running head: in vivo respiration in cef-psi mutants 2 9 10 11 12 … · 133 components of the...

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Running head: In vivo respiration in CEF-PSI mutants 1

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Corresponding author: 5

Miquel Ribas-Carbo 6

Universitat de les Illes Balears 7

Crta. Valldemossa Km 7.5 8

07122 Palma de Mallorca 9

Spain 10

Tel: +34 971173168 11

Fax: +34 971173184 12

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Focus Issue on Metabolism 17

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Plant Physiology Preview. Published on October 19, 2016, as DOI:10.1104/pp.16.01025

Copyright 2016 by the American Society of Plant Biologists

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Impaired cyclic electron flow around Photosystem I disturbs high-light respiratory 19

metabolism1 20

Igor Florez-Sarasa2, Ko Noguchi2, Wagner L. Araújo, Ana Garcia-Nogales, Alisdair R. 21

Fernie, Jaume Flexas, Miquel Ribas-Carbo* 22

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Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 24

Potsdam-Golm, Germany (I.F.-S, A.R.F.); School of Life Sciences, Tokyo University of 25

Pharmacy and Life Sciences, Hachioji, Tokyo 192-0392, Japan (K.N.); Grup de Recerca 26

en Biologia de les Plantes en Condicions Mediterranies, Departament de Biologia, 27

Universitat de les Illes Balears, Carretera de Valldemossa Km 7.5, 07122 Palma de 28

Mallorca, Spain (J.F., M.R.-C.); Max-Planck Partner Group at the Departamento de 29

Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais 36570-000, 30

Brazil (W.L.A.); Área de Ecología, Dpto. Sistemas Físicos, Químicos y Naturales, 31

Universidad Pablo de Olavide, Cta. de Utrera km 1, 41013 Sevilla, Spain (A.G.-N.) 32

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Author contributions 34

I.F-S., K.N. and M. R-C conceived the research plan and designed the experiments. I.F-35

S. and K.N. performed all the respiration measurements. I.F-S., K.N and A. G-N. 36

performed all the photosynthesis measurements and sampling for protein and metabolic 37

analyses. M.R-C. and J.F. supervised the respiration and photosynthesis experiments 38

and discussed the data. W.L.A. performed the GC-MS metabolite profiling analysis and 39

data generated was analyzed by I.F.S together with A.R.F. Western blot and pyridine 40

nucleotide analyses were performed by I.F.S. I.F-S. and K.N. wrote the manuscript. 41

A.R.F., J.F. and M.R-C assisted with the writing of the manuscript. All authors read and 42

approved the final manuscript after critical revision. 43

44

One sentence summary: 45

The cytochrome oxidase pathway mediates photorespiratory glycine oxidation and 46

amino acid synthesis under severe light stress, thus reducing photoinhibition when 47

alternative oxidase is not induced. 48

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Footnotes: 51

52 1This work was supported by funding the Spanish Ministry of Science and Innovation 53

(MICINN) project BFU2008-1072/BFI and BFU2011-23294 (J.F., M.R.-C., I.F.-S.), the 54

Max Planck Society (A.R.F. and W.L.A.) and the Alexander von Humboldt Foundation 55

(I.F.-S.). 56 2These authors contributed equally to this work. 57

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*Author to whom correspondence should be sent: Email: [email protected] 59

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The author(s) responsible for distribution of materials integral to the findings presented 61

in this article in accordance with the policy described in the Instructions for Authors 62

(www.plantphysiol.org) is: Miquel Ribas-Carbo (e-mail: [email protected]) 63

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ABSTRACT 65

The cyclic electron flow around photosystem I (CEF-PSI) increases ATP/NADPH 66

production in the chloroplast acting as an energy balance mechanism. Higher export of 67

reducing power from the chloroplast in CEF-PSI mutants has been correlated with 68

higher mitochondrial alternative oxidase (AOX) capacity and protein amount under high 69

light (HL) conditions. However, in vivo measurements of AOX activity are still required 70

to confirm the exact role of AOX on dissipating the excess of reductant power from the 71

chloroplast. Here, CEF-PSI single and double mutants were exposed to short-term HL 72

conditions. Chlorophyll fluorescence, in vivo activities of the cytochrome oxidase (νcyt) 73

and AOX (νalt) pathways, levels of mitochondrial proteins, metabolite profiles and 74

pyridine nucleotides levels were determined under normal growth and HL conditions. 75

νalt was not increased in CEF-PSI mutants while AOX capacity was positively 76

correlated with photoinhibition, probably due to a ROS-induced increase of AOX 77

protein. The severe metabolic impairment observed in CEF-PSI mutants, as indicated by 78

increase in photoinhibition and changes in the levels of stress-related metabolites, can 79

explain their lack of νalt induction. By contrast, νcyt was positively correlated with 80

photosynthetic performance. Correlations with metabolite changes suggest that νcyt is 81

coordinated with sugar metabolism and stress-related amino acid synthesis. 82

Furthermore, changes in glycine/serine and NADH/NAD+ ratios were highly correlated 83

to νcyt. Taken together, our results suggest that νcyt can act as a sink for the excess of 84

electrons from the chloroplast probably via photorespiratory glycine oxidation thus 85

improving photosynthetic performance when νalt is not induced under severe HL-stress. 86

87

88



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INTRODUCTION 89

Respiration in leaf tissues is influenced by their photosynthetic metabolism while 90

respiratory metabolism affects photosynthesis. This forward-reverse interaction between 91

photosynthesis and respiration has received a great attention during the last decades 92

(Krömer, 1995; Atkin et al., 2000; Raghavendra and Padmasree, 2003; Flexas et al., 93

2006; Yoshida and Noguchi, 2010; Araujo et al., 2014a; Obata et al., 2016). Essentially, 94

while photosynthesis provides carbohydrates for glycolysis, mitochondrial metabolism 95

in illuminated leaves supports photosynthesis, photorespiration, nitrogen metabolism 96

and export of redox equivalents (Yoshida and Noguchi, 2010). Among different redox 97

shuttles, the malate valve operates between chloroplasts, cytosol and mitochondria 98

(Scheibe, 2005) thus allowing the oxidation of chloroplast reductants by the 99

mitochondrial electron transport chain (mETC) (Yoshida and Noguchi, 2010). 100

Particularly under high light (HL) conditions, the alternative components of the mETC 101

have been suggested to accomplish non-phosphorylating oxidation of the excess of 102

reductants from the chloroplast (Yoshida and Noguchi, 2010). 103

104

The plant mETC is highly branched as compared to mitochondria from other eukaryotic 105

cells given that it contains different alternative components that bypass the main 106

complexes of the oxidative phosphorylation pathway- the cytochrome c oxidase (COX) 107

pathway (Rasmusson et al., 2008). Among these energy-bypass systems, the mETC is 108

branched at the ubiquinone (UQ) pool from which the electrons of ubiquinol are used 109

by the alternative oxidase (AOX) to reduce oxygen to water without proton 110

translocation (Moore & Siedow, 1991). In this way, AOX activity can bypass complex 111

III and COX (Complex IV) greatly reducing the efficiency of ATP synthesis by the 112

mETC. Several years ago, it was shown that the AOX pathway competes with the COX 113

pathway for the electrons of the UQ pool (Hoefnagel et al., 1995; Ribas-Carbo et al., 114

1995). These findings imply that the actual in vivo electron partitioning between the 115

COX and AOX pathways can be determined by oxygen isotope fractionation during 116

respiration but not using chemical inhibitors of the two pathways (Day et al., 1996; 117

Ribas-Carbo et al., 2005). While several theories have been formulated about the role of 118

AOX in plants (Gupta et al., 2009; Rasmusson et al., 2009; Van Aken et al., 2009; 119

Vanlerberghe, 2013), there is still little confirmation of such roles by measuring AOX 120

activity in vivo as determined by oxygen isotope fractionation (Yoshida and Noguchi, 121

2010; Vanlerberghe, 2013). 122



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123

Transgenic approaches altering mitochondrial metabolism have provoked different 124

effects on photosynthesis in plants with suppressed tricarboxylic acid (TCA) cycle 125

enzymes (reviewed in Nunes-Nesi et al., 2011; Araujo et al., 2014a) or mETC 126

components (Dutilleul et al., 2003; Sweetlove et al., 2006; Galle et al., 2010; Florez-127

Sarasa et al., 2011; Dahal et al., 2014). Genetic mutations in the main components of 128

the respiratory chain such as Complex I have drastic effects on photosynthesis and 129

photorespiration (Dutilleul et al., 2003; Priault et al., 2006; Galle et al., 2010) and 130

changes on the in vivo electron partitioning were also observed under drought stress and 131

cell death (Galle et al., 2010; Vidal et al., 2007). In respect to the alternative 132

components of the mETC, uncoupling protein (UCP) mutants in Arabidopsis have 133

shown altered photosynthesis due to a limitation on photorespiration (Sweetlove et al., 134

2006). Regarding the AOX, an important role in optimizing photosynthesis has been 135

reported in both Arabidopsis thaliana and tobacco (Yoshida et al., 2011; Florez-Sarasa 136

et al., 2011; Gandin et al., 2012; Dahal et al., 2014), including one study of the AOX 137

activity in vivo under HL conditions (Florez-Sarasa et al., 2011). Using AOX transgenic 138

plants, as an approach to determine its in vivo role, it has recently been confirmed that 139

AOX is involved in preserving photosynthetic capacity under drought stress by reducing 140

chloroplast overreduction and photodamage (Dahal et al., 2014; 2015). 141

142

As another approach to unravel the role of AOX in photosynthesis, respiratory 143

properties have been examined in photosynthetic mutants including the cyclic electron 144

flow around photosystem I (CEF-PSI) mutants and the FtsH2 metalloprotease required 145

for the repair of damaged photosystem II (PSII) (Yoshida et al. 2007; 2008). In the 146

study of Yoshida et al. (2007), the authors reported a correlation between higher export 147

of excess reductant power from the chloroplast with higher AOX capacity and protein 148

amount in A. thaliana mutants with altered CEF-PSI following HL treatment. These 149

mutants showed higher AOX capacity and protein amount even under low light 150

conditions. Importantly, a general lack of relationship between the AOX protein content 151

and its in vivo activity has been reported in HL stress experiments using A. thaliana 152

plants (Florez-Sarasa et al., 2011). Therefore, AOX in vivo activity measurements are 153

crucial for elucidating the possible role of AOX on dissipating the excess of reductant 154

power from the chloroplast. 155

156



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Since various primary metabolites are involved in interactions between chloroplasts and 157

mitochondria such as photorespiration and reductant transport, levels of primary 158

metabolites may be changed following deficiencies in photosynthesis or respiration and 159

by environmental perturbations. We have previously demonstrated that a large number 160

of metabolites increased in leaves of A. thaliana growing in or transiently exposed to 161

HL (Florez-Sarasa et al., 2012). The AOX1a deficiency in A. thaliana altered the levels 162

of certain metabolites, such as sugars and sugar phosphates, in the shoots under low 163

nitrogen stress (Watanabe et al., 2010). However, changes in primary metabolite levels 164

have not yet been related with in vivo partitioning between COX and AOX pathways in 165

photosynthetic (i.e. CEF-PSI) mutants. 166

167

Here, we investigated the effects of HL treatment on the in vivo activities of COX and 168

AOX pathways in leaves of A. thaliana mutants defective in CEF-PSI. Our hypothesis 169

is that CEF-PSI mutants will present higher in vivo flux through AOX for dissipating 170

the excess of reducing power from the chloroplast under HL conditions. We also 171

examined photosynthetic properties using chlorophyll fluorescence and determined 172

mitochondrial proteins and primary metabolite levels, in an attempt to clarify the 173

underlying mechanisms regulating the in vivo activities of COX and AOX pathways 174

under HL. 175

176

RESULTS 177

178

Chlorophyll fluorescence parameters under growth light (GL) and after high light 179

(HL) treatment 180

Under GL conditions, photochemical (qP) and non-photochemical (qN, NPQ) 181

quenching were similar in wild-type (gl1) plants and single mutants (pgr5 and crr4-3) 182

(Fig. 2). qN and NPQ were also unaltered in double mutants (pgr5 crr4-3) compared to 183

the other lines (Fig. 2B and 2D) while qP was clearly lower in this genotype (Fig. 2A). 184

The quantum efficiency of PSII (ΦPSII) and the electron transport rate (ETR) were 185

similar in gl1, crr4-3 and pgr5 while both were lower in the pgr5 crr4-3 double mutants 186

(Fig. 2C and 2E). In addition, maximum efficiency of PSII (Fv/Fm) was also lower in 187

double mutants compared to the other three lines (Fig. 2F) and, in agreement, the 188

percentages of total (% TPI) and chronic (% CPI) photoinhibition in the double mutants 189

were significantly higher than in the other lines (Table I). 190



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191

Under HL conditions, qP was similarly decreased in all lines while NPQ and qN were 192

increased (Fig. 2A, 2B and 2D). During HL treatment, qN was significantly decreased 193

only in double mutants (Fig. 2B and 2D). NPQ was slightly but significantly reduced in 194

pgr5 and crr4-3 at 8h of HL treatment while it was much more reduced in double 195

mutants already at 4h of HL (Fig. 2B and 2D). ΦPSII and ETR were generally lower in 196

both pgr5 and double mutant compared to gl1 and crr4-3 (Fig. 2C and 2E). The ETR in 197

both gl1 and crr4-3 increased after 2h of HL and then decrease afterwards; this initial 198

increase was lacking in pgr5 and double mutant plant (Fig. 2E). On the other hand, 199

Fv/Fm was decreased in all lines after HL treatment (Fig. 2F). However, while Fv/Fm 200

displayed a similar decrease in gl1 and crr4-3, it was more reduced in pgr5 and the 201

double mutant, the later showing the lowest values after HL treatment (Fig 2F). Finally, 202

total % TPI was significantly higher in pgr5 and double mutants than in gl1 and crr4-3, 203

mainly due to higher % CPI (Table I). Among all the genotypes, double mutants 204

exhibited the highest values of % TPI and % CPI (Table I). Following the HL-205

induction, the % CPI was kept constant in all genotypes with the exception of the 206

double mutants in which it was further increased at 4h of HL (Table I). Finally, the 207

percentage of dynamic photoinhibition (% DPI) presented a similar pattern as qN and 208

NPQ in all genotypes. Thus, %DPI was increased and kept high along the HL treatment 209

in gl1 and crr4-3 plants; whereas it was further increased in pgr5 and double mutants 210

after 2h of HL but then decreased at 4h and 8h of HL (Table I). 211

212

In vivo activities of the COX and AOX pathways under GL and after HL 213

treatment 214

The rates of respiration in Figure 3 are presented on a dry weight (DW) basis due to the 215

differences in the specific leaf weight (leaf DW/Area) observed between lines (data not 216

shown). Under GL conditions, total respiration (Vt) as well as in vivo cytochrome 217

oxidase (νcyt) and alternative oxidase (νalt) pathway activities were similar in all four 218

genotypes (Fig. 3). However, the alternative oxidase capacity (Valt), which is a proxy of 219

the AOX protein content, was two-fold higher in double mutants compared to the other 220

lines (Fig. 3D). 221

222

Under HL, Vt significantly increased in all genotypes peaking at 2h and then decreased 223

towards the 8h after HL stress. However, the pgr5 and double mutants presented a 224



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lower HL-induction of Vt than gl1 and crr4-3 plants (Fig. 3A). Notably, the double 225

mutants were the less responsive genotype thus reaching similar Vt rates at 8h as in GL 226

conditions (Fig. 3A). The pattern of HL-induction of νcyt was similar to that of Vt (Fig. 227

3B). On the other hand, νalt was almost unchanged in all lines, with the exception of a 228

significant increase only in gl1 after 2h of high light treatment (Fig. 3C). However, Valt 229

exhibited a general induction pattern with the exception of the crr4-3 plants that kept 230

constant rates until 8h of HL treatment. Valt was significantly increased only in pgr5 231

(1.5 fold-increase) and double mutants (1.3 fold-increase) after 4 and 8h of HL 232

treatment (Fig. 3D), with the double mutants always exhibiting the highest Valt (Fig. 233

3D). 234

235

Relationships between photosynthetic parameters and in vivo respiratory activities 236

after HL treatment 237

The photosynthetic parameters obtained from chlorophyll fluorescence measurements 238

were correlated to the respiratory parameters determined by oxygen isotope 239

fractionation during respiration across genotypes under HL conditions (Table II, 240

Supplemental Fig. 1). Vt was positively and significantly correlated with the ETR, qN, 241

NPQ and Fv/Fm indicating both a direct link between respiration and photosynthetic 242

electron transport chain activity as well as its degree of photoinhibition under HL 243

conditions. Indeed, the % TPI was negatively and significantly correlated to Vt, with the 244

% CPI being the main contributor to the negative correlation to photoinhibition. It was 245

clearly observed that νcyt, but not νalt, was linked to the chloroplast electron transport 246

chain activity and its degree of photoinhibition under HL conditions (Table II). On the 247

other hand, almost all of the photosynthetic parameters significantly correlated with Valt. 248

Notably, the correlations of the photosynthetic parameters with Valt were in the opposite 249

direction to those observed with Vt and νcyt, thus being negative to photosynthetic 250

activity (i.e. ETR) and positive to photoinhibition (% TPI and % CPI). 251

252

Mitochondrial electron transport (mETC) chain protein levels under GL and after 253

HL treatment 254

Different mETC proteins were immunodetected by western blot analyses in whole leaf 255

extracts, including AOX, cytochrome oxidase subunit II (COX), and uncoupling protein 256

(UCP). In addition, porin levels were also determined as a control for mitochondrial 257



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protein loading, and remain similar in all the genotypes and light conditions (Fig. 4 and 258

Supplemental Fig. 2). Band intensities were quantified for all the proteins, and AOX, 259

COXII and UCP protein levels were obtained after correction by the corresponding 260

porin band intensities and then normalized to the levels of the gl1 plants under GL (i.e. 261

gl1 levels for all the proteins are 100%). Two independent experiments were performed 262

(see Materials and Methods section for further details) and the average of the two 263

relative quantifications is presented together with the image of the most representative 264

blot (Fig. 4). The levels of AOX protein were approximately two-fold higher in double 265

mutants than in the other genotypes under GL conditions (Fig. 4), which coincides with 266

the highest AOX capacity observed in this plants (Fig. 3D). By contrast, COX protein 267

levels were lower in the double mutants and UCP levels were similar in all genotypes 268

(Fig. 4). Following HL treatment, the levels of UCP and COX remain relatively 269

constant in all the genotypes as compared to their respective levels under GL, with the 270

exception of COX decreases observed after 8h of HL treatment in gl1 and crr4-3 plants 271

(Fig. 4). On the other hand, the levels of AOX protein were increased in all genotypes 272

after HL treatment, the crr4-3 presenting the lowest increases. After 8h of HL treatment, 273

pgr5 and double mutants presented the highest AOX levels i.e.-an approximately 3-fold 274

increase (Fig. 4). 275

276

Metabolite profiling and pyridine nucleotide levels under GL and after HL 277

treatment 278

A total of 49 metabolites were identified by using gas chromatography-mass 279

spectrometry (GC-MS) including several amino acids, organic acids, some sugars and 280

sugar alcohols (Fig. 5 and Supplemental Table SI). Mutant plants display significant 281

differences in the relative levels of some metabolites under GL conditions as compared 282

to the wild-type (gl1) plants (Fig. 5 and Supplemental Table SI). In all mutant lines, the 283

levels of aspartate, glutamate, and malate were significantly lower as compared to gl1 284

plants while glycerate was significantly higher. In pgr5 plants, the levels of arginine, 285

serine, GABA, fumarate, 2-oxo-butyrate and shikimate were significantly lower than in 286

gl1. On the other hand, the levels of ß-alanine, glycine, ornithine, spermidine, serine, 287

tryptophan, glucose, and glyceraldehyde-3-phosphate were significantly higher in crr4-288

3 than in gl1 plants, while the levels of arginine, asparagine, threonine, 2-oxoglutarate, 289

shikimate and myo-inositol were lower. Finally, the double mutants displayed higher 290

levels of beta-alanine, isoleucine, phenylalanine, 4-hydroxy-proline, serine, tryptophan, 291



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tyrosine, citrate, isocitrate, dehydroascorbate, galactonate and lactate. Among the above 292

mentioned metabolites significantly affected in all the mutant plants, only few 293

metabolites were changed by more than two-fold. Asparagine and glutamate were 0.5- 294

and 0.4-fold lower in crr4-3, whereas glycerate and glycine were 2.5- and 3.3-fold 295

higher than gl1, respectively. Tyrosine and tryptophan levels were 2.3- and 8.4-fold 296

higher in double mutants than in gl1. 297

298

After HL treatment, most of the metabolites were increased except for some organic 299

acids showing significant decreases such as ascorbate, glycerate and shikimate (Fig. 5 300

and Supplemental Table SI). Some metabolites displayed dynamic responses over time 301

after HL treatment (i.e. first increased and then decreased or vice versa) such as 302

mannitol, glucose, galactose, succinate, shikimate and lysine. Nevertheless, several 303

metabolites presented a genotype-specific response to the HL treatment such as glycine, 304

ascorbate among others. These metabolite changes are described below according to 305

their compound class. 306

307

Amino acids showed the highest increases after HL treatment with the exception of 308

cysteine, GABA, glutamine, isoleucine, leucine and putrescine which remained largely 309

unchanged. Glycine was the metabolite exhibiting the highest HL-induction, being 310

approximately 13-fold increase in gl1 and crr4-3 at 8h of HL. However, glycine levels 311

were increased approximately five-fold in pgr5 mutant and it was marginally increased 312

by less than two-fold in the double mutants after HL treatment. Proline was the second 313

most induced metabolite under HL, thus being progressively and similarly increased in 314

all genotypes until 8h of HL. Tyrosine levels increased after HL treatment in all 315

genotypes, and notably double mutants showed the highest levels after 8h of HL 316

(approximately 10-fold). Several other amino acids were showing about two-fold 317

increases after HL treatment. Alanine, ß-alanine and threonine were significantly and 318

continuously increased after HL treatment in all genotypes. Arginine, homoserine and 319

methionine were also significantly increased in all genotypes but to a lesser extent in 320

pgr5 and double mutants after 8h of HL. Glutamate was significantly increased in all 321

genotypes but to a lesser extent in gl1; aspartate showed a similar although less 322

pronounced response to glutamate. Valine was increased after 2h of HL and then 323

maintained at high levels in all genotypes. A similar trend was observed in 324

phenylalanine HL-response in general, although pgr5 and double mutants presented 325



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lower increases. Lysine levels increased after 2h of HL treatment and subsequently 326

decreased, this pattern being observed in all genotypes although the induction being less 327

pronounced in the double mutants. Asparagine displayed a similar pattern as lysine 328

except in gl1 plants. Finally, 4-hydroxy-proline, serine, spermidine and tryptophan 329

levels significantly increased after HL treatment in all genotypes but generally by less 330

than 2-fold. Ornithine level significantly increased after 8h HL only in gl1 and crr4-3 331

lines. 332

333

In contrast to the HL-induced changes in amino acids levels, organic acids displayed 334

some significantly and pronounced decreases, whereas increases of this compound class 335

were few. For instance, malate and 2-oxoglutarate levels were continuously increased 336

after HL treatment in all genotypes although the response of 2-oxoglutarate was less 337

pronounced in pgr5 and double mutants. Similarly, dehydroascorbate was increasing 338

over time in all genotypes but the response was much lower in the double mutants. 339

Also, citrate and fumarate levels presented slight but significant increases after HL in all 340

lines and the levels in the double mutants again displayed a milder, if any. Succinate 341

levels increased after 2h and then decreased towards the 8h of HL treatment; this pattern 342

was observed in all genotypes but the induction was less pronounced in the double 343

mutants. An inverse pattern was observed for shikimate for which the levels decreased 344

at 2h after HL in all genotypes but then increased at 4 and 8h after HL. The ascorbate 345

level was greatly and continuously decreased in gl1 and crr4-3 following HL treatment. 346

In pgr5 mutants, significant decreases in ascorbate were only observed after 4 and 8h 347

while a significant decrease was observed in double mutants only after 8h of HL. 348

Glycerate also significantly decreased to similar levels in all genotypes after HL 349

treatment, although the levels in crr4-3 were much higher under GL conditions. As 350

reported above, the levels of galactonate, isocitrate and lactate were significantly higher 351

in the double mutants in all conditions, and these metabolites were not generally altered 352

after HL treatment. Pyruvate levels remained mostly unchanged after HL treatment in 353

all the lines and the same was observed for 2-oxo-butyrate and benzoate except for 354

slight increases in the double mutant after 8h of HL. 355

356

With respect to the sugars and sugar alcohols, galactose, glucose and mannitol levels 357

peaked after 2h and then decrease towards the 8h of HL treatment in all genotypes and 358

again double mutants display a lower HL-response. Erythritol was also increased 359



13

although to a lesser extent and mostly at the end of the HL treatment in all genotypes. A 360

minor increase was also observed in glyceraldehyde-3-P levels but only apparent in gl1 361

plants. On the other hand, fructose and sucrose were not altered after HL treatment in 362

any genotype, as well as myo-inositol that was generally lower in crr4-3. 363

364

In addition to single metabolite levels, relevant redox-related ratios were calculated (for 365

details see Material and Methods section) and their HL-response was compared among 366

genotypes. The Glycine/Serine ratio was increasing over time thus reaching nine-fold 367

and ten-fold increase at 8h of HL in gl1 and crr4-3, respectively, while pgr5 showed a 368

reduced response (i.e. reaching a maximum of four-fold increase). More severely 369

dampened, double mutants exhibited a lack of HL-induction on glycine/serine ratio. The 370

malate/aspartate ratio was increased after HL in all the genotypes mostly after 8h of HL. 371

The glutamate/2-oxoglutarate ratio was much higher in gl1 under GL conditions as 372

compared to the other genotypes. The glutamate/2-oxoglutarate ratio decreased after 2h 373

HL treatment in gl1 and crr4-3 but not in pgr5 and double mutants. Finally, the 2-374

oxuglutarate/citrate ratio showed generally increases after HL treatment in all genotypes 375

that were less pronounced in pgr5 and double mutants. 376

377

In order to further investigate on the redox changes in the CEF-PSI mutants, we 378

measured the levels of NAD+, NADH, NADP+ and NADPH, and calculated the 379

corresponding redox ratios (Supplemental Fig. S3) in leaf samples of all genotypes and 380

light conditions. Generally, no statistical differences on pyridine nucleotide levels were 381

observed among genotypes when compared in each light condition. Nonetheless, some 382

trends were observed after HL treatment; the levels of NAD+ and NADH tended to 383

increase in all genotypes after HL treatment (Supplemental Fig. S3). After 8h of HL, gl1 384

showed the highest levels of NAD+ as compared to all other genotypes and conditions, 385

while double mutants displayed the highest levels of NADH. As for the NADH, the 386

highest levels of NADPH we detected in double mutants after 8h of HL. With regard to 387

the redox-related ratios, gl1 plants generally displayed the lowest NADH/NAD+ and 388

NADPH/NADP+ ratios while double mutants displayed the highest (Supplemental Fig. 389

S3). 390

391

Relationships between metabolite levels and respiratory activities after HL 392

treatment 393



14

In order to obtain insights into the metabolic regulation or metabolic processes involved 394

in the different respiratory response to HL observed in the CEF around PSI mutants, 395

Pearson correlation coefficients were calculated between the fold-changes of metabolite 396

levels and those of respiratory activities parameters across all four genotypes. 397

Respiratory data were normalized to the mean of gl1 plants under GL conditions as was 398

done for the relative metabolite levels calculations, thus allowing 15 point correlations 399

using the means for each genotype and light treatment. Positive (red) and negative 400

(blue) significant values (P<0.05) of the r-Pearson coefficients are shown in Figure 6. 401

All correlation plots derived from significant (P<0.05) correlations are shown in 402

Supplemental Figure 4. 403

404

Changes in several amino acids, as affected by the genotype and the HL treatment, 405

correlated positively and significantly with changes in total respiration rates (Vt), 406

including glycine, lysine, alanine, phenylalanine, homoserine, methionine, and valine. 407

Only isoleucine changes were negatively correlated to Vt. Regarding organic acids, 408

TCA cycle intermediates such as fumarate, 2-oxoglutarate, succinate and pyruvate were 409

also positively correlated to Vt, while glycerate was negatively correlated to it. On the 410

other hand, sugars such as glucose, galactose, sucrose and the sugar alcohol mannitol 411

were positively correlated to Vt. With regard to redox ratios, glycine/serine and to a 412

lesser extent 2-oxoglutarate/citrate ratios were positively correlated to Vt. In addition, 413

only NADH/NAD+ ratios were significantly and negatively correlated with in vivo 414

respiratory activities. 415

416

Notably, most of the observed significant correlations to Vt were mainly driven by νcyt 417

which in addition was showing positive correlation to arginine, threonine and malate, 418

and negative to ascorbate and benzoate. On the other hand, changes in νalt were 419

presenting only positive correlation to mannitol and negative correlations to glutamine 420

and leucine. Among all the correlations presented in Figure 6, glucose and glycine/ 421

serine ratio with Vt and νcyt were showing the highest Pearson coefficient. 422

423

DISCUSSION 424

The high light (HL) treatment caused a severe stress response in pgr5 and double 425

mutants 426



15

The photosynthetic response of the wild-type (gl1) and the crr4-3 single mutant plants 427

after the HL treatment was generally similar while a severely impaired photosynthetic 428

response was observed in pgr5 and double mutants. The pgr5 mutant is deficient in the 429

ferredoxin (Fd) -dependent CEF-PSI pathway (Munekage et al., 2002), while crr4-3 is 430

deficient in the NAD(P)H dehydrogenase (NDH)-dependent pathway (Kotera et al., 431

2005). While the Fd-dependent CEF-PSI is thought to be the predominant pathway in 432

C3 photosynthesis, the NDH complex may act as a safety valve that prevents over-433

reduction of the stroma (Shikanai, 2007). Although the quantum efficiency of PSII 434

(ΦPSII) and photochemical quenching (qP) were greatly decreased in wild-type (gl1) 435

plants and the crr4-3 after 2h of HL treatment, both genotypes presented an enhanced 436

electron transport rate after 2h of HL that was decreased towards the end of the light 437

treatment. The NPQ and qN values were also up-regulated after 2h of HL in all 438

genotypes and this up-regulation was maintained during the HL treatment except for the 439

double mutant. In prg5 crr4-3 at HL, both the linear electron flow and CEF-PSI were 440

suppressed (Shikanai, 2007). Thus the proton gradient across the thylakoid membrane 441

(ΔpH) may be more gradual in the double mutant, and thereby the NPQ and qN values 442

were decreased. This HL-inhibition of photosynthetic activity was related to the high 443

level of photoinhibition denoted by the low Fv/Fm levels (Fig. 2) and increasing levels 444

of calculated photoinhibition (Table I). Indeed, the percentage of total photoinhibition 445

(% TPI) observed in wild-type (gl1) was higher, around 40% (Table I), as compared to 446

previously reported % TPI, i.e. less than 30%, in Arabidopsis Col-0 plants under very 447

similar HL conditions (Florez-Sarasa et al., 2011). We used Arabidopsis gl1 (glabra1) 448

that is deficient in trichome of leaves (Oppenheimer et al., 1991) and plants on the 449

different developmental stage. Since trichomes can attenuate strong light (Steyn et al., 450

2002), this may explain the severity of the stress response observed in this study. In 451

particular, the pgr5 and double mutant (pgr5 crr4-3) were characterized by a very high 452

percentage of chronic photoinhibition (% CPI) after the HL treatment (Table I). A high 453

% CPI is associated to damage of the PSII (Osmond, 1994; Demming-Adams et al., 454

2012) mostly due to increased ROS production at the chloroplast electron transport 455

chain (Pinto-Marijuan and Munné-Bosch, 2014). In this respect, the observed decreases 456

in ascorbate levels and increases dehydroascorbate levels after HL stress (Fig. 4) denote 457

an important ROS-induced antioxidant response, as compared to the previously reported 458

and minor HL-induced changes of these metabolites in Arabidopsis Col-0 plants 459

(Florez-Sarasa et al., 2012). In addition, proline accumulated at very high levels in all 460



16

genotypes, particularly after 8h (Fig. 4). Proline is involved in ROS-detoxification 461

under many abiotic stresses (Szabados and Savouré, 2010), and notably 4-hydroxy-462

proline levels, a product of proline oxidation, was higher in the double mutants than in 463

the other genotypes. In addition, other stress-related metabolites such as ß-alanine (Stiti 464

et al., 2011) and tyrosine (Yoo et al., 2013) were higher in the double mutants at growth 465

light (GL) and further accumulated after HL, as compared to the other genotypes. 466

Particularly, the most increased metabolite in double mutants was tryptophan, which is 467

a precursor for the synthesis of secondary metabolites such as phytoalexins, 468

glucosinolates and alkaloids, and also of the hormone auxin (Radwanski and Last, 1995; 469

Zhao, 2012). The reduced growth, previously observed in Munekage et al. (2004) and 470

Yamamoto et al. (2011), and stress-related phenotype of the double mutants may be 471

related to the tryptophan accumulation although further research will be needed to 472

unravel the nature of this metabolic alteration. 473

474

The AOX pathway activity in vivo was not higher in CEF-PSI mutants thus 475

partially refuting the initial hypothesis 476

The AOX is hypothesized to be activated in order to dissipate the excess of reducing 477

equivalents under HL stress (Yoshida et al., 2007). Therefore, a higher in vivo AOX 478

activity (νalt) was expected in pgr5 and double mutants due to an even higher excess of 479

reductants in the chloroplast than gl1 and crr4-3 plants. Surprisingly, νalt in the pgr5 and 480

double mutant was not significantly changed after HL treatment, while it was 481

significantly increased in gl1 plants after 2h of HL as previously reported in 482

Arabidopsis Col-0 plants (Florez-Sarasa et al., 2011; 2012). By contrast, the AOX 483

capacity was more HL-induced in pgr5 after than in gl1 plants as previously reported 484

(Yoshida et al., 2007). More importantly, double mutants presented the highest AOX 485

capacity (Valt) even under GL conditions, and it was also significantly increased after 486

HL. Furthermore, Valt presented the highest positive correlation to % CPI, while 487

negative correlations with photosynthetic activity, i.e. ETR (Table II), were observed. 488

These results suggest that the production of ROS associated to the high %CPI 489

(Demmig-Adams et al., 2012) probably increased the ROS-mediated signal that induces 490

the AOX expression (Rhoads et al., 2006) and as a consequence its capacity. Indeed, the 491

levels of AOX protein were higher in double mutants under GL conditions and were 492

further induced after HL treatment (Fig. 4), thus following very similar patterns as Valt 493

(Fig. 3D). On the other hand, the slightly better photosynthetic performance (i.e. higher 494



17

ETR, NPQ, and lower % CPI), as compared to gl1, observed in crr4-3 mutants may 495

partially explain their lack of Valt response following HL treatment. However the nature 496

of the absence of such a response of Valt in crr4-3 remains unclear. That said it appears 497

reasonable to assume that the milder HL-response of the AOX protein levels is the 498

limiting factor of the Valt and νalt response in crr4-3 mutants. The ROS-mediated 499

signaling pathway that induces AOX expression is not fully understood yet (Liu et al., 500

2013). Notably, the AOX was mostly induced in green but not in white areas from 501

leaves of yellow variegated mutants exposed to HL stress (Yoshida et al., 2008) thus 502

denoting that chloroplast photooxidative stress was influencing AOX protein synthesis. 503

The AOX expression and capacity was previously well correlated in CEF-PSI mutants 504

under HL stress (Yoshida et al., 2007), although this does not indicate the in vivo 505

activity (Florez-Sarasa et al., 2011). In this respect, data presented in Figures 3 and 4 are 506

in the line of previous observations, thus confirming that induction of both AOX 507

capacity and protein levels is not always associated to an increase on in vivo AOX 508

activity (i.e.- as in the double mutants). Indeed, it has been demonstrated that AOX is 509

inhibited by lipid peroxidation products (Winger et al., 2005) which are likely to be 510

produced under the photooxidative stress conditions applied in this study. 511

512

In vivo COX instead of AOX activity mediated the mitochondrial response to 513

severe HL stress and was highly coordinated with photosynthetic performance 514

As mentioned above, the νalt was not increased in double mutants under severe HL 515

stress conditions probably due to a ROS-inactivation of the AOX. Moreover, the νalt 516

was also decreasing in gl1 plants from its levels at 2h towards 4h and 8h of HL (Fig. 3). 517

On the other hand, COX pathway activity (νcyt) was significantly induced in all lines 518

after HL treatment (Fig. 3). The observed νcyt induction was not due to COX protein 519

level modifications since the levels of immunodetected COXII in all genotypes were 520

either similar or lower in HL than in GL conditions; these results indicate that COX 521

protein level did not limit mETC activity and increased flux through COP may lead to 522

greater turnover of COX protein. Moreover, νcyt but not νalt was significantly and 523

positively correlated with photosynthetic activity (ETR) and non-photochemical 524

quenching (NPQ) (Table II, Supplemental Fig. 1). Increases in the linear electron flow 525

of PSII induce a proton gradient across thylakoid membranes (ΔpH) which leads to an 526

induction of NPQ (Shikanai, 2007). Also, νcyt was negatively correlated to total (% 527



18

TPI) and chronic (% CPI) photoinhibition. Therefore, νcyt was correlated with a better 528

photosynthetic performance under severe HL stress. While ATP provision by νcyt has 529

been reported as an important role for mitochondrial metabolism in leaves under 530

illumination, there is a high need for energy dissipation under HL conditions that can be 531

accomplished by mitochondrial metabolism (Yoshida and Noguchi, 2010). In this 532

respect, it has been proposed that COX pathway can also allow an uncoupled electron 533

transport under situations of chronic oxidative stress through the activation of the 534

uncoupling proteins (UCPs) (Rasmusson et al., 2009). In the present study, UCP protein 535

levels were generally similar among genotypes and no substantial changes were 536

detected after HL treatment (Fig. 4). However, post-translational activation of UCP 537

proteins cannot be discarded. Indeed, UCP has been shown to be activated by lipid 538

peroxidation products (Vercesi et al., 2006) which would inhibit νalt but not νcyt as 539

observed in here. 540

541

In vivo COX activity is highly coordinated with photorespiratory and amino acid 542

metabolism 543

The active CEF-PSI in gl1 plants after 2h of HL can diminish the excess of reducing 544

power by balancing NADPH/ATP levels and therefore keep an active and less ROS-545

damaged chloroplast electron transport chain. The increased ETR observed in gl1 and 546

crr4-3 plants produced NADPH and ATP, not only for carbon assimilation but also for 547

photorespiration and the export of reductants via malate valve (Yoshida and Noguchi, 548

2010). The three processes co-occurring at HL provide NAD(P)H to the mitochondrial 549

electron transport chain via sugar oxidation, glycine decarboxylation and malate 550

oxidation. Under these conditions, both COX and AOX pathways were oxidizing all the 551

reductant power from the chloroplast as observed in gl1 plants after 2h HL. Indeed, in a 552

very recent study in Arabidopsis AOX1a mutants, we have shown that AOX pathway 553

can support photorespiration under high light conditions (Watanabe et al., 2016). 554

However, when the light stress conditions were more severe (indicated by higher levels 555

of photoinhibition) only the COX but not the AOX pathway was showing a response to 556

HL-stress. Moreover, the impairment of the CEF around PSI in double mutants caused 557

severe damage on the photosynthetic electron transport chain already after 2h of HL, as 558

indicated by the highest levels of CPI. Such severe impairment of the chloroplast ETR 559

probably restricted the generation of chloroplast derived substrates/reductants by any of 560



19

the three processes commented above and thus limited the response of the 561

mitochondrial electron transport chain. Importantly, the statistically significant 562

correlation observed between in vivo respiratory activities and the NADH/NAD+ ratio 563

supports this view (Fig. 6). 564

565

In order to better understand the metabolic links involved in the attenuated respiratory 566

response as a consequence of CEF-PSI impairment under HL, metabolite profiles were 567

analyzed and also their correlation to the respiratory activities in vivo (Fig. 6, 568

Supplemental Fig. 4). The induction pattern of sugar levels such as sucrose, galactose 569

and especially glucose, was highly correlated to νcyt possibly indicating the fueling of 570

respiration by the increase on photosynthetic-derived substrates. In relation to this, 571

pyruvate and TCA cycle intermediates such as succinate, fumarate and 2-oxoglutarate 572

as well as 2-oxoglutarate/ citrate ratio were showing also positive and significant 573

correlations to νcyt. 2-oxoglutarate is a key metabolite in nitrogen metabolism being 574

used as carbon skeleton for amino acid synthesis (Araujo et al., 2014b). In the present 575

study, νcyt was also positively correlated to several amino acids. Taken together, the 576

correlations observed suggest that νcyt may oxidase matrix NADH providing ATP and 577

allowing TCA cycle carbon flow towards amino acid and protein synthesis under severe 578

HL. Proline synthesis requires carbon flow from 2-oxoglutarate and glutamate as well 579

as ATP (Szabados and Savouré, 2010) and remarkably, it was one of the highest 580

accumulated metabolite following HL treatment in all genotypes. Although not being 581

directly correlated to νcyt, a high synthesis of this ROS-protective metabolite can be 582

speculated and which would likely require a high rate of ATP-coupled respiration. In 583

this line, significant and positive correlations of νcyt with phenylalanine may also 584

indicate a high ATP demand for the synthesis of secondary metabolites with an 585

important protective role under HL conditions (Tohge et al., 2013). Also tyrosine was 586

continuously accumulated after HL treatment in very high levels, particularly in double 587

mutants that showed the highest levels after 8h of HL (10-fold increase). Recently a 588

new alternative pathway has been described to link tryrosine and phenylalanine 589

metabolism (Yoo et al., 2013), presenting the possibility that tyrosine accumulation also 590

contributes to the synthesis of the secondary metabolites derived from phenylalanine 591

(Tohge et al., 2013). In addition, given that phenylalanine is a precursor for UQ 592

biosynthesis (Block et al., 2014; Toghe et al., 2014) correlations to an enhanced νcyt 593



20

under HL appear to reveal direct metabolic links to the mitochondrial electron transport 594

which warrant further investigation. 595

596

Finally, glycine was the metabolite which exhibited the greatest increase following HL 597

treatment as previously observed in Arabidopsis Col-0 plants after HL treatment 598

(Florez-Sarasa et al., 2012) and suggests a high photorespiratory activity (Timm and 599

Bauwe, 2013). However, this increase was much lower in pgr5 and, more strikingly, it 600

was almost abolished in the double mutants as compared to gl1 and crr4-3. These 601

results denote a link between CEF-PSI and photorespiration. Recently, it has been 602

reported that CEF-PSI is increased under photorespiratory and HL conditions, thus 603

denoting the cooperation of both processes as energy balancing mechanisms under HL 604

conditions (Walker et al., 2014). Photorespiration under HL contributes to the 605

consumption of the excess of reducing power thus acting as a photoprotective 606

mechanism to avoid photoinihibiton (Takahashi and Badger, 2011). Thus a high 607

photorespiratory flux, as expected in the HL conditions applied in this study, produced a 608

huge increase in glycine which is a major substrate for mitochondria in illuminated 609

leaves (Dry et al., 1983; Igamberdiev et al., 1997). In agreement, glycine and the 610

glycine/ serine ratio showed amongst the highest correlation coefficients with the νcyt, 611

which suggests that COX pathway can be involved in the re-oxidation of the NADH 612

from glycine decarboxylation. In parallel, νcyt was also highly and negatively correlated 613

to NADH/NAD+ ratios and glycerate which is one of the typical metabolites altered in 614

photorespiratory mutants (Timm and Bauwe, 2013). Interestingly, Sweetlove et al. 615

(2006) found that an uncoupled mitochondrial electron transport by the action of UCP 616

was important to keep the photorespiratory oxidation of glycine to serine, which in turn 617

benefits photosynthetic performance. Taken together, these observations strongly 618

suggest that the νcyt permits the oxidation of NADH derived from a HL-stimulated 619

glycine to serine decarboxylation under severe oxidative stress in cooperation with 620

active UCPs. In this way, the νcyt can act as a sink for the excess of electrons from the 621

chloroplast via photorespiratory glycine oxidation thus improving photosynthetic 622

performance and reducing photoinhibition when νalt is not induced due to severe HL-623

induced oxidative stress. Notably, νcyt was more increased in AOX1a antisense plants 624

than in WT under HL, thus compensating for the lack of νalt increase under HL (Florez-625

Sarasa et al., 2011). 626



21

627

CONCLUSIONS 628

The in vivo activities of the mitochondrial COX and AOX pathways were studied for 629

the first time in cyclic electron flow around PSI (CEF-PSI) mutants under growth and 630

high light (HL) conditions. In addition, the AOX pathway capacity was also determined 631

and was highly and positively correlated to photoinhibition probably due to the effect of 632

photosynthetic-derived-ROS on the observed induced AOX expression. However, the 633

AOX pathway activity in vivo (νalt) was not higher in CEF-PSI mutants than in wild-634

type (gl1) plants under HL conditions, thus partially refuting our hypothesis. The severe 635

metabolic impairment observed in CEF-PSI mutants may underlie the reason for the 636

lack of AOX activity response (i.e. due to an inactivation by lipid peroxidation products 637

(Winger et al., 2005)), which was indeed engaged in the less severely stressed gl1 plants 638

after 2h of HL treatment, in agreement with previous results (Florez-Sarasa et al., 2011; 639

2012) and suggestions (Yoshida et al., 2007). Despite the severity of the HL stress, the 640

COX activity in vivo (νcyt) was induced in all genotypes and it was tightly linked to their 641

photosynthetic performance. The correlations with metabolite changes suggest that νcyt 642

is highly coordinated with stress-related amino acid synthesis. More strikingly, the 643

severely attenuated response of the glycine to serine ratio in pgr5 and double mutants 644

suggest an impaired photorespiration that was correlated with an attenuated response of 645

the νcyt. In addition, NADH/NAD+ ratios were strongly and negatively correlated with 646

νcyt. We propose that νcyt can act as a sink for the excess of electrons from the 647

chloroplast via photorespiratory glycine oxidation, thus reducing photoinhibition when 648

νalt is not induced under severe HL-stress. These observations open new perspectives for 649

further studies on the in vivo role and regulation of the mETC in leaves under HL-stress. 650

We speculate that such new in vivo role of COX pathway can be partially accomplished 651

through an ATP-uncoupled electron transport (i.e. ROS-activation of uncoupling 652

proteins), although more experiments will be needed to establish the exact mechanism 653

by which this is occurring. 654

655

MATERIAL AND METHODS 656

657

Plant material and growth conditions 658



22

Plants of Arabidopsis thaliana wild type (ecotype Columbia gl1) and mutants in a 659

growth chamber (Fitotron UIB) under controlled conditions: temperature of 25ºC, 660

relative humidity above 40%, 12 h of photoperiod and light intensity of 80 µmol m-2 s-1 661

(growth light conditions, GL). Plants grown for 4-5 weeks under GL were transferred 662

for 2, 4 and 8 hours to 800 µmol m-2 s-1, considered HL conditions. A. thaliana pgr5 663

(proton gradient reduction) is deficient in the Fd-dependent CEF-PSI pathway 664

(Munekage et al., 2002), while crr4-3 (chlororespiratory reduction) is deficient in the 665

NDH-dependent pathway (Kotera et al., 2005). Also, a double mutant pgr5 crr4-3 was 666

gifted by Prof. Toshiharu Shikanai. The rosettes of the pgr5 and crr4-3 single mutants 667

were slightly smaller than gl1 plants after 4 weeks of growth. On the other hand, double 668

mutants presented pale leaves and growth was more affected and therefore this genotype 669

was grown for 5 weeks in order to reach similar developmental stage (i.e. number of 670

leaves) than the other three genotypes (Figure 1). 671

672

Chlorophyll fluorescence 673

The quantum efficiency of PSII (ΦPSII) was obtained from chlorophyll fluorescence 674

measurements in the light by setting actinic light of a portable pulse amplitude 675

modulation fluorometer (PAM-2000, Walz, Effeltrich, Germany) to 80 or 800 µmol m-2 676

s-1 for growth light and HL measurements, respectively. Chloroplast electron transport 677

rate (ETR) was calculated as the product of ΦPSII x actinic light intensity x 0.84 x 0.5. 678

In addition, photochemical (qP), non-photochemical quenching (qN, NPQ) and 679

maximum quantum efficiency of PSII (Fv/Fm) were obtained from chlorophyll 680

fluorescence measurements in the light and after 30 minutes dark adaptation with the 681

PAM-2000 fluorometer. Also, total, chronic and dynamic photoinhibition were obtained 682

as previously described in Florez-Sarasa et al. (2011) with slight modification; in the 683

present study, the Fv/Fmmax value was obtained from the mean value of Fv/Fm30 under 684

GL for gl1 plants (i.e. % CPI in gl1 plants is 0), in order to compare all the data to the 685

gl1. Ten to twelve replicates were performed per line and experimental condition. 686

687

Respiration measurements 688

Measurements oxygen isotope fractionation during respiration were performed as 689

described in Florez-Sarasa et al. (2007) to determine the activities of the cytochrome 690

oxidase (COX) and alternative oxidase (AOX) pathways in vivo. The oxygen isotope 691

fractionation of the AOX pathway required for the electron partitioning calculation 692



23

(Guy et al., 1989) was determined after 10 mM KCN incubation as previously described 693

(Florez-Sarasa et al., 2007); a mean value of 30.5‰ was used from all the 694

measurements performed in the mutant and wild-type plants because no differences 695

were observed among genotypes (data not shown). On the other hand, the oxygen 696

isotope fractionation of the AOX pathway (Δc) value of 20.9‰ was taken from 697

previously measured in Arabidopsis thaliana leaves (Florez-Sarasa et al., 2007). Four to 698

five replicates per line and experimental condition were performed. 699

700

In addition, the AOX capacity was determined with a Clark-type oxygen electrode as 701

previously described (Florez-Sarasa et al., 2009). Four to ten replicates per line and 702

experimental condition were performed. 703

704

Metabolite profiling and pyridine nucleotides determinations 705

Metabolite extractions were performed as described previously (Lisec et al., 2006) using 706

approx. 150 mg of frozen-powdered leaf tissue. Derivatization and gas chromatography-707

time of flight-mass spectrometry (GC-TOF-MS) analyses were carried out as described 708

previously (Lisec et al., 2006). Metabolites were manually identified using the 709

TagFinder plug-in of the TagFinder software (Luedemann et al., 2008) and the reference 710

library mass spectra and retention indices housed in the Golm Metabolome Database 711

(http://gmd.mpimp-golm.mpg.de (Kopka et al., 2005)). The metabolite ratios were 712

calculated by dividing the signal intensities of the selected masses for the corresponding 713

metabolites and no calibration was performed with known concentrations of the 714

reference compounds; therefore, the ratios obtained are only used to compare their HL-715

responses among the different genotypes but they are not indicating the absolute (actual) 716

ratios. Data were normalized to the mean value of wild-type (gl1) plants at GL 717

conditions (i.e. the value of all metabolites and ratios for gl1 at GL was set to 1). Values 718

presented are the mean ± SE of six replicates, each replicate representing a pool of three 719

rosettes. 720

For pyridine nucleotides, two aliquots of 25 mg each of frozen-powdered leaf tissue (i.e. 721

from the same frozen-powdered used for GC-MS metabolite analysis) were used to 722

determine the reduced (NADH, NADPH) and the oxidized forms (NAD+, NADP+). 723

Extractions and spectrophotometer determinations were performed as described by 724

Kühn et al. (2015). 725

726



24

Western blotting 727

Aliquots of 20 mg of frozen-powdered leaf tissue (i.e. from the same frozen-powdered 728

used for GC-MS metabolite analysis) was used to extract proteins by adding 100 ul of 729

SDS sample buffer [2% (w/v) SDS, 62.5mM Tris–HCl (pH 6.8), 10% (v/v) glycerol and 730

0.007% (w/v) bromophenol blue] and including 50mM DTT and a protease inhibitor 731

tablet (Roche). Samples were then incubated for 30 min in ice to allow full reduction of 732

AOX protein. Thereafter samples were boiled at 95ºC for c. 5 min and the homogenate 733

was centrifuged at 14000 rpm for 10 min. The supernatant was transferred into a new 734

tube and kept at -20ºC for later analysis. Twenty microliters were loaded and separated 735

on 12% SDS–PAGE gels and transferred to nitrocellulose membranes using wet Mini-736

PROTEAN system of Bio-Rad. The following primary antibodies and dilutions were 737

used for detecting mitochondrial proteins: monoclonal anti-Porin, voltage-dependent 738

anion channel porin (PM035, from Dr Tom Elthon, Lincoln, NE) at 1:5000 dilution; 739

polyclonal anti-AOX, alternative oxidase 1 and 2 (AS04054, Agrisera, Sweden) at 740

1:500 dilution; polyclonal anti-COXII, cytochrome oxidase subunit II (AS04053A, 741

Agrisera, Sweden) at dilution 1:1000; and polyclonal anti-UCP, uncoupling protein 742

(AS121850, Agrisera, Sweden) at 1:1000 dilution. Secondary antibodies linked to 743

horseradish peroxidase were used (Sigma-Aldrich Co.). The signals were detected by 744

chemiluminescence using Pierce™ ECL Western Blotting Substrate (ThermoFischer) 745

and a Luminescent Image Analyzer (G-Box-Chemi XT4, Syngene). The protein band 746

quantifications were performed with GeneTools analysis software from the 747

Luminescent Image Analyzer (G-Box-Chemi XT4, Syngene) according to 748

manufacturer’s instructions. The obtained band intensities for AOX, COX and UCP 749

were corrected for their corresponding porin band intensities and then normalized to the 750

levels of the gl1 plants under GL (i.e. gl1 levels for all the proteins are 100%). Two 751

different immunoblot experiments per protein were performed with very similar results 752

(data not shown), and images shown in Figure 4 and Supplemental Figure 2 belong to 753

one of the two membranes obtained. Samples used in each of the two immunoblot 754

experiments were a mixture of aliquots belonging to two biological replicates from the 755

same six biological replicates used for the GC-MS metabolite analyses-i.e. four of the 756

six biological replicates available were used. The percentage values presented in Figure 757

4 are the mean of the two immunoblot experiments. 758

759

Statistical analysis 760



25

For statistical analyses of Figures 2, 3, Supplemental Figure 3 and Table I, a one way 761

analysis of variance (ANOVA) with a level of significance of p-value <0.05 was 762

performed with SPSS for Windows 17.0 and Duncan post hoc test was to determine 763

statistically significant differences. Pearson correlations (Figure 6 and Table II) and 764

their significance (p-value <0.05) between the fold-changes in metabolite levels and 765

fold-changes in respiratory or photosynthetic parameters were performed with 766

Microsoft Excel Software 2010. Student’s t-tests were used for statistical analyses in 767

Supplemental Table S1 in order to compare all genotypes under the different light 768

treatments to the gl1 under GL levels. 769

770

ACKNOWLEDGEMENTS 771

We would like to thank all the staff at the Serveis Cientifico-Tecnics of the Universitat 772

de les Illes Balears for their help while running these experiments, with especial 773

mention to Dr Biel Martorell for his technical help on the IRMS. We are also very 774

grateful to Yunuén Avalos Padilla for her assistance during the Western blot 775

experiments. 776

777

778

779

780



26

Table I. Percentage of total (TPI), chronic (CPI) and dynamic (DPI) photoinhibition in leaves of gl1, crr4-3, pgr5 and pgr5 crr4-3 plants under 781

growth light (GL) and after 2, 4 and 8h of high light (HL) treatment. TPI, CPI and DPI were obtained as previously described in Florez-Sarasa et 782

al. (2011) and the Fv/Fmmax value was obtained from the mean value of Fv/Fm30 under GL for gl1 plants (i.e. % CPI in gl1 plants is 0). Values 783

are means ± SE of 10-12 replicates. Different letters denote significant differences (P < 0.05) between species. 784

785 786 787

Genotype % TPI % CPI % DPI GL 2h HL 4h HL 8h HL GL 2h HL 4h HL 8h HL GL 2h HL 4h HL 8h HL

gl1 2.3±0.5a 38.5±1.9cd 40.2±2.7cd 41.7±3.9d 0.0±0.3a 26.4±1.4cd 27.1±2.3cd 30.1±3.3d 2.3±0.2a 12.1±1.1de 13.1±0.8def 11.6±2.6de

crr4-3 2.9±0.4a 32.8±2.7c 38.1±2.7cd 38.7±3.4cd 0.4±0.4a 20.9±2.0c 25.2±2.1cd 28.3±3.0cd 3.3±0.2a 11.9±0.8de 12.9±0.9def 10.5±1.0cde

pgr5 3.4±0.7a 67.3±3.4e 68.8±2.4e 67.1±3.7e 0.3±0.4a 52.9±3.9e 59.1±2.9ef 59.6±3.7ef 3.0±0.4a 14.4±1.0ef 9.7±1.2cd 7.5±0.8bc

pgr5 crr4-3

14.4±3.9b 81.1±2.2f 83.0±1.2f 79.8±2.4f 8.6±2.8b 64.4±3.4f 77.3±2.0g 74.1±3.4g 5.9±1.1ab 16.7±1.9f 5.7±1.6ab 5.7±1.8ab

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27

Table II. Pearson correlation coefficients (r) between photosynthetic and respiratory 788

parameters. Twelve data points, corresponding to the means for each parameter of each 789

genotype under the different hours of high light treatment, were used in the correlation 790

analyses. Values in bold indicate statistically significant Pearson r correlations (P < 791

0.05). Vt (total respiration); νcyt (cytochrome oxidase pathway activity); νalt (alternative 792

oxidase pathway activity); Valt (alternative oxidase pathway capacity); ETR (chloroplast 793

electron transport rate); Fv/Fm (maximum quantum efficiency of PSII); qP 794

(photochemical quenching); qN and NPQ (non-photochemical quenching); % TPI, % 795

CPI and % DPI (percentage of total, chronic and dynamic photoinhibition). 796

797 Vt νcyt νalt Valt

ETR 0.74 0.73 0.25 -0.75 Fv/Fm 0.80 0.81 0.22 -0.92

qP 0.29 0.22 0.24 -0.14 NPQ 0.85 0.78 0.39 -0.89 qN 0.66 0.56 0.41 -0.69

% TPI -0.76 -0.80 -0.14 0.88 % CPI -0.80 -0.81 -0.21 0.92 % DPI 0.53 0.39 0.47 -0.60

798 799



28

FIGURE LEGENDS 800

Figure 1. Photograph of representative wild-type (gl1) and cyclic electron flow around 801

photosystem I (CEF-PSI) mutant plants after 4 weeks of growth. The light treatments, 802

measurements and harvesting were performed after 4 weeks of growth in gl1 and CEF-803

PSI single mutant plants (crr4-3 and pgr5) which were showing slight growth 804

retardation. On the other hand, double mutants (pgr5 crr4-3) presented pale green 805

leaves and a more pronounced growth retardation, and therefore were grown for 5 806

weeks to reach a similar developmental stage as the other genotypes. 807

808

Figure 2. Photosynthetic parameters obtained by chlorophyll fluorescence analysis in 809

wild-type (gl1) and cyclic electron flow around PSI mutants. (A) Photochemical 810

quenching (qP); (B, D) non-photochemical quenching (qN, NPQ); (C) quantum 811

efficiency of PSII (ΦPSII); (E) chloroplast electron transport rate (ETR); and maximum 812

quantum efficiency of PSII (Fv/Fm) were determined in leaves of gl1, crr4-3, pgr5 and 813

pgr5 crr4-3 plants under growth light (0h) and after 2, 4 and 8h of high light (HL) 814

treatment. The chlorophyll fluorescence analysis, parameter calculations, light 815

treatments and genotypes are detailed in material and methods section. Data represent 816

means ± SE of ten to twelve replicates and different letters denote statistically 817

significant differences (P < 0.05). 818

819

Figure 3. In vivo respiratory activities and capacity of the alternative oxidase (AOX) in 820

wild-type (gl1) and cyclic electron flow around PSI mutants. (A) Total respiration (Vt), 821

(B) cytochrome oxidase pathway activity in vivo (νcyt), (C) AOX pathway activity in 822

vivo (νalt) and (D) AOX capacity (Valt) were determined in leaves of gl1, crr4-3, pgr5 823

and pgr5 crr4-3 plants under growth light (0h) and after 2, 4 and 8h of high light (HL) 824

treatment. The respiration analysis, light treatments and genotypes are detailed in 825

material and methods section. Data represent means ± SE of four to ten replicates and 826

different letters denote statistically significant differences (P < 0.05). 827

828

Figure 4. Mitochondrial electron transport chain proteins detected by Western blot in 829

leaves of gl1, crr4-3, pgr5 and pgr5 crr4-3 plants under growth light (GL) and after 4 830

and 8h of high light (HL) treatment. The intensities of the signals from the alternative 831

oxidase (AOX), cytochrome oxidase subunit II (COX) and uncoupling protein (UCP) 832

were normalized to those from the porin and expressed as percentages relative to values 833



29

of gl1 under GL intensity. The percentage values denoted are the average of two 834

independent blots each using two biological replicates. 835

836

Figure 5. Heat map the relative levels of the GC-MS analysed metabolites in wild-type 837

(gl1) and cyclic electron flow around PSI mutants under growth light and after HL 838

conditions. Metabolites were clustered per class into amino acids, organic acids, sugar 839

and sugar alcohols, and some metabolite ratios were also calculated. Relative metabolite 840

levels of in leaves of gl1, crr4-3, pgr5 and pgr5 crr4-3 plants under all light conditions 841

(see Material and Methods section for further details) were normalized to the mean level 842

of the gl1 plants under GL conditions and then fold-change values were log2 843

transformed (i.e. the level of all metabolites of gl1 plants under GL are 0). In this heat 844

map, red and green colours represent log2 fold-increased and fold-decreased 845

metabolites, respectively. Values are means ± SE of 6 replicates and statistically 846

significant differences to gl1 plants under GL conditions are presented in Supplemental 847

Table SI. 848

849

Figure 6. Pearson correlation coefficients between fold-changes in metabolite levels 850

and in vivo respiratory activities in wild-type (gl1) and cyclic electron flow around PSI 851

mutants. As for the calculation of the metabolite relative levels, respiratory activities 852

were also normalized to those of the gl1 plants under GL condition. Then, all fold-853

change values were log10 transformed and used for the Pearson correlations. The values 854

used for the correlations were the means of all the genotypes under each light condition 855

thus allowing 15 point correlation. Only the metabolites showing statistically significant 856

(P < 0.05) Pearson correlation coefficients to at least one respiratory parameter are 857

presented and their positive (red) and negative (blue) r values are shown. 858

859

SUPPLEMENTAL DATA 860

Supplemental Table SI. Metabolite levels in leaves of gl1, crr4-3, pgr5 and pgr5 crr4-861

3 plants under growth light (GL) and after 2, 4 and 8h of high light (HL) treatment. 862

Supplemental Table SII (xlsx). Parameters used for peak annotation in GC-MS 863

analysis. 864

Supplemental Figure S1. Plots showing all the relationships between photosynthetic 865

and respiratory parameters. 866



30

Supplemental Figure S2. Images showing membranes blotted from entire SDS-PAGE 867

gels of the immunodetected mitochondrial proteins alternative oxidase (AOX), 868

cytochrome oxidase subunit II (COX), uncoupling protein (UCP) and porin in leaf 869

extracts of gl1, crr4-3, pgr5 and pgr5 crr4-3 plants under growth light (GL) and after 4 870

and 8h of high light (HL) treatment. 871

Supplemental Figure S3. Pyridine nucleotides levels in wild-type (gl1) and cyclic 872

electron flow around PSI mutants. 873

Supplemental Figure S4. Plots showing the statistically significant (P<0.05) 874

relationships between fold-changes in metabolite levels and in vivo respiratory activities 875

in wild-type (gl1) and cyclic electron flow around PSI mutants. 876

877

878

879

Supplemental Table SI. Metabolite levels in leaves of gl1, crr4-3, pgr5 and pgr5 crr4-880

3 plants under growth light (GL) and after 2, 4 and 8h of high light (HL) treatment. Data 881

is presented as means and SE for six biological replicates. Significant differences (p < 882

0.05) to the gl1 under GL are denoted in bold font. 883

884

Supplemental Table SII (xlsx). Parameters used for peak annotation in GC-MS 885

analysis. 886

Supplemental Figure S1. Plots showing all the relationships between photosynthetic 887

and respiratory parameters. Vt (total respiration); νcyt (cytochrome oxidase pathway 888

activity); νalt (alternative oxidase pathway activity); Valt (alternative oxidase capacity); 889

ETR (chloroplast electron transport rate); Fv/Fm (maximum quantum efficiency of PSII); 890

qP (photochemical quenching); qN and NPQ (non-photochemical quenching); %TPI, 891

%CPI and %DPI (percentage of total, chronic and dynamic photoinhibition). 892

893

Supplemental Figure S2. Images showing membranes blotted from entire SDS-PAGE 894

gels of the immunodetected mitochondrial proteins alternative oxidase (AOX), 895

cytochrome oxidase subunit II (COX), uncoupling protein (UCP) and porin in leaf 896

extracts of gl1, crr4-3, pgr5 and pgr5 crr4-3 plants under growth light (GL) and after 4 897

and 8h of high light (HL) treatment. A sample of isolated mitochondria (pre-treated 898

with DTT) from wild-type Arabidopsis leaves (Mito) was loaded in the same gel. All 899

antibodies recognized the corresponding band with the expected molecular weight (see 900



31

molecular marker lane, MM) that matched the band detected in the isolated 901

mitochondrial sample. 902

903

Supplemental Figure S3. Pyridine nucleotides levels in wild-type (gl1) and cyclic 904

electron flow around PSI mutants. (A) NAD+, (B) NADP+, (C) NADH, (D) NADPH, 905

(E) sums of NAD+ and NADH, (F) sums of NADP+ and NADPH, (G) NADH/NAD+ 906

ratios and (H) NADPH/NADP+ ratios in leaves of gl1, crr4-3, pgr5 and pgr5 crr4-3 907

plants under growth light (0h) and after 2, 4 and 8h of high light (HL) treatment. The 908

pyridine nucleotide determinations, light treatments and genotypes are detailed in 909

material and methods section. Data represent means ± SE of six replicates and different 910

letters denote statistically significant differences (P < 0.05). 911

912

Supplemental Figure S4. Plots showing the statistically significant (P<0.05) 913

relationships between fold-changes in metabolite levels and in vivo respiratory activities 914

in wild-type (gl1) and cyclic electron flow around PSI mutants. Respiratory activities 915

were also normalized to those of the gl1 plants under GL condition. All fold-change 916

values were log10 transformed and plotted. Vt (total respiration); νcyt (cytochrome 917

oxidase pathway activity); νalt (alternative oxidase pathway activity). 918

919

920



32

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Parsed CitationsAraújo WL, Martins OA, Fernie AR, Tohge T (2014b) 2-Oxoglutarate: linking TCA cycle function with amino acid, glucosinolate,flavonoid, alkaloid, and gibberellin biosynthesis. Front Plant Sci 5: 552.

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Araújo WL, Nunes-Nesi A, Fernie AR (2014a) On the role of plant mitochondrial metabolism and its impact on photosynthesis inboth optimal and sub-optimal growth conditions. Photosynth Res 119: 141-156.


Atkin OK, Millar AH, Gardeström P, Day DA (2000) Photosynthesis, carbohydrate metabolism and respiration in leaves of higherplants. In Leegood RC, Sharkey TD and von Caemmerer S, eds. Photosynthesis: Physiology and Metabolism, Kluwer, Dordrecht,pp 153-17.


Block A, Widhalm JR, Fathi A, Cahoon RE, Wamboldt Y, Elowsky C, Mackenzie SA, Cahoon EB, Chapple C, Dudareva N, Basset GJ(2014) The origin and biosynthesis of the benzoid moiety of ubiquinone (Coenzyme Q) in Arabidopsis. Plant Cell 26: 1938-1948.


Dahal K, Martyn GD, Vanlerberghe GC (2015) Improved photosynthetic performance during severe drought in Nicotiana tabacumoverexpressing a nonenergy conserving respiratory electron sink. New Phytol. doi: 10.1111/nph.13479.


Dahal K, Wang J, Martyn GD, Rahimy F, Vanlerberghe GC (2014) Mitochondrial alternative oxidase maintains respiration andpreserves photosynthetic capacity during moderate drought in Nicotiana tabacum. Plant Physiol 166: 1560-1574.


Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM, Wiskich JT (1996) The cyanide-resistant oxidase: to inhibit or not toinhibit, that is the question. Plant Physiology 110: 1-2.


Demmig-Adams B, Cohu CM, Muller O, Adams WW, III (2012) Modulation of photosynthetic energy conversion efficiency in nature:from seconds to seasons. Photosynth Res 113: 75-88.


Dry IB, Day DA, Wiskich JT (1983) Preferential oxidation of glycine by the respiratory chain of pea leaf mitochondria. FEBS Lett 158:154-158.


Dutilleul C, Driscoll S, Cornic G, De Paepe R, Foyer CH, Noctor G (2003) Functional mitochondrial complex I is required for optimalphotosynthetic performance in photorespiratory conditions and during transients. Plant Physiol 131: 264-275.


Flexas J, Bota J, Galmes J, Medrano H, Ribas-Carbo M (2006) Keeping a positive carbon balance under adverse conditions:responses of photosynthesis and respiration to water stress. Physiol Plant 127: 343-352.


Florez-Sarasa I, Araujo WL, Wallstrom SV, Rasmusson AG, Fernie AR, Ribas-Carbo M (2012) Light-responsive metabolite andtranscript levels are maintained following a dark-adaptation period in leaves of Arabidopsis thaliana. New Phytol 195: 136-148.


Florez-Sarasa I, Flexas J, Rasmusson AG, Umbach AL, Siedow JN, Ribas-Carbo M (2011) In vivo cytochrome and alternativepathway respiration in leaves of Arabidopsis thaliana plants with altered alternative oxidase under different light conditions. PlantCell Environ 34: 1373-1383.

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http://scholar.google.com/scholar?as_q=Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant&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=Effects of drought stress and subsequent rewatering on photosynthetic and respiratory pathways in Nicotiana sylvestris wild type and the mitochondrial complex I-deficient CMSII mutant&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Galle&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Gandin A%2C Duffes C%2C Day DA%2C Cousins AB %282012%29 The absence of alternative oxidase AOX1A results in altered response of photosynthetic carbon assimilation to increasing CO2 in Arabidopsis thaliana%2E Plant Cell Physiol 53%3A 1627%2D1637%2E&dopt=abstract

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Yamamoto H, Peng L, Fukao Y, Shikanai T (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for thechloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23: 1480-1493.


Yoo H, Widhalm JR, Qian Y, Maeda H, Cooper BR, Jannasch AS, Gonda I, Lewinsohn E, Rhodes D, Dudareva N (2013) Analternative pathway contributes to phenylalanine biosynthesis in plants via a cytosolic tyrosine:phenylpyruvate aminotransferase.Nat Commun 4: 2833.


Yoshida K, Noguchi K (2010) Interaction between chloroplasts and mitochondria: activity, function, and regulation of themitochondrial respiratory system during photosynthesis. In Kempken, F, ed. Plant Mitochondria. Springer, New York, pp. 383-409.


Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48: 606-614.


Yoshida K, Watanabe C, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrialalternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49:592-603.


Yoshida K, Watanabe CK, Terashima I, Noguchi K (2011) Physiological impact of mitochondrial alternative oxidase onphotosynthesis and growth in Arabidopsis thaliana. Plant Cell Environ 34: 1890-1899.


Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5: 334-338.


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http://www.ncbi.nlm.nih.gov/pubmed?term=Walker BJ%2C Strand DD%2C Kramer DM%2C Cousins AB %282014%29 The Response of cyclic electron flow around Photosystem I to changes in photorespiration and nitrate assimilation%2E Plant Physiol 165%3A 453%2D462%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Watanabe CK%2C Hachiya T%2C Takahara K%2C Kawai%2DYamada M%2C Uchimiya H%2C Uesono Y%2C Terashima I%2C Noguchi K %282010%29 Effects of AOX1a deficiency on plant growth%2C gene expression of respiratory components and metabolic profile under low%2Dnitrogen stress in Arabidopsis thaliana%2E Plant Cell Physiol 51%3A 810%2D822%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Winger AM%2C Millar AH%2C Day DA %282005%29 Sensitivity of plant mitochondrial terminal oxidases to the lipid peroxidation product 4%2Dhydroxy%2D2%2Dnonenal %28HNE%29 Biochem J 387%3A 865%2D870%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yamamoto H%2C Peng L%2C Fukao Y%2C Shikanai T %282011%29 An Src homology 3 domain%2Dlike fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase%2Dlike complex in Arabidopsis%2E Plant Cell 23%3A 1480%2D1493%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoo H%2C Widhalm JR%2C Qian Y%2C Maeda H%2C Cooper BR%2C Jannasch AS%2C Gonda I%2C Lewinsohn E%2C Rhodes D%2C Dudareva N %282013%29 An alternative pathway contributes to phenylalanine biosynthesis in plants via a cytosolic tyrosine%3Aphenylpyruvate aminotransferase%2E Nat Commun 4%3A 2833%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Noguchi K %282010%29 Interaction between chloroplasts and mitochondria%3A activity%2C function%2C and regulation of the mitochondrial respiratory system during photosynthesis%2E In Kempken%2C F%2C ed%2E Plant Mitochondria%2E Springer%2C New York%2C pp%2E 383%2D409%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Terashima I%2C Noguchi K %282007%29 Up%2Dregulation of mitochondrial alternative oxidase concomitant with chloroplast over%2Dreduction by excess light%2E Plant Cell Physiol 48%3A 606%2D614%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yoshida K, Terashima I, Noguchi K (2007) Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. Plant Cell Physiol 48: 606-614.


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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Watanabe C%2C Kato Y%2C Sakamoto W%2C Noguchi K %282008%29 Influence of chloroplastic photo%2Doxidative stress on mitochondrial alternative oxidase capacity and respiratory properties%3A a case study with Arabidopsis yellow variegated 2%2E Plant Cell Physiol 49%3A 592%2D603%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yoshida K%2C Watanabe CK%2C Terashima I%2C Noguchi K %282011%29 Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana%2E Plant Cell Environ 34%3A 1890%2D1899%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yoshida K, Watanabe CK, Terashima I, Noguchi K (2011) Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Environ 34: 1890-1899.


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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhao Y %282012%29 Auxin biosynthesis%3A a simple two%2Dstep pathway converts tryptophan to indole%2D3%2Dacetic acid in plants%2E Mol Plant 5%3A 334%2D338%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5: 334-338.

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