membrane proteins 159



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(Pearce and Sherman, 1995; Nakai et al., 1995; Kambacheld et al., 2005; Augustin 160

et al., 2005) as well as misfolded small TIM chaperones (translocase of the inner 161

membrane) of the intermembrane space (IMS) (Baker et al., 2012). Non-assembled 162

respiratory chain proteins have been identified as proteolytic substrates for the 163

human i-AAA protease (Stiburek et al., 2012). So far, there is no information about 164

oxidatively damaged proteins being substrates of these i-AAA proteases. However, 165

an increasing amount of evidence indicates their crucial role in mitochondrial quality 166

control (Baker et al., 2011). It seems that the i-AAA protease-mediated proteolysis 167

controls mitochondrial dynamics in multiple ways. Yeast i-AAA was found to degrade 168

the phospholipid transfer proteins UPS1 and UPS2, responsible for the distribution of 169

cardiolipin (CL) and phosphatidylethanolamine (PE) in mitochondrial membranes 170

(Potting et al., 2010). Both phospholipids have a critical impact on several 171

mitochondrial functions including fusion and fission (Joshi et al., 2012; Pan et al., 172

2014). Next, it was shown that Yme1 processes Atg32, a mitochondrial outer 173

membrane receptor ensuring specificity of mitophagy (Wang et al., 2013). 174

Furthermore, in mammals and yeast, i-AAA proteases regulate mitochondrial 175

morphology and dynamics by processing the conserved fusion mediator OPA1 176

(Mgm1 in yeast) (Anand et al., 2013; Ruan et al., 2013). Finally, recent findings 177

indicate that Yme1L regulates mitochondrial dynamics, mitochondrial cristae 178

structure and nucleoid organization by controlling the Mic60/Mitofilin homeostasis (Li 179

et al., 2015). Other postulated biological roles for i-AAA proteases are dependent 180

exclusively on the chaperone-like activity of these enzymes. Specifically, the yeast 181

Yme1 protease has been proposed to act as a chaperone in the folding of numerous 182

proteins in the IMS (Fiumera et al., 2009, Schreiner et al., 2012), and in the assembly 183

of complex V (Francis and Thorsness, 2011). Further, Yme1 was shown to mediate 184

protein import into the intermembrane space (Rainey et al., 2006). 185

In Arabidopsis the loss of FTSH4 protease, one of the two i-AAA proteases in 186

plant mitochondria, impairs development and leaf morphology at the late stage of 187

rosette growth under short-day photoperiod, but not under long days (Gibala et al., 188

2009; Kicia et al., 2010). These conditional, morphological and developmental 189

alternations correlated with elevated levels of ROS and carbonylated proteins, and 190

were accompanied by ultrastructural changes in mitochondria and chloroplasts 191

(Gibala et al., 2009; Kicia et al., 2010). We also found that FTSH4 is significant for 192

assembly/stability of complex I and especially complex V (Kolodziejczak et al., 2007). 193



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More recently, Zhang et al. (2014a) confirmed our observations linking the lack of 194

FTSH4 protease, oxidative stress and alternations in plant development and 195

architecture. These authors also revealed additional non-mitochondrial players such 196

as cytoplasmic peroxidases and auxin homeostasis (Zhang et al., 2014a; Zhang et 197

al., 2014b). They proposed that FTSH4 mediates the peroxidase-dependent interplay 198

between hydrogen peroxide and auxin homeostasis to regulate plant growth and 199

development. 200

In the present study, we compared the mitochondrial proteome and 201

oxyproteome of wild type and ftsh4 mutants grown under conditions inducing the 202

phenotypic alterations in ftsh4 (short days at optimal temperature and long days 203

under continuous moderate heat stress) and found that diverse proteins from various 204

submitochondrial compartments were carbonylated in ftsh4 mitochondria, indicating a 205

widespread oxidative stress. We postulate that this oxidative stress proceeds 206

progressively and is mainly associated with the FTSH4 function to maintain a proper 207

phospholipid content, especially cardiolipin, in the mitochondrial membrane. 208

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RESULTS 228

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ftsh4 Mutants Show Similar Morphological Changes Under Short-Day 230

Photoperiod at Normal Temperature and in Long Days Under Continuous 231

Moderate Heat Stress 232

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Aging ftsh4-1 and ftsh4-2 Arabidopsis plants grown in short days at normal 234

temperature (SD, 22°C) were previously shown to display severe morphological and 235

developmental alterations compared to wild type (Gibala et al., 2009; Kicia et al., 236

2010). In these studies we further demonstrated that the post-germination growth of 237

ftsh4 under long-day photoperiod (LD, 22°C) was not affected. Here, however, we 238

present data indicating that phenotypic abnormalities are noticeable even in LD, 239

when ftsh4 plants were grown at slightly higher temperature than optimal (30°C). 240

Phenotypic features seen under these both regimens are: a significantly reduced 241

rosette size (Gibala et al., 2009; Fig. 1A and 1C), a developmental delay in the 242

appearance of true leaves (Gibala et al., 2009; Fig. 1B) and irregular serration of leaf 243

blades (Gibala et al., 2009, Fig. 1D), the latter two more visible at the end of 244

vegetative growth. These comparable defects suggest similar molecular alterations 245

activated under two specific conditions in the ftsh4 mutant. We denote these 246

conditions as inducing the phenotype. 247

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Mitochondrial Proteome is Altered in ftsh4 Mutants Under Conditions Inducing 249

the Phenotype 250

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To gain insight into molecular alterations activated in ftsh4 mutants in 252

conditions inducing the phenotype we analysed their mitochondrial proteomes using 253

Two-Dimensional Fluorescence Difference Gel Electrophoresis (2D-DIGE). 254

Mitochondrial proteins of 9-week-old ftsh4-1 and wild type plants grown in soil under 255

SD, 22°C as well as 3-week-old ftsh4-1, ftsh4-2 and wild type seedlings grown 256

hydroponically under LD, 30°C were differentially labelled using G-Dyes (NH 257

DyeAGNOSTICS) and subjected to IEF/SDS-PAGE. Thus, three experimental setups 258

were analysed (SD, 22°C for ftsh4-1; LD, 30°C for ftsh4-1 and LD, 30°C for ftsh4-2) 259

and protein spots with fold changes in abundance of greater than ±1.2 (p ≤ 0.05) 260

between ftsh4 and wild type in at least one experimental setup were picked from the 261



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gel and identified by MALDI-TOF (PMF, Peptide Mass Fingerprinting). Overall, 63 262

unique and 3 redundant proteins (serine transhydroxymethyltransferase 1, SHM1 - 263

protein spot numbers 28, 29 and 30; ATP synthase subunit 2, ATP2 - protein spot 264

numbers 6, 7, 8, and 9; heat shock protein 60, HSP60-2 - protein spot numbers 38 265

and 39) with significant Mowse scores were identified and classified into different 266

functional categories (Table I, Supplemental Table S1, and Supplemental Fig. S1). 267

Most of these proteins were common to two tested setups and six were common to 268

all three variants assayed. Four of these common proteins are OXPHOS subunits 269

and two are associated with the TCA cycle. These proteins are indicated in a 270

representative analytical 2D-DIGE gel shown in Supplemental Fig. S2. 271

Collectively, several subunits of complex I and V and the majority of enzymes 272

of the TCA cycle were lower in abundance in mitochondria of FTSH4-deficient plants, 273

while chaperones, antioxidant enzymes and proteins involved in the transport 274

accumulated (Table I). A decrease in abundance of the components of OXPHOS and 275

TCA cycle and induction of expression of proteins that have an antioxidant and stress 276

response function is characteristic for mitochondrial proteomes under sub-lethal 277

doses of oxidative stress (Sweetlove et al., 2002). Thus, the proteomic data indicate 278

that ftsh4 mutants suffer an endogenous oxidative stress. The comparative proteomic 279

analysis revealed also that, in contrast to the several enzymes of amino acid 280

metabolism to be decreased in ftsh4, isovaleryl-CoA dehydrogenase (IVDH), which is 281

involved in the catabolism of branched-chain amino acids and lysine, accumulated in 282

both ftsh4 mutants in LD, 30°C (Table I). Degradation products of these amino acids 283

can provide electrons to the respiratory chain via the ETF complex (Araújo et al., 284

2011). One can assume that in ftsh4 mutants this catabolic pathway compensates for 285

the reduced electron supply from the TCA cycle at least in LD, 30°C. 286

287

Proteins Carbonylated to a Higher Extent in ftsh4 than in Wild Type 288

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Extensive carbonylation of mitochondrial proteins was observed in ftsh4 290

mutants growing under LD, 30°C (Fig. 2B), confirming data on plants grown at SD, 291

22°C (Gibala et al., 2009). To prove a direct and/or indirect role of FTSH4 in 292

preventing accumulation of carbonylated proteins we used a revertant line of ftsh4-1 293

(ftsh4-1-FTSH4) constitutively expressing full-length FTSH4 cDNA under the control 294

of the CaMV 35S promoter. As expected, the level of carbonylated proteins in ftsh4-295



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1-FTSH4 was comparable to that in wild type plants and the revertant plants had lost 296

the morphological aberrations characteristic for ftsh4-1 seedlings in LD, 30°C (Fig. 297

2A and Fig. 2B). 298

To identify the proteins carbonylated in the absence of FTSH4, mitochondrial 299

protein samples isolated from WT and ftsh4 plants grown under conditions inducing 300

the phenotype were first separated according to their pI, derivatized in-gel with 2,4-301

dinitrophenylhydrazine (DNPH), and then resolved by SDS-PAGE. After blotting the 302

membrane was probed with polyclonal anti-DNP-adduct antibodies (Fig. 3). A protein 303

spot was considered to be significantly increased in carbonylation level if the 304

oxidation fold of its immunological signal in ftsh4 to that in the WT gel was ≥1.2. 305

Protein spots found to be increasingly carbonylated in ftsh4 were matched to the 306

corresponding spots in an IEF/SDS-PAGE gel stained with Coomassie and identified 307

by mass spectrometry. The carbonylated proteins accumulating in ftsh4-1 under SD, 308

22°C and in ftsh4-1 or ftsh4-2 under LD, 30°C are listed in the Supplemental Table 309

S2. 310

In total, 26 mitochondrial proteins were more heavily carbonylated in ftsh4 311

than in wild type plants. They represented several functional groups located in 312

different mitochondrial compartments (Supplemental Table S2 and Supplemental Fig. 313

S3). Nine of those 26 proteins were identified in all analyzed conditions: two subunits 314

of complex V (ATP synthase subunit 1, ATP1 and ATP2), two components of the 315

TCA cycle (fumarase 1, FUM1 and succinyl Co-A ligase, SuCoA), three associated 316

with photorespiration (lipoamide dehydrogenase, MTLPD1, aminomethyltransferase, 317

GDC-T and SHM1), a stress-related protein (manganese superoxide dismutase 1, 318

MSD1), and a protease (mitochondrial processing peptidase subunit beta, 319

MPPBETA) (Supplemental Table S2). Furthermore, a number of proteins like 320

aconitase 2 (ACO2), SHM1, GDC-T, ATP1 and ATP2 were found to be more 321

extensively carbonylated in more than one spot on the 2D-OxyBlots. The different 322

spots of ACO2 and SHM1 showed differences in pI, while those of GDC-T, ATP1 and 323

ATP2 - in molecular weight; thus the last three are typical examples of protein 324

degradation products (Supplemental Table S2). 325

However, the proteins identified as carbonylated more strongly in ftsh4 than in 326

wild type plants using the OxyBlot analysis showed diverse changes in abundance as 327

determined by the 2D-DIGE assay, some being up- and some down-regulated (Table 328

I, Supplemental Table S1). Therefore, to find proteins carbonylated to a higher extent 329



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in ftsh4 than in wild type, oxidation indexes were determined for each spot of interest. 330

To calculate the oxidation index, the carbonyl immunoreactivity of each spot was 331

divided by the relative protein abundance estimated by the DIGE analysis 332

(Supplemental Table S3). Regardless of the conditions tested, ACO2 was found to 333

be more heavily carbonylated in ftsh4 compared to wild type plants (Table II, 334

Supplemental Table S3). ACO2 represents a group of proteins with a high oxidation 335

index (≥1) and a decreased protein amount estimated by DIGE (Table II, 336

Supplemental Table S3). This set of proteins includes complex I (75-kDa subunit) 337

and complex V (ATP1, ATP2, and ATP synthase subunit Fad, MGP1) subunits, TCA 338

cycle components (ACO2, SuCoA subunit beta, and malate dehydrogenase 2, 339

MDH2), enzymes of cysteine (cysteine synthase C1, ATCYSC1) and glutamate 340

(glutamate dehydrogenase 2, GDH2) metabolism, and MPPBETA. Analysis of 341

transcript level of these proteins using quantitative PCR (Fig. 4A) indicates that 342

except ATP2 other proteins did not show any decrease in mRNA expression. Thus, it 343

is conceivable that these particular proteins are extensively oxidatively damaged and 344

thus degraded in plants lacking FTSH4. In contrast, the remaining proteins with a 345

high oxidation index were found to accumulate in ftsh4 plants according to 2D-DIGE. 346

This group of proteins comprises an enzyme of the TCA cycle (FUM1), four 347

photorespiration enzymes (GDC-T, SHM1, MTLPD1, and formate dehydrogenase, 348

FDH), glutamate dehydrogenase 1 (GDH1) and a key enzyme in the elimination of 349

mitochondrial superoxide radicals, MSD1. qRT-PCR analyses indicated that 350

accumulation of these proteins is not accompanied with an increase in their transcript 351

level (Fig. 4A). Most transcripts exhibited statistically insignificant changes in ftsh4-1 352

and ftsh4-2 compared to wild type, with a log2 ratio below 0.5. Unexpectedly, the 353

transcript level of GDC-T and SHM1, proteins that accumulate in our experimental 354

conditions in the ftsh4 mutants, substantially decreased (Fig. 4A). 355

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Increased Expression Level of ATP-dependent Proteases in ftsh4 Mitochondria 357

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In yeast and mammals it was shown that carbonylated proteins are removed 359

by ATP-dependent proteases, presumably to avoid formation of harmful aggregates 360

(Anand et al., 2013). Therefore, we examined the expression level of known 361

mitochondrial ATP-dependent proteases in the ftsh4 mutant compared to wild type 362

plants. No significant changes were observed in the expression of mitochondrial 363



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ATP-dependent proteases in ftsh4 plants grown under LD, 22 °C, neither at the 364

transcript nor at the protein level (Fig. 5A). However, under conditions inducing the 365

phenotype, when carbonylated proteins accumulated in mitochondria of ftsh4, we 366

observed a significant increase of FTSH10 protease at the transcript and protein 367

levels, and a higher abundance of FTSH3 at the protein level (Fig. 5A, B and C). The 368

accumulation of LON1 detected by 2D-DIGE agrees with its transcriptional up-369

regulation (Fig. 5A). The abundance of other plant mitochondrial proteases (FTSH11, 370

LON4, CLP) because of a lack of corresponding antibodies was estimated only at the 371

transcript level, which did not change significantly in the ftsh4 mutant compared to 372

wild type plants (Fig. 5A). Taken together, the accumulation of carbonylated proteins 373

under conditions inducing the phenotype in ftsh4 was correlated with elevated 374

expression of at least three ATP-dependent proteases: LON1, FTSH3 and FTSH10. 375

376

ftsh4 Contains a Decreased Abundance and Activity of Complexes I and V as 377

well as an Reduced Intra-mitochondrial Pool of ATP 378

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Previously, using a combination of blue-native polyacrylamide gel 380

electrophoresis (BN-PAGE) and histochemical staining, we have observed that loss 381

of FTSH4 was associated with a decreased abundance and activity of complexes I 382

and V in plants growing in SD, 22°C (Kolodziejczak et al., 2007). Using the same 383

approach we observed reduced amount and activity of complexes I and V in ftsh4-1 384

and ftsh4-2 mutants growing in LD, 30°C as well (Fig. 6B, C). Additionally, a slight 385

(~20%), but statistically significant decrease of activity of the analyzed complexes 386

was also detected in the ftsh4 mutants in LD at 22°C (Fig. 6A, C). Moreover, DIGE 387

analysis confirmed these results; lower amounts of NADH-ubiquinone oxidoreductase 388

75-kDa belonging to complex I, as well as ATP1 and ATP2 of complex V were found 389

in the ftsh4 mutants compared to wild type in all experimental setups (Table I). A 390

clear exception was gamma carbonic anhydrase 2 (CA2), a subunit of complex I, 391

which accumulated in the mutants. Thus, two experimental approaches, BN-PAGE 392

and 2D-DIGE, indicate that FTSH4 is essential for stability/assembly/activity of 393

complexes I and V under conditions inducing the phenotype. 394

We next tested whether this defect in the OXPHOS complexes of ftsh4 is 395

associated with a reduced intra-mitochondrial pool of ATP. Therefore, using a 396

bioluminescence assay, the ATP content was examined in mitochondria obtained 397



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from 3-week-old WT or ftsh4 plants grown under LD, 30°C. The amount of ATP in 398

mitochondria of ftsh4 was approx. 30-40% lower than in wild type (6.42 ± 2.01 for 399

WT, 3.81 ± 1.48 for ftsh4-1 and 4.3 ± 0.72 for ftsh4-2, in pmol/mg of protein; Fig. 6D). 400

This significantly reduced intra-mitochondrial pool of ATP in plants lacking FTSH4 401

protease likely reflects a perturbation in ATP formation due to a defect in 402

stability/activity of complex V. 403

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Availability of ATP Limits Degradation Rate of Carbonylated Proteins in 405

Mitochondria of ftsh4 406

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Given the apparent increase in abundance of ATP-dependent proteases in 408

mitochondria of ftsh4 grown at the phenotype-inducing conditions, it was surprising to 409

note that carbonylated proteins were not efficiently removed. Thus, we hypothesized 410

that in the mutants carbonylated mitochondrial proteins accumulated due to a lack of 411

ATP, required for the proteolytic activity of the ATP-dependent proteases. To test this 412

hypothesis we performed in vitro time-course experiments monitoring the level of 413

carbonylated proteins in mitochondria isolated from 2-week-old seedlings grown 414

under LD, 30°C in the absence or presence of ATP (Fig 7A). Densitometric analyses 415

indicated that the total amount of carbonylated proteins in WT mitochondria 416

significantly decreased (about 40%) when incubated without ATP for 16 h at 22°C, 417

while in ftsh4-1 and ftsh4-2 mitochondria the amount of carbonylated proteins did not 418

change significantly under the same conditions (Fig. 7A). However, in the presence 419

of ATP the amount of carbonylated proteins was strongly diminished in ftsh4 420

mitochondria incubated for 16 h at 22°C, practically exceeding the level observed in 421

wild type sample (Fig. 7A). 422

The same assay was performed on freshly isolated mitochondria from WT and 423

ftsh4 seedlings grown at LD, 22°C, incubated with succinate and antimycin A, an 424

inhibitor of complex III and a well-known inducer of oxidative stress (Fig. 7B). 425

Treatment of ftsh4 mitochondria with antimycin A for 16 h in the absence of ATP 426

resulted in a significant accumulation of carbonylated proteins, while supplementing 427

the incubation medium with ATP induced a strong decrease of oxidatively modified 428

proteins (approx. 60%, Fig. 7B). Addition of AEBSF, an inhibitor of serine proteases, 429

to the medium prevented the carbonylated protein content from decreasing in WT 430

and ftsh4-1, indicating an important contribution of serine proteases in eliminating 431



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oxidatively modified proteins in plant mitochondria (Fig. 7B). No such effect could be 432

observed using ortho-phenanthroline, an inhibitor of metalloproteases (Fig. 7B). 433

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ftsh4 Contains Altered Mitochondrial Morphology and Phospholipid Content 435

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Several recent findings point to an essential role of yeast and mammalian i-437

AAA proteases in the mitochondrial quality control at the organellar level (Stiburek et 438

al., 2012; Li et al., 2015; Qi et al., 2015). To look into a putative role of FTSH4 in 439

plant mitochondrial dynamics, we first examined the mitochondrial morphology of wild 440

type and ftsh4-1 plants grown under LD, 22°C (no visible phenotype) and LD, 30°C 441

(visible phenotype), transformed with a construct expressing mitochondria-targeted 442

green fluorescent protein (GFP) under the control of the CaMV 35S promoter. 443

Analysis of confocal microscopy photographs revealed the existence of a 444

heterogeneous mitochondrial population in ftsh4-1 protoplasts compared to WT (Fig. 445

8A). This heterogeneous population was characterized by the appearance of 446

enlarged, spherical mitochondria, termed “giant” mitochondria, among healthy, oval 447

forms (Fig. 8A). While the giant mitochondria were rare in ftsh4-1 protoplasts isolated 448

from plants grown at 22°C, their number and area were highly increased, when the 449

plants were exposed to the moderately elevated temperature of 30°C (Fig. 8A). In 450

addition, some of giant mitochondria displayed GFP voids, with reduced or absent 451

fluorescence signal, the feature characteristic for oxidative stress (Fig. 8A) (Logan et 452

al., 2003). Even mitochondrial enlargement was reported to be caused by oxidative 453

stress (Scott and Logan, 2008), but also by depletion of cardiolipin (CL), a signature 454

phospholipid of mitochondria (Pineau et al., 2013; Pan et al., 2014). To investigate, if 455

the aberrant mitochondrial morphology observed in ftsh4 plants is associated with 456

perturbed cardiolipin abundance, we determined the lipid composition of 457

mitochondrial membranes in WT and ftsh4 mutants grown under LD, 22°C and LD, 458

30°C using a comparative quantitative lipidomic approach (shotgun lipidomics) (Fig. 459

8B). Figure 8B shows quantification of CL and lipids involved in this phospholipid 460

biosynthesis (PA, phosphatidic acid; DAG, diacylglycerol; PI, phosphatidylinositol; 461

PG, phosphatidylglycerol) as well as the most abundant lipids of mitochondrial 462

membrane (PC, phosphatidylcholine; PE, phosphatidylethanolamine). The 463

quantitative analysis of all identified lipid classes is presented in Supplemental Fig. 464

S4. Our results indicate that the level of cardiolipin was slightly decreased in 465



15

mitochondria of ftsh4 plants grown under LD, 22°C. This effect was more pronounced 466

under LD, 30°C, compared to wild type (Fig. 8B). Additionally, we detected an 467

accumulation of phosphatidyloglicerol (PG) in ftsh4 mitochondria under LD, 22°C, 468

which was stronger under LD, 30°C. Furthermore, the levels of phosphatidyloinositol 469

(PI) and diacyloglicerol (DAG) in ftsh4 were slightly increased (Fig. 8B). It should be 470

emphasized that DAG, PI and PG are involved in the cardiolipin biosynthesis 471

pathway, and possibly their accumulation in ftsh4 mitochondria is related to the 472

deficiency of CL; similar changes of the PG level were observed in an Arabidopsis 473

mutant disrupted in the single-copy gene encoding cardiolipin synthase (Pan et al., 474

2014). While no significant difference was observed in the amount of 475

phosphatidyloethanolamine (PE) in wild type and ftsh4 grown at LD, 22°C, ftsh4 476

plants grown at LD, 30°C had lower level of PE in their mitochondrial membranes 477

(Fig. 8B). This effect might reflect a complex regulation of the phospholipid level, 478

since both CL and PE are known to be involved in similar processes in mitochondrial 479

membranes (Joshi et al., 2012; Böttinger et al., 2012). Taken together, these results 480

demonstrate that FTSH4 protease affects the abundance of cardiolipin, and in turn 481

mitochondrial dynamics. 482

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DISCUSSION 499

500

In this study, we show that loss of the FTSH4 mitochondrial protease under 501

conditions inducing the phenotype leads to oxidative damage of many mitochondrial 502

proteins different in function and submitochondrial localization. We believe that the 503

main cause of this phenotype is altered content of cardiolipin in the mitochondrial 504

membrane, associated with perturbation of at least two processes: functionality of the 505

OXPHOS system and mitochondrial dynamics. Deregulation of these processes 506

disturbs the mitochondrial quality control on molecular and organellar level, and leads 507

to the accumulation of oxidatively damaged proteins (Fig. 9). In other words, we 508

argue here that the accumulation of carbonylated proteins found in ftsh4 plants is due 509

to their more intensive generation, an ineffective system for their removal by ATP-510

dependent proteases and an altered system of mitochondrial 511

fusion/fission/mitophagy. 512

513

Diverse Mitochondrial Proteins Undergo Carbonylation in ftsh4 Grown Under 514

Conditions Inducing the Phenotype 515

516

We previously reported that ageing ftsh4 plants growing in SD, 22°C, 517

experienced oxidative stress (Gibala et al., 2009, Kicia et al., 2010). We have now 518

extended those studies by identifying the proteins to be excessively carbonylated in 519

ftsh4 and linking their oxidation status with their abundance estimated by 2D-DIGE 520

(Tables I and II). These experiments were not limited to ftsh4 growing under SD, 521

22°C, but similar analysis was also performed for ftsh4-1 and ftsh4-2 growing under 522

LD, 30°C. Diverse proteins from the OXPHOS system, TCA cycle, and 523

photorespiration, as well as manganese superoxide dismutase and cysteine synthase 524

were found to be more excessively carbonylated in the mutant than in wild type 525

mitochondria (Table II). It should be emphasized that all the oxidatively damaged 526

proteins identified in ftsh4 have been reported earlier as targets for carbonylation in 527

plant mitochondria (Kristensen et al., 2004; Smakowska et al., 2014). Those proteins, 528

which were predominantly carbonylated in the absence of FTSH4, were also 529

identified by 2D-DIGE analyses, and found to be differentially expressed compared to 530

the wild type mitochondrial proteome (Table I). A decrease in abundance was 531

observed for two enzymes of the TCA cycle (ACO2 and SuCoA), two subunits of 532



17

complex V (ATP1 and ATP2) and the 75-kDa subunit of complex I, while fumarase 533

and two enzymes of photorespiration (GDC-T and MTLPD1) showed increased 534

abundance (Tables I and II). The lower abundance and enhanced carbonylation of 535

complex I and V subunits in mitochondria from ftsh4 were presumably caused by a 536

defect in their assembly/stability (Kolodziejczak et al., 2007). This defect may 537

increase the pool of unassembled/misfolded proteins, which will undergo 538

carbonylation and subsequent degradation. We believe that in ftsh4 the breakdown 539

of ATP1 and ATP2, ACO2 and SuCoA occurs to a certain degree after oxidation, 540

particularly since the level of their transcripts did not decrease significantly (Fig. 4). 541

The question arises as to why the carbonylated enzymes FUM1, GDC-T, 542

MTLPD1, in contrast to carbonylated ATP2 or ACO2, are present in higher 543

abundance in ftsh4 (Table II). In light of the report showing that chloroplast FTSH 544

proteases degrade functionally assembled proteins that have undergone oxidation 545

(Lindahl et al., 2000), it seems likely that FTSH4 fulfills a similar function in 546

mitochondria and its loss causes accumulation of its substrates - a specific set of 547

highly carbonylated proteins. However, there is a topological incompatibility: the 548

catalytic domain of FTSH4 protease faces the intermembrane space, while GDC-T, 549

MTLPD1 and FUM1 are matrix proteins. At this stage, we do not know how to explain 550

this observation. 551

552

ftsh4 Displays Altered Metabolic Pathways As a Response to Oxidative Stress 553

554

The ftsh4 mutant seems to provide protection against the oxidizing conditions 555

in mitochondria at several levels. Induction of non-phosphorylating alternative 556

pathways is indicated by increased transcription of the genes encoding AOX1A, 557

NDB2 and NDB4 (Fig. 4B). These pathways are known to play an essential role in 558

the response of plant mitochondria to oxidative stress mainly by preventing the 559

overreduction of the mitochondrial electron transport chain and thus the production of 560

ROS (Moller, 2001; Vanlerberghe, 2013). Furthermore, the obvious up-regulation of 561

isovaleryl-CoA dehydrogenase at the transcript and protein level (Fig. 4A, Table I) 562

suggests another non-classical entry route of electrons to the respiratory chain to be 563

activated, provided by the catabolism of branched-chain and aromatic amino acids 564

(Araújo et al., 2010). This makes sense in the light of the elevated amino acids poll 565

generated by degradation of carbonylated proteins in the ftsh4 mutant. The activation 566



18

of this pathway by oxidative stress was reported earlier by Lehmann et al. (2009). 567

Using 2D-DIGE we further confirmed our earlier findings (Gibala et al., 2009) that 568

mitochondrial chaperones are accumulating in the ftsh4 mutant (Table I). The up-569

regulation of HSP70 and HSP60 chaperones on transcript and protein level in ftsh4 is 570

consistent with their protective roles against aggregation of mitochondrial proteins 571

under oxidative stress conditions (Table I, Fig. 4A) (Bender et al., 2011). 572

573

In ftsh4 the Defective OXPHOS System is Linked to Enhanced Generation of 574

ROS and Carbonylated Proteins 575

576

The increase in steady-state level of ROS observed in ftsh4 plants under 577

conditions inducing the phenotype (Gibala et al., 2009, Kicia et al., 2010) is leading in 578

consequence to the generation of carbonylated proteins. The trigger of the oxidative 579

stress observed in ftsh4 most likely is the dysfunctional assembly/stability/activity of 580

complex I and V under conditions inducing the phenotype (Kolodziejczak et al., 2007, 581

Fig. 6B and C). Under optimal conditions (LD, 22°C) these alterations were mild (Fig. 582

6A), but with time (late phase of vegetative growth in SD, 22°C) or under conditions 583

with a higher probability of electron leakage like moderate heat stress (LD, 30°C), 584

harmful overproduction of ROS occurs. Defects in the OXPHOS system caused by 585

the absence of FTSH4 could be explained by at least two not mutually excluding 586

mechanisms: i) The lack of chaperone-like activity of FTSH4 protease required for 587

the formation/stability of complex I and V and ii) the low level of membrane CL 588

documented in this study (Fig. 8). It is well known that CL is a structural component 589

of many protein complexes and supercomplexes of the inner mitochondrial 590

membrane in yeast, human and in plant mitochondria (Pfeiffer et al., 2003; Petrosillo 591

et al., 2007; Pineau et al., 2013; Gonzalvez et al., 2013). Reduced content of the 592

respiratory complex I/complex III supercomplex and to a lesser extent complex I was 593

found in an Arabidopsis thaliana knock-out mutant depleted in the final enzyme of the 594

cardiolipin biosynthesis (Pineau et al., 2013) 595

The results presented here suggest also that extended oxidative stress in 596

ftsh4 creates other additional sources of ROS, which further accelerate this stress. 597

Oxidatively damaged iron-sulfur proteins like aconitase or the 75-kDa subunit of 598

complex I could accelerate oxidative stress by the Fenton reaction (Moller et al., 599

2011). The finding of several mitochondrial enzymes of photorespiration being highly 600



19

carbonylated (GDC-T, SHM1 and MTLPD1), combined with the decreased 601

abundance of other photorespiration enzymes (GLDP1 and GLDP2) suggests that 602

this process is at least slowed down in ftsh4 mitochondria (Tables I and II). Since 603

photorespiration is considered to be important to prevent ROS accumulation (Voss et 604

al., 2013), the postulated decreased activity of the GDH/SHMT complex could be an 605

additional cause for oxidative stress in ftsh4. Furthermore, among the proteins 606

carbonylated preferentially in ftsh4 is the manganese superoxide dismutase, a key 607

enzyme to eliminate mitochondrial superoxide radicals (Wang et al., 2010). This 608

enzyme is probably inactive in ftsh4 due to oxidative modification (Qin et al., 2009) 609

and it was found to be highly carbonylated in all the conditions examined (Table II). 610

611

In ftsh4 the Defective OXPHOS System is Linked to Limited ATP-dependent 612

Degradation of Carbonylated Proteins 613

614

The protease responsible to degrade oxidatively damaged matrix proteins in 615

yeast (Bender et al., 2011; Bayot et al., 2010) and mammalian mitochondria (Bota 616

and Davies, 2002) is the ATP-dependent Lon protease. However, recent studies 617

indicate in Arabidopsis the mitochondrial LON1 protease to be nonessential for the 618

turnover of oxidized proteins (Solheim et al., 2012). Nevertheless, in the absence of 619

FTSH4 we observed overexpression of mitochondrial ATP-dependent proteases, 620

potentially able to degrade oxidized proteins, at the transcriptional (LON1 and 621

FTSH10) and protein (FTSH3) levels (Fig. 5). Curiously, despite this increased 622

expression of ATP-dependent proteases, we documented that degradation of 623

carbonylated proteins in mitochondria isolated from ftsh4 was less efficient than in 624

wild type in the absence of ATP, but similar to wild type after addition of ATP (Fig. 7). 625

Using respective inhibitors we could support a previous study (Sweelove et al., 2002) 626

showing serine proteases to be mainly responsible for the degradation of oxidatively 627

modified proteins in plant mitochondria (Fig. 7). Thus, the accumulation of 628

carbonylated proteins in ftsh4 seems to be caused by limited ATP-dependent 629

proteolytic capacity in ftsh4 mitochondria. The lower ATP content found in ftsh4 630

mitochondria compared to wild type (Fig. 6D) most probably results from impaired 631

efficiency of the OXPHOS system, particularly the substantially decreased activity of 632

the ATP synthase. 633



20

Decreased Level of CL induces Giant Mitochondria and Accumulation of 634

Carbonylated Proteins in ftsh4 635

636

One of the most exciting conclusions rationalizing the accumulation of 637

carbonylated proteins in ftsh4 is based on the observation of giant mitochondria and 638

on CL deficiency in the mitochondrial membrane in the absence of FTSH4 (Fig. 8A 639

and B). In Arabidopsis, CL deficiency has previously been linked to restricted fission, 640

which in turn causes the appearance of giant mitochondria (Pan et al., 2014). 641

Ongoing cycles of fusion and fission of mitochondrial membranes are essential for an 642

efficient defense against mitochondrial damage (Tatsuta and Langer, 2008). 643

Furthermore, in animals it was documented that giant mitochondria block mitophagy, 644

the elimination of damaged mitochondria (Zhang et al., 2014c). Thus, we postulate 645

that in mitochondria of ftsh4 carbonylated proteins are not removed efficiently, not 646

only because of the limited capacity of the ATP-dependent proteolytic system, but 647

also because of a restricted fission/mitophagy (Fig. 9). 648

It is well documented that the proteolytic activity of FTSH4 homologues in 649

yeast and mammalian is controlling the accumulation of key mitochondrial 650

phospholipids by turn-over of the phospholipid regulators (Potting et al., 2010; Potting 651

et al., 2013). In yeast, the proteins Ups1 and Ups2 in the intermembrane space act 652

as central regulators of mitochondrial phospholipid homeostasis. The turnover of 653

Ups2 is mediated by the i-AAA protease Yme1, whereas Ups1 is degraded by Yme1 654

and the metallopeptidase Atp23. Our results point to FTSH4 being a part of a 655

regulatory pathway that influences the abundance of CL in plant mitochondria. It 656

seems that this pathway is at least to some extent similar to that discovered in yeast, 657

given that in the Arabidopsis genome there is a homologue of the Ups1 protein 658

(At5g13070), while a homologue of Ups2 has not yet been found. 659

660

Conclusions 661

662

Overall, the presented results indicate that the plant protease FTSH4 663

suppresses oxidative damage in mitochondrial proteins indirectly by controlling the 664

abundance of cardiolipin, a key phospholipid within the mitochondrial membrane. 665

Availability of CL has previously been shown to stabilize respiratory complexes and 666

mitochondrial dynamics. Our findings indicate that both of these processes are 667



21

impaired in mitochondria lacking FTSH4 and in consequence plants suffer oxidative 668

stress. Although we have been unable to identify carbonylated proteins as direct 669

substrates for FTSH4, we believe this protease could functionally resemble 670

chloroplastic FTSH in this respect (Lindahl et al., 2000), but in different 671

developmental stages and/or environmental conditions than used in our work. 672

673

674

675

676

677

678

679

680

681

682

683

684

685

686

687

688

689

690

691

692

693

694

695

696

697

698

699

700

701



22

MATERIALS AND METHODS 702

703

Plant Material and Growth Conditions 704

Arabidopsis thaliana wild type and T-DNA insertion lines were of the Columbia-0 705

(Col-0) ecotype. The transgenic lines ftsh4-1 (SALK_035107/TAIR) and ftsh4-2 706

(GABI_103H09/TAIR) were obtained from the Salk Institute and the Max Planck 707

Institute for Breeding Research, respectively. The lines were previously characterized 708

in Gibala et al. (2009). Plants were grown in growth chambers in a 16 h light/8 h dark 709

(long day, LD) photoperiod at 22°C and 30°C for 2 or 3 weeks (agar plates or 710

hydroponic culture) as well as in soil in a 8 h light/16 h dark (short day, SD) 711

photoperiod at 22°C for 9 weeks and for 4 weeks in LD at 22°C or 30°C, with a light 712

intensity of 150 μmol m-2 s-1. 713

714

Isolation of Mitochondria 715

Isolation of mitochondria from 9-week-old rosettes was performed as described by 716

Urantowka et al. (2005), and from the seedlings as described by Day et al. (1985). 717

Purified mitochondrial fractions were resuspended in a final wash buffer at a 718

concentration of 10 to 20 mg of mitochondrial protein/ml. The protein concentration 719

was determined using the DC Protein Assays (Bio-Rad, Hercules, California, USA). 720

721

Protein Leaf Extracts 722

Total protein extract was obtained from 3-week-old hydroponic cultures as described 723

by Martinez-Garcia et al. (1999). Protein concentration was determined using the DC 724

Protein Assay. 725

726

Immunoblot Analysis 727

Equal amounts of proteins from wild type (WT) and ftsh4 plants (25 μg per line) were 728

separated by SDS-PAGE according to Laemmli (1970). After electrophoresis, 729

proteins were transferred to PVDF membrane and immunostained with appropriate 730

antibodies. The antibodies used were purchased from Agrisera: anti-AtFTSH10 731

(AS07 251, Sweden) and anti-AtFTSH3 (AS07 204, Sweden) (Piechota et al., 2010). 732

Immunodetection was performed using the WesternBrightTM Quantum Western 733

Blotting Detection Kit (Advansta, Menlo Park, California, USA). The membranes were 734

documented using a chemiluminescence imager (G-BOX ChemiXR5, Syngene) and 735



23

the optical density of the bands was quantified using the Image Quant software 736

(Molecular Dynamics, Sunnyvale, California, USA). 737

738

BN-PAGE and Catalytic Staining 739

Blue-native gel electrophoresis (BN-PAGE) was performed as described by 740

Kolodziejczak et al. (2007). The catalytic staining of mitochondrial complex I and 741

supercomplex I + III2 was carried out according to Zerbetto et al. (1997), while the 742

staining of complex V according to Van Lis et al. (2003). 743

744

Two-Dimensional Fluorescence Difference Gel Electrophoresis (2D-DIGE) 745

For 2D-DIGE analysis mitochondrial proteins from wild type and mutant (ftsh4-1 and 746

ftsh4-2) were precipitated with cold acetone for 2 h at -20°C and pelleted at 18000 g 747

and 4°C for 30 min. Mitochondrial protein pellets were resuspended in lysis buffer (8 748

M urea, 4% w/v CHAPS, 50 mM DTT, 40 mM Tris-HCl, pH 7.5) at a concentration of 749

10 mg of mitochondrial protein/ml and vortexed for 30 min at 4°C. The non-soluble 750

material was removed by centrifugation at 18000 g for 20 min. Each 25 μg of 751

biological replicate sample was labeled with 0.1 nmol G-Dyes (G-200 or G-300, 752

DyeAgnostics, Halle, Germany) on ice for 30 min in the dark according to 753

manufacturer’s instruction. The reaction was stopped with 1 nmol of lysine. A G-100 754

stained sample (25 μg of mitochondrial proteins), composed of equal amounts of wild 755

type and ftsh4-1 or ftsh4-2 mitochondrial protein extracts, constituted an internal 756

standard (IS) used for normalization of 2D-DIGE gels. 25 μg aliquots of each 757

differentially labeled mitochondrial sample (G-100-, G-200- and G-300-labelled 758

sample) were pooled, mixed with rehydration solution (7 M urea, 2 M thiourea, 2% 759

CHAPS, 20 mM DTT, 0.6% IPG buffer 3-11 NL (GE Healthcare, Uppsala, Sweden)) 760

and loaded on a 24-cm, pH 3-11 NL Immobiline DryStrip (GE Healthcare). 761

Rehydration of the strips and first dimension electrophoresis (isoelectric focusing, 762

IEF) were conducted in an Ettan IPGphor Isoelectric Focusing System (GE 763

Healthcare) at 50 V for 12 h (rehydration), 500 V for 3 h (step), 2000 V for 2 h (step), 764

8000 V for 1 h (gradient), 8000 V for 10 h (step) at a maximum setting of 50 μA per 765

strip. After IEF, the strips were equilibrated for 15 min in the equilibration buffer (6 M 766

urea, 30% glycerol, 50 mM Tris-HCl (pH 8.8.), 2% w/v SDS, trace of bromophenol 767

blue) supplemented with 65 mM dithiothreitol and then for a further 15 min in the 768

same buffer with 135 mM iodoacetamide. The strips were laid on top of 12.5% w/v 769



24

polyacrylamide gels (26 x 20 cm) and sealed with 0.5% agarose in 25 mM Tris-HCl, 770

192 mM glycine, 0.2% SDS. Second dimension electrophoresis was performed 771

overnight in an Ettan Dalt II electrophoresis unit (GE Healthcare) at 20°C and 1 W 772

per gel. After electrophoresis the gels were scanned with a Typhoon 9400 scanner 773

(GE Healthcare) at the excitation wavelengths corresponding to each of the G-Dyes. 774

The images of the gels from three independent biological repetitions were analysed 775

using DeCyder software version 6.5 (GE Healthcare) for normalization and statistical 776

analysis. Protein spots that showed a significant difference in abundance (fold 777

difference ±1.2, p 0.05) between ftsh4 and wild type were picked from the gel and 778

identified by MALDI-TOF (PMF, Peptide Mass Fingerprinting). In this approach three 779

experimental setups were analyzed (SD, 22°C for ftsh4-1; LD, 30°C for ftsh4-1 and 780

LD, 30°C for ftsh4-2) in three independent biological replicates. 781

782

Detection of Carbonylated Proteins on One-Dimensional gels 783

Carbonylated proteins were detected and analyzed following derivatization of protein 784

carbonyl groups with 2,4-dinitrophenylhydrazine (DNPH), using the OxyBlot kit 785

(Millipore, Billerica, California, USA). Immunodetection was performed with a primary 786

antibody directed against dinitrophenylhydrazone using 25 μg of total protein extract 787

or 30 μg mitochondrial proteins from ftsh4 and WT plants per lane. The carbonylated 788

proteins were visualized with the WesternBrightTM Quantum Western Blotting 789

Detection Kit. 790

791

Two-Dimensional OxyBlots 792

Mitochondrial protein extracts (150-200 μg) of wild type, ftsh4-1 and ftsh4-2 lines 793

were prepared as described above. After IEF, the strips were frozen at -80°C for 2 h. 794

Derivatization of protein carbonyl groups was done by incubation of the strips in a 795

buffer containing 2 M HCl and 10 mM 2,4-dinitrophenylhydrazine for 20 min at room 796

temperature. Derivatized proteins were neutralized by repeated incubation of the 797

strips in a solution of 2 M Tris base and 30% glycerol (v/v) for 20 min at room 798

temperature. Afterwards, the strips were equilibrated and proteins were resolved on 799

second-dimension gels as described above. After electrophoresis, proteins were 800

electrotransferred onto a PVDF membrane (Bio-Rad) and subjected to 801

immunodetection of carbonyl groups using the OxyBlot kit (Millipore). 802

Immunodetection was performed with a primary antibody directed against 803



25

dinitrophenylhydrazone and the Amersham ECL Prime Western Blotting Detection 804

system (GE Healthcare). 805

Quantitative Analysis of Two-Dimensional OxyBlots 806

Protein spots on two-dimensional OxyBlots were quantified using ImageJ Fiji 807

software (Fiji). For different experimental setups and type of sample (WT, ftsh4-1 and 808

ftsh4- 2), each spot was quantified and normalized to the total background intensity 809

of each OxyBlot. Then, the ftsh4/WT oxidation ratio was calculated for each spot. 810

Standard deviation (SD) was calculated and statistical significance was assessed 811

using Student’s t-test for three independent experiments (n=3) for each experimental 812

setup (ftsh4-1/WT, LD, 30°C; ftsh4-2/WT, LD, 30°C; ftsh4-1/WT, SD, 22°C). 813

Oxidation indexes were calculated as the ratio between oxidation fold and protein 814

abundance fold (oxidation fold/protein fold) obtained by 2D-DIGE for each spot of 815

interest. 816

817

Mass Spectrometry and Protein Identification 818

For protein identification, 150 μg of protein sample consisting of equal amounts of 819

wild type and ftsh4 mitochondrial protein extracts was run on preparative SDS gels. 820

The gels were stained with colloidal Coomassie and protein spots showing significant 821

difference in abundance between samples were manually or automatically excised 822

from the gels with an Ettan Spot Picker (GE Healthcare). Gel pieces were washed 823

briefly with deionized water and incubated for 1 h in a solution of 35% acetonitrile 824

(ACN) and 20 mM NH4HCO3. Two further washes (each 10 min) were performed with 825

100% ACN to dehydrate the gels. In-gel protein digestion was performed with 5 ng/μl 826

trypsin (Promega V5111, Madison, USA) in 20 mM NH4HCO3/10% ACN overnight at 827

37°C. The peptides were extracted with 1% trifluoroacetic acid (TFA) for 30 min at 828

room temperature and occasional shaking. A volume of 1 μl of peptide mixture was 829

spotted on an ABI-PerSpective Voyager DE STR MALDI plate (Applied Biosystems, 830

Foster City, California, USA) covered with 1 μl of alpha-cyano-4-hydroxycinnamic 831

acid (HCCA) as a matrix in a solution of 50% ACN and 0.1% TFA. Peptide mass 832

fingerprints (PMFs) of the samples were acquired using a Voyager-DE STR MALDI-833

TOF (Applied Biosystems) mass spectrometer. Peptide calibration standard mixture 834

in the mass range 800-4000 Da (Sequazyme, Applied Biosystems Siex) was used for 835

calibration of the mass spectrometer. The PMFs were searched against the 836

Arabidopsis Information Resource (TAIR) database. The fixed and variable 837



26

modifications were cysteine carbamidomethylation and methionine oxidation, 838

respectively, with the maximum number of missed cleavages of 2. Peptide mass 839

precision tolerance error was set to 100 ppm. Proteins were identified with the 840

VoyagerTM 5 Software (Applied Biosystems) using the Mascot 2.3 search engine 841

(Matrix science, www.matrixscience.com). 842

843

RNA Isolation and cDNA Synthesis 844

Total RNA was isolated from 3-week-old hydroponically grown seedlings and rosettes 845

of plants grown in soil for approximately 9 weeks using the GeneMATRIX Universal 846

RNA Purification Kit (EURx, Gdansk, Poland). The reverse transcription reaction was 847

performed using up to 2 μg of total RNA and a reverse transcription kit (Applied 848

Biosystems). Resulting cDNA was used as a template for quantitative real-time PCR. 849

850

Real-Time PCR Analysis 851

Real-time PCR analyses were performed in a LightCycler 2.0 instrument (Roche 852

Applied Science, Mannheim, Germany). Real-Time 2x PCR Master Mix SYBR 853

version B (A&A Biotechnology, Gdynia, Poland) was used. Reactions were carried 854

out in a total volume of 15 μl with a final concentration of 0.5 μM primers. Material 855

from wild type plant served as the calibrator, and the PP2AA3 (protein phosphatase 856

2A subunit A3) gene (At1g13320) was used as a reference. The values of 857

amplification efficiency of the analysed amplicons were calculated based on standard 858

curves generated for serial 2-fold dilutions of the cDNA samples. The amplification 859

protocol comprised: denaturation, 95°C for 1 min; amplification, 45 cycles at 95°C for 860

10 s, 55-65°C (the annealing temperature was specific for primers used) for 10 s, 861

72°C for 20 s with single data acquisition; cooling, 40°C for 30 s. The specificity of 862

the amplification products was verified by melting curve analysis. The primers used 863

are listed in Supplemental Table S4. 864

865

Plasmid Construction 866

The original FTSH4 cDNA was cloned in pTZ57 R/T vector (ThermoFisher Scientific, 867

Carlsbad, Massachusetts, USA), sequenced and recloned into pENTRTM/D-TOPO® 868

(ThermoFisher Scientific) using primes described in Supplemental Table S4. In the 869

second step of cloning by the Gateway method FTSH4 was introduced under CaMV 870

35S promoter to the destination vector pGWB514 (a kind gift from Dr. Tsuyoshi 871



27

Nakagawa, Nakagawa et al., 2007) containing the HA-tag at the C-terminus. The final 872

construct was subjected to the complementation analysis. 873

874

Agrobacterium-Mediated Transformation of A. thaliana 875

The pGWB514 plasmid was introduced into Agrobacterium tumefaciens strain 876

LBA4404 by electroporation. The obtained bacterial strain was used for the floral dip 877

vacuum infiltration of the ftsh4-1 mutants as described by Desfeux et al. (2000). 878

Transformants were checked for complementation of the developmental defects 879

under appropriate conditions. 880

881

Lipidomic analysis 882

Lipid extraction, mass spectrometric analysis and data analysis were done by 883

Lipotype GmbH (Germany). For shotgun lipidomics, lipids were extracted with 884

chloroform and methanol from either mitochondria isolated from WT, ftsh4-1 and 885

ftsh4-2 2-week-old seedlings or leaf homogenates as described in Sampaio et al. 886

2011. Samples were spiked with known amounts of lipid class-specific internal 887

standards prior to extraction and lipid extracts were subjected to mass spectrometric 888

analysis. Mass spectra were acquired on a hybrid quadrupole/Orbitrap mass 889

spectrometer (Q-Exactive, ThermoFisher Scientific) equipped with an automated 890

nano-flow electrospray ion source (Triversa Nanomate, Advion, Ithaca, New York, 891

USA) in both positive and negative ion mode. Lipid identification using Lipotype 892

Xplorer was performed as previously described (Herzog et al. 2011; Herzog et al. 893

2012). Precursor ion intensity values from mass spectra were normalized to 894

intensities of their respective internal standards to obtain pmol values. These values 895

were converted to mol% (mole fraction), to show the stoichiometric relationship 896

between lipids. 897

898

Plant Protoplast Isolation and Confocal Imaging 899

Protoplasts were isolated from leaves of 4-week-old WT and ftsh4-1 plants grown in 900

soil under LD, 22°C and LD, 30°C, and expressing mitochondria-targeted green 901

fluorescent protein (GFP) under the control of the CaMV 35S promoter, using the 902

method described by Yoo et al. (2007). In order to target GFP into mitochondria, the 903

N-terminal targeting sequence from the gene encoding mitochondrial F1F0 ATP 904

synthase delta subunit was used (Sakamoto and Hoshino, 2004). The images of 905



28

protoplasts were acquired using a Zeiss LSM510 confocal laser scanning microscope 906

equipped with a 40x water immersion objective. The GFP signal was visualized with 907

a 488-nm argon laser and a BP505-530 filter. 908

909

In Vitro Mitochondrial Protein Degradation Assay 910

To test the rate of degradation of carbonylated proteins in mitochondria of WT and 911

ftsh4 mutants, the freshly isolated mitochondria (30 µg) from 2-week-old seedlings 912

grown in LD, 30°C on agar plates were resuspended in a washing buffer (0.3 M 913

sucrose, 10 mM TES, pH 7.5) and incubated for 16 h at 22°C with or without 3.5 mM 914

ATP. In order to induce an oxidative stress, mitochondria obtained from seedlings 915

grown in LD, 22°C were resuspended in a washing buffer containing 8 µM antimycin 916

A and 5 mM succinate and incubated for 16 h at 22°C in the presence or absence of 917

3.5 mM ATP. For protease inhibitor assays, the inhibitors of serine proteases (2 mM 918

AEBSF, Sigma, St. Louis, USA) and metalloproteases (25 mM ortho-phenanthroline, 919

Sigma) were added into the incubation medium and the mitochondrial protein 920

samples were incubated under the same conditions. After the incubation, the 921

samples were centrifuged for 10 min at 21000 g and 4°C and the mitochondrial 922

pellets were further analysed for protein carbonylation by immunodetection with anti 923

DNP-antibodies using the OxyBlot kit (Millipore). The densitometry analyses of the 924

carbonylated proteins were performed using ImageJ Fiji software (Fiji). 925

926

Measurement of Mitochondrial ATP 927

The ATP amounts in mitochondria of WT and ftsh4 plants were calculated from an 928

ATP standard curve using the ATP Determination Kit (ThermoFisher Scientific), 929

following the manufacturer’s instructions. The measured mitochondrial ATP content 930

was expressed as pmol/mg of mitochondrial protein. Mitochondria were isolated in 931

sterile conditions from 3-week-old seedlings grown in LD, 30°C. Statistical analysis of 932

differences between the ATP amounts was performed by unpaired two-tailed Student 933

t-test. 934

935

936

937

938

939



29

Supplemental Data 940

The following materials are available in the online version of this article. 941

942

Supplemental Figure S1. Proportion, number and functional categories of 943

mitochondrial proteins differing in abundance between ftsh4 and wild type 944

Arabidopsis plants growing under different conditions inducing the phenotype. 945

946

Supplemental Figure S2. Representative differential 2D IEF/SDS-PAGE gel of 947

ftsh4-1 versus wild type mitochondrial proteins from plants grown in LD, 30°C. 948

949

Supplemental Figure S3. Proportion, number and functional categories of identified 950

mitochondrial carbonylated proteins in the ftsh4 mutants. 951

952

Supplemental Figure S4. Total lipid content and classes in mitochondria of WT, 953

ftsh4-1 and ftsh4-2 grown under optimal (22°C) and moderately elevated temperature 954

(30°C) determined by mass spectrometry (Shotgun lipidomics). 955

956

Supplemental Table S1. Identification of proteins differentially abundant in ftsh4-1 957

and ftsh4-2 in comparison to WT in 2D-DIGE. 958

959

Supplemental Table S2: Identification of carbonylated proteins accumulating in 960

ftsh4-1 and ftsh4-2 in comparison to WT in 2D-OxyBlot analysis. 961

962

Supplemental Table S3. Protein abundance, oxidation folds and oxidation indexes 963

estimated for all tested experimental setups (LD, 30°C for ftsh4-1, ftsh4-2 and SD, 964

22°C for ftsh4-1). 965

966

Supplemental Table S4. Primers used for qRT-PCR. 967

968

Supplemental Table S5. Primers used for plasmid construction, cloning and 969

genotyping. 970

971

972

973



30

Acknowledgements 974

975

We thank Dr. Harald Aigner (Dept. of Chemistry, Umeå University, Sweden) for help 976

in designing and performing 2D-DIGE analyses. 977

978

We thank Dr. Michal Surma (Lipotype GmbH, Dresden) for help, advice and 979

discussion concerning lipidomic analysis. 980

981

The Proteomics Facility of the Chemical Biological Centre of Umeå University 982

provided the facilities for performing the 2D-DIGE experiment and the MALDI-TOF 983

mass spectrometry analyses. 984

985

986

987

988

989

990

991

992



31

Table I. Comparative DIGE analysis of the Arabidopsis ftsh4 mitochondrial proteomes. Protein spots with abundances 993 differing between ftsh4 and WT were identified by PMF. 994 995

Protein spot

number

Accession

number (TAIR)

Name of the protein

Statistical analysis

2D-DIGE LD 30°C

2D-DIGE SD 22°C

OXPHOS

ftsh4-1/ WT*

p value ftsh4-2/ WT*

p value ftsh4-1/ WT*

p value

Complex I 1 ATMG00510.1 NADH dehydrogenase subunit 7 (NAD7)

[2.03] [0.02] 1.48 0.04

2 AT5G37510.1 NADH-ubiquinone oxidoreductase subunit 75 kDa -1.5 0.03 -1.67 0.01 -3.04 0

3 AT1G47260.1 Gamma carbonic anhydrase 2 (CA2) 2.08 0 2.78 0.04 1.98 0.01

4 AT5G66510.1 Gamma carbonic anhydrase 3 (CA3) -1.44 0.04 -1.29 0.02

ATP synthase 5 ATMG01190.1 ATP synthase subunit alpha (ATP1)

-1.6 0 -1.49 0.02 -2.01 0.02

6 AT5G08670.1 AT5G08690.1 AT5G08680.1

ATP synthase subunit beta (ATP2)

-1.26

0.01

-1.48

0.02

-3.39

0

7 AT5G08670.1 AT5G08690.1 AT5G08680.1

ATP synthase subunit beta (ATP2) [-1.27] [0.1] -1.93 0.01

8 AT5G08670.1 AT5G08690.1 AT5G08680.1

ATP synthase subunit beta (ATP2) [-1.5] [0] -1.54 0.03 -1.26 0

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32

9 AT5G08670.1 AT5G08690.1 AT5G08680.1

ATP synthase subunit beta (ATP2) -1.27 0.11

10 AT3G52300.1 ATP synthase D subunit (ATPQ) -1.48 0.04 -1.67 0

11 AT2G21870.1 ATP synthase subunit Fad (MGP1) -1.6 0.01 [-1.45] [0.05] [-2.7] [0.01]

TCA cycle 12 AT2G44350.1 Citrate synthase (ATCS)

-1.04 0.05 -1.32 0.01 -1.43 0

13 AT4G26970.1 Aconitase 2 (ACO2) [-1.65] [0.03] -4.85 0 -2.94 0.02

14 AT5G03290.1 NAD+-dependent isocitrate dehydrogenase V (IDH-V) -1.43 0.03

15 AT5G65750.1 2-oxoglutarate dehydrogenase E1 subunit [-1.45] [0.03] -1.65 0.03

16 AT2G20420.1 Succinyl-CoA ligase beta subunit -1.34 0.04 -1.46 0.03 1.26 0.01

17

AT5G66760.1 Succinate dehydrogenase flavoprotein subunit (SDH1-1) 1.96 0.01 1.37 0.04 14.51 0.01

18 AT2G47510.1 Fumarase 1 (FUM1) 1.59 0.01 1.3 0.05 1.02 0.01

19 AT3G15020.2 Malate dehydrogenase 2 (MDH2) -1.13 0.04 -1.3 0.02

TCA cycle adjacent 20 AT5G18170.1 Glutamate dehydrogenase 1 (GDH1)

1.87 0.01 -1.08 0.04

21 AT5G07440.1 Glutamate dehydrogenase 2 (GDH2) -1.34 0.01 [-1.12] [0.01]

22 AT3G22200.1 Gamma-aminobutyrate transaminase (GABA-T) -1.45 0.04 [-1.25] [0.85]

Photorespiration and one carbon metabolism 23 AT4G33010.1 Glycine decarboxylase P-protein 1 (GLDP1) [-1.87] [0.01] [-1.32] [0.01] -3.21 0


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24 AT2G26080.1 Glycine decarboxylase P-protein 2 (GLDP2)

-1.3 0.05 -1.04 0 -2.94 0.02

25 AT1G48030.1 Lipoamide dehydrogenase (MTLPD1) 1.2 0.05 1.43 0

26 AT1G11860.1 Aminomethyltransferase (GDC-T) 1.36 0.02 1.25 0.06

28 AT4G37930.1 Serine transhydroxymethyltransferase 1 (SHM1) -2.85 0

29 AT4G37930.1 Serine transhydroxymethyltransferase 1 (SHM1) 1.66 0.03 1.15 0.05 [-1.32] [0.04]

30 AT4G37930.1 Serine transhydroxymethyltransferase 1 (SHM1) 1.22 0.02 1.13 0.04

31 AT5G14780.1 Formate dehydrogenase (FDH) [1.45] [0.11] 2.14 0.01

Amino acid metabolism 32 AT3G45300.1 Isovaleryl-CoA -dehydrogenase (IVDH)

1.3 0.04 1.42 0.05

33 AT5G62530.1 Pyrroline-5-carboxylate dehydrogenase (P5CDH) -1.5 0 [-1.26] [0]

34 AT3G61440.1 Cysteine synthase C1 (ATCYSC1) -1.18 0 -1.07 0.09 -1.47 0

35 AT3G59760.3 O-acetylserine(thiol)lyase (OAS-C) -1.82 0.04 [-1.94] [0.04]

36 AT4G08870.1 Arginine amidohydrolase 2 (ARGAH2) -2.15 0.01

Chaperones and stress-related 37 AT3G13860.1 Heat shock protein 60-3A (HSP60-3A)

3.2 0.01

38 AT2G33210.1 Heat shock protein 60-2 (HSP60-2) 1.63 0.05 [1.25] [0.02] 1.42 0.01

39 AT2G33210.1 Heat shock protein 60-2 (HSP60-2) 1.38 0.43

40 AT4G37910.1 Heat shock protein 70-1 (mtHSP70-1) 1.62 0.02 [1.6] [0]


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41 AT5G09590.1 Heat shock protein 70-2 (mtHSP70-2)

1.12 0.01 1.48 0.02 1.89 0

42 AT5G40770.1 Prohibitin 3 (PHB3) 1.09 0 1.74 0.04 1.72 0

43 AT3G10920.2 Manganese superoxide dismutase 1 (MSD1) 1.03 0.05 1.29 0.01 1.23 0.04

Proteases 44 AT5G26860.1 LON protease 1 (LON1)

1.56 0.02

45 AT1G51980.1 Probable mitochondrial processing peptidase subunit alpha-1 (Alpha MPP1) -1.31 0.02 [-1.56] [0.01] -1.21 0.02

46 AT3G02090.1 Mitochondrial processing peptidase subunit beta (MPPBETA) -1.01 0.04 -1.57 0.02 -1.02 0.05

Transport 47 AT5G15090.1 Voltage-dependent anion-selective channel 3 (VDAC3)

3.35 0 1.46 0.01

48 AT5G67500.1 Voltage-dependent anion-selective channel 2 (VDAC2) [1.53] [0] 1.42 0.03

49 AT3G01280.1 Voltage-dependent anion-selective channel 1 (VDAC1) 1.57 0.05 1.7 0

Miscellaneous 51 AT3G48000.1 Aldehyde dehydrogenase (ALDH2B4)

-1.52 0

52 AT4G11010.1 Nucleoside diphosphate kinase 3 (NDPK3) -1.25 0.01

53 AT5G63400.1 Adenylate kinase (ADK1) -1.79 0.01

54 AT4G02930.1 Elongation factor Tu (EF-Tu) -1.27 0.03

55 AT3G07480.1 Electron carrier/ iron-sulfur cluster binding; ferredoxin-like 1.84 0.03

Contaminations


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56 AT3G01500.1 Carbonic anhydrase 1 (CA1) (chloroplast) -3.14 0 1.22 0.05

57 AT2G33150.1 Peroxisomal 3-ketoacyl-CoA thiolase 3 (PKT3) (peroxisome. glyoxisome) -2.08 0.01 -2.94 0.05

58 AT2G13360.1 Alanine:glyoxylate aminotransferase (AGT) (peroxisome) 2.94 0.05

59 AT1G20620.1 Catalase 3 (CAT3) (peroxisome) 2.22 0 1.79 0.01

60 AT5G14920.1 Gibberellin-regulated family protein (extracellular) -2.55 0 1.89 0.04

61 AT1G78850.1 Curculin-like (mannose-binding) lectin family protein (extracellular) 1.57 0.05

62 AT4G32900.1 Aminoacyl-tRNA hydrolase (cytosol) -1.33 0.03

63 AT5G45150.1 RNase THREE-like protein (RTL3) (nucleus) -1.45 0.03

64 AT2G20630.2 Protein phosphatase 2C (PP2C) (cytosol) -1.65 0.03

65 AT2G26430.1 Arginine -rich cyclin 1 (RCY1) (nucleus) -1.27 0.03

66 AT5G60240.1 Unknown protein (nucleus) -4.05 0

67 AT1G14060.1 GCK domain-containg protein (nucleus) -3.81 0

68 AT3G16420.1 PYK10-binding protein 1 (PBP1) 1.45 0

69 AT1G17290.1 Alaninine aminotransferase (ALAAT1) (cytosol) -1.38 0.04 [-1.34] [0] -1.64 0

70 AT2G29420.1 Glutathione S-transferase U7 (ATGSTU7) (cytosol) -1.04 0.06 -1.87 0.04

996 *fold change in abundance of ftsh4/WT with cut-off 1.2 and t-test p value (p≤0.05). Values not passing this cut-off are written in 997

italics, values in [ ] correspond to spots only identified based on their positions in 2D-DIGE gels due to technical limitations. 998


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36

Table II. Average oxidation indexes (ftsh4/WT) for selected mitochondrial proteins in all tested experimental setups (A, LD, 30°C for ftsh4-1; B) 1 ftsh4-2, and C) SD, 22°C for ftsh4-1). Spot quantification (percentage volume of each spot) was performed on 2D-OxyBlots from WT and ftsh4 2 mitochondria using ImageJ Fiji software and on 2D-DIGE gels using DeCyder 2D 6.5 software. The oxidation fold was normalized by the 3 corresponding protein fold to assess the oxidation index. Columns from left show: protein spot number on 2D-OxyBlot, accession number (TAIR), 4 protein name annotation and oxidation indexes. 5 A) LD/30°C ftsh4-1/WT B) LD/30°C ftsh4-2/WT C) /SD/22°C ftsh4-1/WT 6

7 Protein

spot number

Accession number (TAIR)

Name of the protein Oxidation Indexes SD/22°C

ftsh-1/WT 14 AT4G26970.1 Aconitate hydratase 2

(ACO2) 14.62

15 AT4G26970.1 Aconitate hydratase 2 (ACO2) 11.99

28 AT3G61440.1 Cysteine synthase (ATCYSC1) 9.4

1 AT5G37510.2 NADH dehydrogenase (ubiquinone). 75 kDa

subunit 7.21

22 AT4G37930.1 Serine

hydroxymethyltransferase 1 (SHM1)

6.08

26 AT5G18170.1 Glutamate

dehydrogenase 1 (GDH1)

5.5

24 AT1G48030.1 Mitochondrial lipoamide

dehydrogenase 1 (MTLPD1)

4.28

17 AT2G47510.1 Fumarase (FUM1) 4.15

7 ATMG01190.1 ATP synthase subunit alpha (ATP1) 3.49

19 AT1G11860.1 Aminomethyltransferase (GDC-T) 3.41

16 AT2G20420.1 Succinyl-CoA ligase subunit beta 2.95



2.71

8 AT5G08670.1 ATP synthase subunit beta (ATP2) 2.41

25 AT5G14780.1 Formate dehydrogenase (FDH) 1.82

5 AT3G02090.1 Mitochondrial processing peptidase subunit beta

(MPPBETA)1.66

9 AT5G08670.1. AT5G08690.1. AT5G08680.1

ATP synthase subunit beta (ATP2) 1.63

29 AT3G10920.2 Manganese superoxide dismutase 1 (MSD1) 1.23

Protein spot

number Accession

numer (TAIR) Name of the protein Oxidation Indexes




8.29


(MPPBETA) 7.29


17 AT2G47510.1 Fumarase (FUM1)

5.68


18 AT3G15020.2 Malate dehydrogenase (MDH2) 4.95




4.02


10 AT2G21870.1 ATP synthase subunit Fad (MGP1) 2.72

9 AT5G08670.1. AT5G08690.1. AT5G08680.1


26 AT5G18170.1 Glutamate dehydrogenase 1 (GDH1) 1.76

28 AT3G61440.1 Cysteine synthase (ATCYSC1) 1.72

13 AT2G44350.1 Citrate synthase (ATCS)

1.58

4 AT5G66760.1 Succinate dehydrogenase

flavoprotein subunit (SDH1-1)

1.09

2 AT1G47260.1 Gamma carbonic

anhydrase 2 (CA2)

1

Protein spot

number Accession

number (TAIR) Name of the protein Oxidation Indexes


8 AT5G08670.1 ATP synthase subunit beta (ATP2) 8.35


9 AT5G08670.1. AT5G08690.1. AT5G08680.1



(MPPBETA) 4.02

1 AT5G37510.2 NADH dehydrogenase (ubiquinone). 75 kDa

subunit 3.83



3.29




2.96


17 AT2G47510.1 Fumarase (FUM1) 2.61





1.76


30 AT5G15090.1 Voltage-dependent anion-

selective channel 3 (VDAC3)

1.63


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37

Figure legends 8

9

Figure 1. Morphology of ftsh4 and WT plants growing under LD, 30°C. A, 2-week-old 10

WT and ftsh4 plants grown on agar plates. B, Delay time (in days) in leaf emergence 11

of ftsh4-1 and ftsh4-2 compared to WT. Plants were staged as described by Boyes et 12

al. (2001). C, Rosette diameter of plants grown in soil at indicated time points after 13

sowing. Mean values ± SD from three measurements are shown. Significant 14

differences are indicated by asterisks (one-sample t-test *p<0.05). D, 5-week-old 15

rosette leaves of plants grown in soil. 16

17

Figure 2. A, Morphology of 2-week-old WT, ftsh4-1 and ftsh4-1-FTSH4 (revertant) 18

seedlings grown under LD, 30°C on agar plates. B, Carbonylated proteins in a total 19

protein extract of the above genotypes. Immunodetection with anti-DNP antibodies 20

and quantification of carbonylated proteins in total protein extract, separated by one-21

dimensional gel electrophoresis. Anti-DNP signals from entire lanes were quantified 22

densitometrically. In each experiment, the values for the relative carbonylated protein 23

amount were calculated as a percentage of the value determined for the wild type 24

plants (set to 100%). Mean values ± SD from at least three independent experiments 25

are shown. Statistically significant differences in abundance between WT, ftsh4-1 and 26

ftsh4-1-FtsH4 plants are indicated by asterisks (one-sample t-test *p<0.05). 27

28

Figure 3. Comparison of mitochondrial carbonylated proteins from WT (left) and 29

ftsh4-1 (right) plants growing in LD, 30°C. Proteins separated by IEF/SDS two-30

dimensional gel electrophoresis were transferred on PVDF membrane to 31

subsequently detect carbonylated proteins using the OxyBlot technique. Arrowheads 32

refer to protein spots accumulating in ftsh4 mitochondria, which are identified in all 33

tested setups. Protein spots are listed in Table II and Supplemental Table S2. 34

35

Figure 4. Relative transcript levels for selected genes encoding mitochondrial 36

proteins in ftsh4-1 and ftsh4-2 mutants growing in LD, 30°C compared to wild type 37

plants. A, The level of transcripts for genes encoding proteins identified by DIGE 38

analysis. B, The level of transcripts for genes encoding proteins usually up-regulated 39

by oxidative stress. Relative abundance of transcripts is expressed as log2 ratios. 40

Mean values ± SD from at least three independent experiments are shown. The 41



38

dotted lines indicate the cut-off value +/- 0.5 (log2) of the ratio corresponding to the 42

threshold level for significant up- and down-regulation of the transcripts in ftsh4. Full 43

names of genes are given in Table I and Supplemental Table S1. 44

45

Figure 5. A, Relative transcript levels for genes encoding mitochondrial ATP-46

dependent proteases in ftsh4-1 and ftsh4-2 mutants grown in LD, 22°C and LD, 30°C 47

compared to wild type plants. The relative abundance of transcripts is expressed as 48

log2 ratios. Mean values ± SD from at least three independent experiments are 49

shown. The dotted lines indicate the cut-off value +/- 0.5 (log2) of the ratio 50

corresponding to the threshold level for significant up- and down-regulation of the 51

transcripts in ftsh4. B, Representative images of immunodetection of selected 52

mitochondrial proteases in ftsh4-1 mutant compared to wild type plants growing in 53

LD, 22°C, LD, 30°C or SD, 22°C. C. Densitometric quantification of immunoblots 54

presented in B. Intensity of bands was estimated using Image Quant software 55

(Molecular Dynamics). Data for ftsh4-1 are expressed as percentage of the value for 56

wild type plants. Mean values ± SD from at least three experiments are shown. 57

Significant differences in abundance between WT and ftsh4-1 mutant are indicated 58

by asterisks (one-sample t-test *p<0.05). 59

60

Figure 6. Amounts and activities of respiratory complexes (A,B,C) and the level of 61

ATP (D) in ftsh4 and WT plants. Mitochondria were isolated from 3-week-old WT and 62

mutant plants (ftsh4-1 and ftsh4-2) growing hydroponically in LD, 22°C and LD, 30°C. 63

A, B Coomassie brilliant blue (CBB) and in-gel activity staining of complex I (CI) and 64

V (CV) after blue-native polyacrylamide gel electrophoresis. C, Quantification of 65

activities of complexes I and V. The intensity of bands was estimated by 66

densitometric analysis using Image Quant software (Molecular Dynamics). Relative 67

complex activity from mutant mitochondria was calculated as percentage of that in 68

WT plants. Differences in activity between WT and mutants are in all cases 69

statistically significant (in one-sample t-test p<0.05). Mean values ± SD from three 70

experiments are shown. D, The ATP content in WT and ftsh4 mitochondria. 71

Mitochondria were isolated from 3-week-old WT, ftsh4-1 and ftsh4-2 seedlings grown 72

under LD, 30°C. The ATP concentration was determined as described in Materials 73



39

and Methods. The unpaired t-test was used to estimate the p values: *p<0.05. Error 74

bars correspond to SD (n=6). 75

76

Figure 7. In vitro carbonylated protein degradation in the WT and ftsh4 mitochondria. 77

Immunodetection of carbonylated proteins separated by one-dimensional gel 78

electrophoresis was estimated with anti-DNP antibodies. Anti-DNP signals from 79

entire lanes were quantified densitometrically. Mean values ± SD from three 80

experiments are shown. A, Mitochondria were isolated from 2-week-old WT, ftsh4-1 81

and ftsh4-2 seedlings grown under LD, 30°C and incubated at 22°C for 16 hours in 82

the absence or presence of 3.5 mM ATP. The unpaired t-test was used to estimate 83

the p values: *p<0.05. B, Mitochondria were isolated from 2-week-old WT, ftsh4-1 84

and ftsh4-2 seedlings grown under LD, 22°C and incubated at 22°C for 16 hours in 85

the presence of 5 mM succinate and 8 μM antimycin A, with or without of 3.5 mM 86

ATP. For protease inhibitor assay, the inhibitors of serine proteases (2 mM AEBSF) 87

and metalloproteases (25 mM ortho-phenanthroline, O-Phe) have been added into 88

the incubation medium. Mean values ± SD from three experiments are shown. The 89

unpaired t-test was used to estimate the p values: *p<0.05. 90

91

Figure 8. Mitochondrial morphology and class of lipids involved in cardiolipin 92

biosynthesis, differing in ftsh4. A, Mitochondrial morphology was observed by 93

scanning single protoplasts expressing GFP targeted to mitochondria of WT and 94

ftsh4-1 using Zeiss Confocal Microscopy LSM 510 Meta. Giant mitochondria are 95

highlighted with white arrows. Scale bar 5 µm. * An asteriks indicates a spherical 96

mitochondrion displaying reduced GFP fluorescence pointing out an occurence of 97

oxidative stress. B, Lipids of WT, ftsh4-1 and ftsh4-2 grown under optimal (22°C) and 98

moderately elevated temperature (30°C) were measured by mass spectrometry. Lipid 99

classes are shown in mol% of total lipids in the sample and are sums of individually 100

quantified lipid species. The unpaired t-test was used to calculate the p values: 101

p<0.05. Error bars correspond to SD (n=3). CL, cardiolipin; DAG, diacylglycerol; PC, 102

phosphatidylcholine; PE, phosphatidylethanolamine; PG, phosphatidylglicerol; PI, 103

phosphatidylinositol; PA, phosphatidic acid. Only selected classes are shown - see 104

Supplemental Fig. S4 for the complete data set. 105

106



40

Figure 9. A hypothetical scenario of the events leading to the accumulation of 107

carbonylated proteins in mitochondria of A. thaliana in the absence of FTSH4. The 108

direction of short green arrows specifies change in abundance of cardiolipin (CL), 109

complex I (CI), complex V (CV), ROS, ATP and carbonylated proteins, in the 110

absence of FTSH4. Black lines ending with arrowheads indicate activating effects, 111

while perpendicular lines indicate inhibiting effects. The decreased content of CL as 112

well as absence of the chaperone-like activity of FTSH4 lead to lower stability/activity 113

of complex I and V, which in turn results in accumulation of ROS and decrease of 114

ATP, respectively. The lower concentration of ATP restricts activity of mitochondrial 115

ATP-dependent proteases, which are not able to degrade all carbonylated proteins 116

accumulating in consequence of the elevated ROS level. The lower content of CL 117

further restricts fission, which in turn causes the appearance of giant mitochondria 118

and also blocks mitophagy, important to eliminate mitochondria damaged by 119

oxidative stress. 120

121

122

123

124

125

126

127

128

129

130

131

132

133

134

135

136

137

138

139

140



41

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0

2

4

6

8

10

12

14

16

17 22 35 42

Ros

ette

dia

met

er (c

m)

Day after sowing (days) WT ftsh4-1 ftsh4-2

0

1

2

3

4

5

6

1.02 1.03 1.04 1.05 1.06 1.07 1.08 1.09

Del

ay in

leaf

dev

elop

men

t vs

WT

(day

s)

Growth stage ftsh4-1 ftsh4-2

Figure 1. Morphology of ftsh4 and WT plants growing under LD, 30°C. A, 2-week-old WT and ftsh4 plants grown on

agar plates. B, Delay time (in days) in leaf emergence of ftsh4-1 and ftsh4-2 compared to WT. Plants were staged as

described by Boyes et al. (2001). C, Rosette diameter of plants grown in soil at indicated time points after sowing.

Mean values ± SD from three measurements are shown. Significant differences are indicated by asterisks (one-sample

t-test *p<0.05). D, 5-week-old rosette leaves of plants grown in soil.

A

C

WT ftsh4-1 ftsh4-2

B

D

WT ftsh4-1 ftsh4-2

1 cm

WT ftsh4-1 ftsh4-2

1 cm * * * * * *

* *

* *

* *

*

*

*

*

*

* *



Figure 2. A, Morphology of 2-week-old WT, ftsh4-1 and

ftsh4-1-FTSH4 (revertant) seedlings grown under LD,

30°C on agar plates. B, Carbonylated proteins in a total

protein extract of the above genotypes. Immunodetection

with anti-DNP antibodies and quantif ication of

carbonylated proteins in total protein extract, separated by

one-dimensional gel electrophoresis. Anti-DNP signals

from entire lanes were quantified densitometrically. In

each experiment, the values for the relative carbonylated

protein amount were calculated as a percentage of the

value determined for the wild type plants (set to 100%).

Mean values ± SD from at least three independent

experiments are shown. Statistically significant differences

in abundance between WT, ftsh4-1 and ftsh4-1-FtsH4

plants are indicated by asterisks (one-sample t-test

*p<0.05).

A

B

WT ftsh4-1 – FTSH4 ftsh4-1

0

20

40

60

80

100

120

140

160

180

Rel

ativ

e ca

rbon

ylat

ed p

rote

ins

leve

l

(% o

f WT)

WT ftsh4-1 ftsh4-1-FTSH4

*

1 cm



Figure 3. Comparison of mitochondrial carbonylated proteins from WT (left) and ftsh4-1 (right) plants growing in LD,

30°C. Proteins separated by IEF/SDS two-dimensional gel electrophoresis were transferred on PVDF membrane to

subsequently detect carbonylated proteins using the OxyBlot technique. Arrowheads refer to protein spots

accumulating in ftsh4 mitochondria, which are identified in all tested setups. Protein spots are listed in Table II and

Supplemental Table S2.

pH11$pH$11$94$

66$

45$

14$

20$

30$

pH$3$

MSD1$

SHM1$MPP$B$

ATP1$

Succ$Co$Ligase$

ATP2$

FUM1$

GDC@T$

MTLPD1$

94$

66$

45$

14$

20$

30$

pH$11$pH$3$

Succ$Co$Ligase$

FUM1$ATP1$

GDC@T$

MTLPD1$

MSD1$

SHM1$MPP$B$

ATP2$

MW$$(kDa)$

MW$$(kDa)$

pH$11$WT ftsh4-1



Figure 4. Relative transcript levels for selected genes encoding mitochondrial proteins in ftsh4-1 and ftsh4-2 mutants growing in LD, 30°C

compared to wild type plants. A, The level of transcripts for genes encoding proteins identified by DIGE analysis. B, The level of

transcripts for genes encoding proteins usually up-regulated by oxidative stress. Relative abundance of transcripts is expressed as log2

ratios. Mean values ± SD from at least three independent experiments are shown. The dotted lines indicate the cut-off value +/-0.5 (log2)

of the ratio corresponding to the threshold level for significant up- and down-regulation of the transcripts in ftsh4. Full names of genes are

given in Table I and Supplemental Table S1.

A

B

WT

ftsh4-1 ftsh4-2

Photorespiration and carbon metabolism

Chaperones and stress related

TCA cycle adjacent

Amino acid metabolism Contam. C I C II ATP synthase TCA cycle Proteases Transport

!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!"

!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!"

WT

ftsh4-1 ftsh4-2

!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!"

!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!"



Figure 5. A, Relative transcript levels for genes encoding mitochondrial ATP-dependent proteases in ftsh4-1 and ftsh4-2

mutants grown in LD, 22°C and LD, 30°C compared to wild type plants. The relative abundance of transcripts is expressed

as log2 ratios. Mean values ± SD from at least three independent experiments are shown. The dotted lines indicate the cut-

off value +/- 0.5 (log2) of the ratio corresponding to the threshold level for significant up- and down-regulation of the

transcripts in ftsh4. B, Representative images of immunodetection of selected mitochondrial proteases in ftsh4-1 mutant

compared to wild type plants growing in LD, 22°C, LD, 30°C or SD, 22°C. C. Densitometric quantification of immunoblots

presented in B. Intensity of bands was estimated using Image Quant software (Molecular Dynamics). Data for ftsh4-1 are

expressed as percentage of the value for wild type plants. Mean values ± SD from at least three experiments are shown.

Significant differences in abundance between WT and ftsh4-1 mutant are indicated by asterisks (one-sample t-test

*p<0.05).

A

B

C

0

20

40

60

80

100

120

140

160

180

LD, 22°C LD, 30°C SD, 22°C LD, 22°C LD, 30°C SD, 22°C

FTSH10 FTSH3

Rel

ativ

e pr

otei

n ab

unda

nce

(% o

f WT)

WT ftsh4-1

* *

*



Figure 6. Amounts and activities of respiratory complexes (A,B,C) and the level of ATP (D) in ftsh4 and WT plants.

Mitochondria were isolated from 3-week-old WT and mutant plants (ftsh4-1 and ftsh4-2) growing hydroponically in LD,

22°C and LD, 30°C. A, B Coomassie brilliant blue (CBB) and in-gel activity staining of complex I (CI) and V (CV) after

blue-native polyacrylamide gel electrophoresis. C, Quantification of activities of complexes I and V. The intensity of

bands was estimated by densitometric analysis using Image Quant software (Molecular Dynamics). Relative complex

activity from mutant mitochondria was calculated as percentage of that in WT plants. Differences in activity between

WT and mutants are in all cases statistically significant (in one-sample t-test p<0.05). Mean values ± SD from three

experiments are shown. D, The ATP content in WT and ftsh4 mitochondria. Mitochondria were isolated from 3-week-

old WT, ftsh4-1 and ftsh4-2 seedlings grown under LD, 30°C. The ATP concentration was determined as described in

Materials and Methods. The unpaired t-test was used to estimate the p values: *p<0.05. Error bars correspond to SD

(n=6).

C I C V CBB

I+III2

I V

III2

C I C V CBB

WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2

A B LD, 30°C LD, 22°C

C


I+III2

I V

III2

0

20

40

60

80

100

120

LD 22°C LD 30°C LD 22°C LD 30°C

C I C V

Rel

ativ

e ac

tivity

(% o

f WT)

WT ftsh4-1 ftsh4-2

D

* *

0

1

2

3

4

5

6

7

8

9

WT ftsh4-1 ftsh4-2

* *

ATP

cont

ent (

pmol

/mg

prot

ein)



A

LD, 30°C

0h 16h 16h


Time [h] ATP - - - - - - + + +

B LD, 22°C; antimycin A

- - - - - - + + + + + + + + +

WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2 WT ftsh4-1 ftsh4-2

Time [h]

ATP

0h 16h 16h 16h 16h

O-Phe AEBSF - - - - - - - - - + + + - - -

- - - - - - - - - - - - + + +

Figure 7. In vitro carbonylated protein degradation in the WT and ftsh4 mitochondria. Immunodetection of

carbonylated proteins separated by one-dimensional gel electrophoresis was estimated with anti-DNP antibodies.

Anti-DNP signals from entire lanes were quantified densitometrically. Mean values ± SD from three experiments are

shown. A, Mitochondria were isolated from 2-week-old WT, ftsh4-1 and ftsh4-2 seedlings grown under LD, 30°C and

incubated at 22°C for 16 hours in the absence or presence of 3.5 mM ATP. The unpaired t-test was used to estimate

the p values: *p<0.05. B, Mitochondria were isolated from 2-week-old WT, ftsh4-1 and ftsh4-2 seedlings grown under

LD, 22°C and incubated at 22°C for 16 hours in the presence of 5 mM succinate and 8 µM antimycin A, with or

without of 3.5 mM ATP. For protease inhibitor assay, the inhibitors of serine proteases (2 mM AEBSF) and

metalloproteases (25 mM ortho-phenanthroline, O-Phe) have been added into the incubation medium. Mean values ±

SD from three experiments are shown. The unpaired t-test was used to estimate the p values: *p<0.05.

0

20

40

60

80

100

120

140

160

Rel

ativ

e le

vel o

f car

bony

late

d pr

otei

ns

(% o

f the

leve

l in

time

0h)

0h 16h - ATP 16h + ATP

WT ftsh4-1 ftsh4-2

* * *

0

20

40

60

80

100

120

140

160

180

Rel

ativ

e le

vel o

f car

bony

late

d pr

otei

ns

(% o

f the

leve

l in

time

0h)

0h 16h-ATP 16h+ATP 16h+ATP+AEBSF 16h+ATP+O-Phe WT ftsh4-1 ftsh4-2

*

* *

*

*



Figure 8. Mitochondrial morphology and class of lipids involved in cardiolipin biosynthesis, differing in ftsh4. A,

Mitochondrial morphology was observed by scanning single protoplasts expressing GFP targeted to mitochondria of

WT and ftsh4-1 using Zeiss Confocal Microscopy LSM 510 Meta. Giant mitochondria are highlighted with white

arrows. Scale bar 5 µm. * An asteriks indicates a spherical mitochondrion displaying reduced GFP fluorescence

pointing out an occurence of oxidative stress. B, Lipids of WT, ftsh4-1 and ftsh4-2 grown under optimal (22°C) and

moderately elevated temperature (30°C) were measured by mass spectrometry. Lipid classes are shown in mol% of

total lipids in the sample and are sums of individually quantified lipid species. The unpaired t-test was used to

calculate the p values: p<0.05. Error bars correspond to SD (n=3). CL, cardiolipin; DAG, diacylglycerol; PC,

phosphatidylcholine; PE, phosphatidylethanolamine; PG, phosphatidylglicerol; PI, phosphatidylinositol; PA,

phosphatidic acid. Only selected classes are shown - see Supplemental Fig. S4 for the complete data set.

B

A

LD, 30° C

LD, 22° C

WT-GFP ftsh4-1-GFP

22° 30° 22° 30° 22° 30° 22° 30° 22° 30° 22° 30° 22° 30° 0

5

10

15

20

25

30

35

40

45

50

mol

%

Lipid class

* * * * *

CL DAG PC PE PG PI PA



Figure 9. Figure 9. A hypothetical scenario of the events leading to the accumulation of carbonylated proteins in mitochondria of A.

thaliana in the absence of FTSH4. The direction of short green arrows specifies change in the abundance of cardiolipin (CL),

complex I (CI), complex V (CV), ROS, ATP and carbonylated proteins, in the absence of FTSH4. Black lines ending with

arrowheads indicate activating effects, while perpendicular lines indicate inhibiting effects. The decreased content of CL and a lack

of chaperone-like activity of FTSH4 lead to a reduced stability/activity of complex I and V, which in turn results in higher amount of

ROS and decrease of ATP. The lower concentration of ATP restricts activity of mitochondrial ATP-dependent proteases, which are

not able to degrade all carbonylated proteins accumulating in consequence of the elevated ROS level. The lower content of CL

further restricts fission, which in turn causes the appearance of giant mitochondria as well as blocks mitophagy, important to

eliminate mitochondria damaged by oxidative stress. OMM-mitochondrial outer membrane; IMS-intermembrane space of

mitochondria; IMM-inner mitochondrial membrane; FTSH- filament-forming temperature- sensitive, ATP-dependent

metalloprotease of mitochondrial inner membrane; LON-ATP-dependent serine protease of mitochondrial matrix; Clp- ATP-

dependent serine protease of mitochondrial matrix; PHB complex-prohibitin complex; CI-V-oxidative phosphorylation complex I-V;

CL-cardiolipin; ROS-reactive oxygen species; ATP- adenosine triphosphate.

FTSH4

CL#

CL#

ROS#

CARBONYLATED PROTEINS

ATP#

IMS

IMM

OMM

MATRIX

CIV$

FISSION MITOPHAGY

GIANT MITOCHONDRIA #

FTSH3$ FTSH10$ FTSH3/10$

PHB$$complex$

PHB$$complex$

PHB$$complex$

LON1$

CLPX(1;3)$LON4$

FTSH11$

CI$

CIII$

CII$

CV$



Parsed CitationsAnand R, Langer T, Baker MJ (2013) Proteolytic control of mitochondrial function and morphogenesis. Mol Cell Res 1833: 195-204

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Araújo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham JA, Leaver CJ, Fernie AR(2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysinecatabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22: 1549-1563


Araújo WL, Tohge T, Ishizaki K, Leaver CJ, Fernie AR (2011) Protein degradation-an alternative respiratory substrate for stressedplants. Trends Plant Sci 16: 489-498


Augustin S, Nolden M, Müller S, Hardt O, Arnold I, Langer T (2005) Characterization of peptides released from mitochondria:evidence for constant proteolysis and peptide efflux. J Biol Chem 280: 2691-2699


Baker MJ, Mooga VP, Guiard B, Langer T, Ryan MT, Stojanovski D (2012) Impaired folding of the mitochondrial small TIMchaperones induces clearance by the i-AAA protease. J Mol Biol 424: 227-239


Baker MJ, Palmer CS, Stojanovski D (2014) Mitochondrial protein quality control in health and disease. Br J Pharmacol 171: 1870-1889


Baker MJ, Tatsuta T, Langer T (2011) Quality Control of Mitochondrial Proteostasis. Cold Spring Harb Perspect Biol 3:1-19Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bayot A, Gareil M, Rogowska-Wrzesinska A, Roepstorff P, Friguet B, Bulteau AL (2010) Identification of novel oxidized proteinsubstrates and physiological partners of the mitochondrial ATP-dependent Lon-like protease Pim1. J Biol Chem 285: 11445-11457


Bender T, Lewrenz I, Franken S, Baitzel C, Voos W (2011) Mitochondrial enzymes are protected from stress-induced aggregationby mitochondrial chaperones and the Pim1/LON protease. Mol Biol Cell 22: 541-554


Bota DA, Davies KJ (2002) Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulatedmechanism. Nat Cell Biol 4: 674-680


Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis ofArabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13: 1499-510


Böttinger L, Horvath ES, Kleinschroth T, Hunte C, Daum G, Pfanner N, Becker T (2012) Phosphatidylethanolamine and cardiolipindifferentially affect the stability of mitochondrial respiratory chain supercomplexes. J Mol Biol 423: 677-686


Day DA, Neuburger M, Douce R (1985) Biochemical characterization of chlorophyll-free mitochondria from pea leaves. Aust J PlantPhysiol 12: 219-228


Desfeux C, Clough SJ, Bent AF (2000) Female reproductive tissues are the primary target of Agrobacterium-mediatedhttps://plantphysiol.orgDownloaded on November 24, 2020. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

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Elgass K, Pakay J, Ryan MT, Palmer CS (2013) Recent advances into the understanding of mitochondrial fission. Biochim BiophysActa. 1833: 150-161


Fischer F, Hamann A, Osiewacz HD (2012) Mitochondrial quality control: an integrated network of pathways. Trends Biochem Sci37: 284-292


Fiumera HL, Dunham MJ, Saracco SA, Butler CA, Kelly JA, Fox TD (2009) Translocation and assembly of mitochondrially codedSaccharomyces cerevisiae cytochrome c oxidase subunit Cox2 by Oxa1 and Yme1 in the absence of Cox18. Genetics 182: 519-528


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http://scholar.google.com/scholar?as_q=Translocation and assembly of mitochondrially coded Saccharomyces cerevisiae cytochrome c oxidase subunit Cox2 by Oxa1 and Yme1 in the absence of Cox18&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Translocation and assembly of mitochondrially coded Saccharomyces cerevisiae cytochrome c oxidase subunit Cox2 by Oxa1 and Yme1 in the absence of Cox18&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fiumera&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mitochondrion%5BTitle%5D%29 AND 11%5BVolume%5D AND 587%5BPagination%5D AND Francis BR%2C Thorsness PE%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Francis BR, Thorsness PE (2011) Hsp90 and mitochondrial proetases Yme1 and Yta10/12 participate in ATP synthase assembly in Saccharomyces cerevisiae. Mitochondrion 11: 587-600

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http://scholar.google.com/scholar?as_q=Hsp90 and mitochondrial proetases Yme1 and Yta10/12 participate in ATP synthase assembly in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Hsp90 and mitochondrial proetases Yme1 and Yta10/12 participate in ATP synthase assembly in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Francis&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 290%5BVolume%5D AND 9284%5BPagination%5D AND Gaspard GJ%2C McMaster CR%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=The mitochondrial quality control protein Yme1 is necessary to prevent defective mitophagy in a yeast model of Barth syndrome&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The mitochondrial quality control protein Yme1 is necessary to prevent defective mitophagy in a yeast model of Barth syndrome&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gaspard&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 59%5BVolume%5D AND 685%5BPagination%5D AND Gibala M%2C Kicia M%2C Sakamoto W%2C Gola EM%2C Kubrakiewicz J%2C Smakowska E%2C Janska H%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gibala&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biochim Biophys Acta %2D Mol Basis Dis%5BTitle%5D%29 AND 1832%5BVolume%5D AND 1194%5BPagination%5D AND Gonzalvez F%2C D%27Aurelio M%2C Boutant M%2C Moustapha A%2C Puech JP%2C Landes T%2C Arnaun�%2DPelloquin L%2C Vial G%2C Taleux N%2C Slomianny C%2C Wanders RJ%2C Houtkooper RH%2C Bellenguer P%2C Moller IM%2C Gottlieb E%2C Vaz FM%2C Manfredi G%2C Petit PX%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Barth syndrome: cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Barth syndrome: cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gonzalvez&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28LipidXplorer%3A a software for consensual cross%2Dplatform lipidomics%2E%5BTitle%5D%29 AND Herzog R%2C Schuhmann K%2C Schwudke D%2C Sampaio JL%2C Bornstein SR%2C Schroeder M%2C Shevchenko A%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Herzog&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=LipidXplorer: a software for consensual cross-platform lipidomics.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=LipidXplorer: a software for consensual cross-platform lipidomics.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Herzog&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28A novel informatics concept for high%2Dthroughput shotgun lipidomics based on the molecular fragmentation query language%2E%5BTitle%5D%29 AND Herzog R%2C Schwudke D%2C Schuhmann K%2C Sampaio JL%2C Bornstein SR%2C Schroeder M%2CShevchenko A%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Herzog&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biochim Biophys Acta%5BTitle%5D%29 AND 1797%5BVolume%5D AND 1071%5BPagination%5D AND Janska H%2C Piechota J%2C Kwasniak M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Janska H, Piechota J, Kwasniak M (2010) ATP-dependent proteases in biogenesis and maintenance of plant mitochondria. Biochim Biophys Acta 1797: 1071-1075

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Janska&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=ATP-dependent proteases in biogenesis and maintenance of plant mitochondria&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=ATP-dependent proteases in biogenesis and maintenance of plant mitochondria&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Janska&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 287%5BVolume%5D AND 17589%5BPagination%5D AND Joshi AS%2C Thompson MN%2C Fei N%2C H�ttemann M%2C Greenberg ML%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Cardiolipin and mitochondrial phosphatidylethanolamine have overlapping functions in mitochondrial fusion in Saccharomyces cerevisiae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Joshi&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 280%5BVolume%5D AND 20132%5BPagination%5D AND Kambacheld M%2C Augustin S%2C Tatsuta T%2C M�ller S%2C Langer T%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Signal Behav%5BTitle%5D%29 AND 5%5BVolume%5D AND 126%5BPagination%5D AND Kicia M%2C Gola EM%2C Janska H%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kicia M, Gola EM, Janska H (2010) Mitochondrial protease AtFtsH4 protects ageing Arabidopsis rosettes against oxidative damage under short-day photoperiod. Plant Signal Behav 5:126-128

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kicia&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mitochondrial protease AtFtsH4 protects ageing Arabidopsis rosettes against oxidative damage under short-day photoperiod&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mitochondrial protease AtFtsH4 protects ageing Arabidopsis rosettes against oxidative damage under short-day photoperiod&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kicia&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Physiol Plant%5BTitle%5D%29 AND 129%5BVolume%5D AND 135%5BPagination%5D AND Kolodziejczak M%2C Gibala M%2C Urantowka A%2C Janska H%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kolodziejczak M, Gibala M, Urantowka A, Janska H (2007) The significance of Arabidopsis AAA proteases for activity and assembly/stability of mitochondrial OXPHOS complexes. Physiol Plant 129: 135-142

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kolodziejczak&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The significance of Arabidopsis AAA proteases for activity and assembly/stability of mitochondrial OXPHOS complexes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The significance of Arabidopsis AAA proteases for activity and assembly/stability of mitochondrial OXPHOS complexes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kolodziejczak&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Phytochemistry%5BTitle%5D%29 AND 65%5BVolume%5D AND 1839%5BPagination%5D AND Kristensen BK%2C Askerlund P%2C Bykova N%2C Egsgaard H%2C Moller IM%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kristensen BK, Askerlund P, Bykova N, Egsgaard H, Moller IM (2004) Identification of oxidized proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry. Phytochemistry 65: 1839-1851

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kristensen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Identification of oxidized proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Identification of oxidized proteins in the matrix of rice leaf mitochondria by immunoprecipitation and two-dimensional liquid chromatography-tandem mass spectrometry&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kristensen&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Nature%5BTitle%5D%29 AND 227%5BVolume%5D AND 680%5BPagination%5D AND Laemmli UK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Laemmli&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cleavage of structural proteins during the assembly of the head of bacteriophage T4&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cleavage of structural proteins during the assembly of the head of bacteriophage T4&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Laemmli&as_ylo=1970&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Mol Plant%5BTitle%5D%29 AND 2%5BVolume%5D AND 390%5BPagination%5D AND Lehmann M%2C Schwarzl�nder M%2C Obata T%2C Sirikantaramas S%2C Burow M%2C Olsen CE%2C Tohge T%2C Fricker MD%2C Moller BL%2C Fernie AR%2C Sweetlove LJ%2C Laxa M%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lehmann M, Schwarzl�nder M, Obata T, Sirikantaramas S, Burow M, Olsen CE, Tohge T, Fricker MD, Moller BL, Fernie AR, Sweetlove LJ, Laxa M (2009) The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol Plant 2: 390-406

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lehmann&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lehmann&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Cell Death Differ%5BTitle%5D%29 AND 102%5BVolume%5D AND 1%5BPagination%5D AND Li H%2C Ruan Y%2C Zhang K%2C Jian F%2C Hu C%2C Miao L%2C Gong L%2C Sun L%2C Zhang X%2C Chen S%2C Chen H%2C Liu D%2C Song Z%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li H, Ruan Y, Zhang K, Jian F, Hu C, Miao L, Gong L, Sun L, Zhang X, Chen S, Chen H, Liu D, Song Z (2015) Mic/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization. Cell Death Differ 102: 1-13

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Li&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mic/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mic/Mitofilin determines MICOS assembly essential for mitochondrial dynamics and mtDNA nucleoid organization&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 12%5BVolume%5D AND 419%5BPagination%5D AND Lindahl M%2C Spetea C%2C Hundal T%2C Oppenheim A%2C Adam Z%2C Andersson B%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Moller&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moller&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moller&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biosci Bioeng%5BTitle%5D%29 AND 104%5BVolume%5D AND 34%5BPagination%5D AND Nakagawa T%2C Kurose T%2C Hino T%2C Tanaka K%2C Kawamukai M%2C Niwa Y%2C Toyooka K%2C Matsuoka K%2C Jinbo T%2C Kimura T%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nakagawa&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

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Pan R, Jones AD, Hu J (2014) Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis. Plant Cell 26: 391-409


Pearce DA, Sherman F (1995) Degradation of cytochrome oxidse subunits in mutants of yeast lacking cytochrome c andsuppression of the degradation by mutation of yme1. J Biol Chem 270: 20879-20882


Petrosillo G, Portincasa P, Grattagliano I, Casanova G, Matera M, Ruggiero FM, Ferri D, Paradies G (2007) Mitochondrialdysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin. Biochim BiophysActa 1767: 1260-1267


Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, and Hermann Schägger (2003) Cardiolipin Stabilizes RespiratoryChain Supercomplexes. J Biol Chem 278: 52873-52880


Piechota J, Kolodziejczak M, Juszczak I, Sakamoto W, Janska H (2010) Identification and characterization of high molecular weightcomplexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. J Biol Chem 285: 12512-12521


Pineau B, Bourge M, Marion J, Mauve C, Gilard F, Maneta-Peyret L, Moreau P, Satiat-Jeunemaître B, Brown SC, De Paepe R,Danon A (2013) The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development,and stress responses in Arabidopsis. Plant Cell 25: 4195-4208


Potting C, Tatsuta T, König T, Haag M, Wai T, Aaltonen MJ, Langer T (2013) TRIAP1/PRELI complexes prevent apoptosis bymediating intramitochondrial transport of phosphatidic acid. Cell Metab 18: 287-295


Potting C, Wilmes C, Engemann T, Osman C, Langer T (2010) Regulation of mitochondrial phospholipids by Ups/PRELI-likeproteins depends on proteolysis and Mdm35. EMBO J 29: 2888-2898


Qi Y, Liu H, Daniels MP, Zhang G, Xu H (2015) Loss of Drosophila i-AAA protease, dYME1L causes abnormal mitochondria andapoptotic degeneration. Cell Death Differ 94: 1-12


Qin G, Meng X, Wang Q, Tian S (2009) Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redoxproteomics analysis. J Prot Res 8: 2449-2462


Rainey RN, Glavin JD, Chen HW, French SW, Teitell MA, Koehler CM (2006) A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space. Mol Cell Biol 26: 8488-8497


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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Osellame&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cellular and molecular mechanisms of mitochondrial function&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cellular and molecular mechanisms of mitochondrial function&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Osellame&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 26%5BVolume%5D AND 391%5BPagination%5D AND Pan R%2C Jones AD%2C Hu J%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pan R, Jones AD, Hu J (2014) Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis. Plant Cell 26: 391-409

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pan&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cardiolipin-mediated mitochondrial dynamics and stress response in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pan&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 270%5BVolume%5D AND 20879%5BPagination%5D AND Pearce DA%2C Sherman F%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pearce DA, Sherman F (1995) Degradation of cytochrome oxidse subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1. J Biol Chem 270: 20879-20882

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pearce&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Degradation of cytochrome oxidse subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Degradation of cytochrome oxidse subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pearce&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biochim Biophys Acta%5BTitle%5D%29 AND 1767%5BVolume%5D AND 1260%5BPagination%5D AND Petrosillo G%2C Portincasa P%2C Grattagliano I%2C Casanova G%2C Matera M%2C Ruggiero FM%2C Ferri D%2C Paradies G%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Petrosillo G, Portincasa P, Grattagliano I, Casanova G, Matera M, Ruggiero FM, Ferri D, Paradies G (2007) Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin. Biochim Biophys Acta 1767: 1260-1267

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Petrosillo&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Petrosillo&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 278%5BVolume%5D AND 52873%5BPagination%5D AND Pfeiffer K%2C Gohil V%2C Stuart RA%2C Hunte C%2C Brandt U%2C Greenberg ML%2C and Hermann Sch�gger%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, and Hermann Sch�gger (2003) Cardiolipin Stabilizes Respiratory Chain Supercomplexes. J Biol Chem 278: 52873-52880

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pfeiffer&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cardiolipin Stabilizes Respiratory Chain Supercomplexes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cardiolipin Stabilizes Respiratory Chain Supercomplexes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pfeiffer&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Biol Chem%5BTitle%5D%29 AND 285%5BVolume%5D AND 12512%5BPagination%5D AND Piechota J%2C Kolodziejczak M%2C Juszczak I%2C Sakamoto W%2C Janska H%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Piechota J, Kolodziejczak M, Juszczak I, Sakamoto W, Janska H (2010) Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. J Biol Chem 285: 12512-12521

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Piechota&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Piechota&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Cell%5BTitle%5D%29 AND 25%5BVolume%5D AND 4195%5BPagination%5D AND Pineau B%2C Bourge M%2C Marion J%2C Mauve C%2C Gilard F%2C Maneta%2DPeyret L%2C Moreau P%2C Satiat%2DJeunema�tre B%2C Brown SC%2C De Paepe R%2C Danon A%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Pineau B, Bourge M, Marion J, Mauve C, Gilard F, Maneta-Peyret L, Moreau P, Satiat-Jeunema�tre B, Brown SC, De Paepe R, Danon A (2013) The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis. Plant Cell 25: 4195-4208

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pineau&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pineau&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Cell Metab%5BTitle%5D%29 AND 18%5BVolume%5D AND 287%5BPagination%5D AND Potting C%2C Tatsuta T%2C K�nig T%2C Haag M%2C Wai T%2C Aaltonen MJ%2C Langer T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Potting C, Tatsuta T, K�nig T, Haag M, Wai T, Aaltonen MJ, Langer T (2013) TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid. Cell Metab 18: 287-295

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Potting&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=TRIAP1/PRELI complexes prevent apoptosis by mediating intramitochondrial transport of phosphatidic acid&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Potting&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28EMBO J%5BTitle%5D%29 AND 29%5BVolume%5D AND 2888%5BPagination%5D AND Potting C%2C Wilmes C%2C Engemann T%2C Osman C%2C Langer T%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Potting C, Wilmes C, Engemann T, Osman C, Langer T (2010) Regulation of mitochondrial phospholipids by Ups/PRELI-like proteins depends on proteolysis and Mdm35. EMBO J 29: 2888-2898

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Potting&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Regulation of mitochondrial phospholipids by Ups/PRELI-like proteins depends on proteolysis and Mdm35&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Regulation of mitochondrial phospholipids by Ups/PRELI-like proteins depends on proteolysis and Mdm35&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Potting&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Cell Death Differ%5BTitle%5D%29 AND 94%5BVolume%5D AND 1%5BPagination%5D AND Qi Y%2C Liu H%2C Daniels MP%2C Zhang G%2C Xu H%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Qi Y, Liu H, Daniels MP, Zhang G, Xu H (2015) Loss of Drosophila i-AAA protease, dYME1L causes abnormal mitochondria and apoptotic degeneration. Cell Death Differ 94: 1-12

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Qi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Loss of Drosophila i-AAA protease, dYME1L causes abnormal mitochondria and apoptotic degeneration&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Loss of Drosophila i-AAA protease, dYME1L causes abnormal mitochondria and apoptotic degeneration&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Qi&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Prot Res%5BTitle%5D%29 AND 8%5BVolume%5D AND 2449%5BPagination%5D AND Qin G%2C Meng X%2C Wang Q%2C Tian S%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Qin G, Meng X, Wang Q, Tian S (2009) Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redox proteomics analysis. J Prot Res 8: 2449-2462

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http://scholar.google.com/scholar?as_q=Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redox proteomics analysis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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Sampaio JL, Gerl ML, Klose Ch, Ejsing CS, Beug H, Simons K, Shevchenko A (2011) Membrane lipidome of an epithelial cell line.Proc Natl Acad Sci U S A 108: 1903-1907


Schreiner B, Westerburg H, Forne I, Imhof A, Neupert W, Mokranjac D (2012) Role of the AAA protease Yme1 in folding of proteinsin the intermembrane space of mitochondria. Mol Bio Cell 23: 4335-4346


Scott I, Logan DC (2008) Mitochondrial morphology transition is an early indicator of subsequent cell death in Arabidopsis. NewPhytologist 177: 90-101


Smakowska E, Czarna M, Janska H (2014) Mitochondrial ATP-dependent proteases in protection against accumulation ofcarbonylated proteins. Mitochondrion 19: 245-251


Solheim C, Li L, Hatzopoulos P, Millar AH (2012) Loss of Lon1 in Arabidopsis changes the mitochondrial proteome leading toaltered metabolite profiles and growth retardation without an accumulation of oxidative damage. Plant Physiol 160: 1187-1203


Stiburek L, Cesnekova J, Kostkova O, Fornuskova D, Vinsova K, Wenchich L, Houstek J, Zeman J (2012) YME1L controls theaccumulation of respiratory chain subunits and is required for apoptotic resistance, cristae morphogenesis, and cell proliferation.Mol Biol Cell 23: 1010-1023


Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress onArabidopsis mitochondria. Plant J 32: 891-904


Tatsuta T, Langer T (2007) Studying proteolysis within mitochondria. Methods Mol Biol 372: 343-360Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Tatsuta T, Langer T (2008) Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 27: 306-314Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, Yuan J,Deeney JT, Corkey BE, Shirihai OS (2008) Fission and selective fusion govern mitochondrial segregation and elimination byautophagy. EMBO J 27: 433-446


Urantowka A, Knorpp C, Olczak T, Kolodziejczak M, Janska H (2005) Plant mitochondria contain at least two i-AAA-like complexes.Plant Mol Biol 59: 239-252


Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasisduring abiotic and biotic stress in plants. Int J Mol Sci 14: 6805-6847


Van Lis R, Atteia A, Mendoza-Hernandez G, Gonzalez-Halphen D (2003) Identification of novel mitochondrial protein componentsof Chlamydomonas reinhardtii. A proteomic approach. Plant Physiol 132: 318-330

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