Plant Physiology Preview. Published on March 10, 2016, as ...€¦ · 2016-03-10 · 54 Katina Kiep: Evonik Industries AG, Essen, Germany 55 • Corresponding author: Christoph Wittmann,

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Running Head 1

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Screening technology for quantitiative isotope experiments 3

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Address of corresponding author: Institute of Systems Biotechnology, Saarland 5

University, Campus A1.5, 66123 Saarbrücken, Germany, Phone: +49-681-302-6

71971, Fax: +49-681-302-71972, Email: [email protected] 7

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Research area: Breakthrough Technologies 9

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Plant Physiology Preview. Published on March 10, 2016, as DOI:10.1104/pp.15.01217

Copyright 2016 by the American Society of Plant Biologists

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High-throughput plant metabolic profiling by stable 12

isotope labelling and combustion isotope ratio mass 13

spectrometry: In vivo assimilation and molecular re-14

allocation of carbon and nitrogen in rice 15

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Lisa Maria Dersch1, Veronique Beckers1, Detlev Rasch2, Guido 18 Melzer2, Christoph Bolten2, Katina Kiep2, Horst Becker3, Oliver 19 Ernst Bläsing4, Regine Fuchs4, Thomas Ehrhardt4 and Christoph 20 Wittmann1,* 21 22 23 24 1 Institute of Systems Biotechnology, Saarland University, Germany 25 2 Institute of Biochemical Engineering, University of Technology Braunschweig, 26

Germany 27 3 BASF SE, Limburgerhof, Germany 28 4 Metanomics GmbH, Berlin, Germany 29 30 31

32 * Address of corresponding author: Institute for Systems Biotechnology, Saarland 33 University, Campus A1.5, 66123 Saarbrücken, Germany, Phone: +49-681 302 34 71971, Fax: +49-681 302 71972, E-mail: [email protected] 35 36 37 38 Summary: 39 Stable isotopic labelling combined with combustion isotope ratio mass spectrometry 40 elucidates metabolic properties of whole plants under strictly controlled physiological 41 conditions. 42

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Footnotes: 49

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• Present addresses: 51

Guido Melzer: Sandoz GmbH, Frankfurt am Main, Germany 52

Christoph Bolten: Nestlé Suisse S.A., La Tour-de-Peilz, Switzerland 53

Katina Kiep: Evonik Industries AG, Essen, Germany 54

• Corresponding author: Christoph Wittmann, E-mail: christoph.wittmann@uni-55

saarland.de 56



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Abstract 57

Here, we demonstrate whole plant metabolic profiling by stable isotope labelling and 58

combustion isotope-ratio mass spectrometry for precise quantification of 59

assimilation, translocation and molecular reallocation of 13CO2 and 15NH4NO3. The 60

technology was applied to Oryza sativa plants at different growth stages. For adult 61

plants, 13CO2 labelling revealed enhanced carbon assimilation of the flag leaf from 62

flowering to late grain filling stage, linked to efficient translocation into the panicle. 63

Simultaneous 13CO2 and 15NH4NO3 labelling with hydroponically-grown seedlings 64

were used to quantify the relative distribution of carbon and nitrogen. Two hours 65

after labelling, assimilated carbon was mainly retained in the shoot (69%), whereas 66

7% entered the root and 24% was respired. Nitrogen, taken up via the root, was 67

largely translocated into the shoot (85%). Salt stressed seedlings showed 68

decreased uptake and translocation of nitrogen (69%), whereas carbon metabolism 69

was unaffected. Coupled to a gas chromatograph, labelling analysis provided 70

enrichment of proteinogenic amino acids. This revealed significant protein synthesis 71

in the panicle of adult plants, whereas protein biosynthesis in adult leaves was 72

eightfold lower than that in seedling shoots. Generally, amino acid enrichment was 73

similar among biosynthetic families and allowed to infer labelling dynamics of their 74

precursors. On this basis, early and strong 13C enrichment of Embden-Meyerhof-75

Parnas pathway and pentose phosphate pathway intermediates indicated high 76

activity of these routes. Applied to mode-of-action analysis of herbicides, the 77

approach showed severe disturbance in the synthesis of branched-chain amino 78

acids upon treatment with imazapyr. The established technology displays a 79

breakthrough for quantitiative high-throughput plant metabolic phenotyping. 80

81

Key words: GC-C-IRMS, Metabolic Flux Analysis, Oryza sativa, Pulse, Rice, Salt 82

Stress, Whole Plant, 13C, 15N 83

84

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5

Introduction 86

Metabolically engineered crops are highly desired to ensure global food supply 87

(Khush, 2003) and to produce various chemicals and materials (Fischer and Emans, 88

2000; Sharma and Sharma, 2009). Without doubt, tailored plant metabolic 89

engineering requires a good knowledge of the underlying metabolism. This explains 90

the strong interest in tools and technologies to analyze plants on the systems level. 91

Particularly, analysis of plant metabolic pathways and intracellular fluxes by means 92

of isotope experiments, coupled to MS and NMR (Ratcliffe and Shachar-Hill, 2006; 93

Young et al., 2011), has predictive power for metabolic engineering (Kruger and 94

Ratcliffe, 2009; Shachar-Hill, 2013). Such analyses, reported for cell suspension 95

cultures (Rontein et al., 2002; Kruger et al., 2007; Williams et al., 2008), and isolated 96

plant organs like leaves (Schaefer et al., 1980; Cegelski and Schaefer, 2005; 97

Hasunuma et al., 2010), tubers (Roessner-Tunali et al., 2004) and seeds 98

(Schwender et al., 2003; Junker et al., 2007), provide valuable insight into 99

metabolism, but fail to describe the behaviour of intact, whole plants (Allen et al., 100

2009), which is necessary to give a systemic picture of metabolic functions under 101

physiologically relevant conditions (Cliquet et al., 1990; Römisch-Margl et al., 2007). 102

This is overcome by performing isotope labelling experiments in entire plants, 103

preferably using 13CO2, a far safer tracer compound than its radiolabelled equivalent 104 14CO2 (Römisch-Margl et al., 2007), combined with labelling analysis by MS and 105

NMR (Chen et al., 2011). Such experiments, however, suffer from extended 106

labelling time periods up to several hours or even days (Hutchinson et al., 1975; 107

Nouchi et al., 1994; Wu et al., 2009) and CO2 concentrations beyond natural 108

abundance to reach detectable amounts of enrichment (Römisch-Margl et al., 2007). 109

As example, the application of elevated CO2 levels can induce changes in plant 110

metabolism, e.g. sink:source ratios, photosynthetic activity and respiration, thereby 111

affecting carbon sequestration and growth (Arp, 1991; Zhu et al., 2014). Compared 112

to conventional MS (0.05 atom%) and NMR, combustion isotope ratio mass 113

spectrometry (C-IRMS) provides a far higher precision (0.0002 atom%) (Meier-114

Augenstein, 1999b), which makes this technique particularly attractive to analyse 115

plants at low enrichment. The high precision of C-IRMS even allows for metabolic 116

studies without preceding tracer application (Tcherkez et al., 2003; Yousfi et al., 117

2012; Yousfi et al., 2013). Selected applications, which coupled C-IRMS with 118

elemental analysis (EA) have been used to trace turnover and incorporation 119

processes in plants (Cliquet et al., 1990; Dyckmans et al., 2000; Nogués et al., 120

2004), as well as to analyse plant interactions with the soil microbial community 121



6

(Griffiths et al., 2004; Leake et al., 2006; Wu et al., 2009). With the availability of 122

GC-coupled isotope ratio MS (GC-C-IRMS), enrichment analysis could be targeted 123

to individual metabolic compounds, like sugars, fatty acids and amino acids (Derrien 124

et al., 2004; Olsson et al., 2005; Molero et al., 2011; Lattanzi et al., 2012). 125

126

Here, we describe a novel approach, which combines 13C- and 15N-based whole 127

plant studies with subsequent labelling analysis of entire plants, plant tissues and 128

individual metabolites using EA-C-IRMS and GC-C-IRMS for in vivo metabolic 129

fingerprinting of the model crop Oryza sativa under physiologically relevant 130

conditions. For the isotope experiments, specific labelling reactors were designed 131

and constructed, which allowed precise 13C-pulse labelling of plants as well as 132

simultaneous 13C and 15N tracing under well-defined environmental conditions. This 133

offered a major benefit compared to previous studies: the applicability of 134

physiological concentrations of 13CO2 and short labelling periods under highly 135

controlled conditions regarding light, temperature and humidity. The developed 136

approach was applied to compare rice plants at different developmental stages, 137

concerning assimilation, translocation and incorporation of label into metabolic 138

intermediates after single or double labelling with 13CO2 and 15NH4NO3. Particularly, 139

studies combining 13C and 15N label detection in plants are rare so far (Cliquet et al., 140

1990; Dyckmans et al., 2000). Thereby, the interaction of C/N metabolism and 141

relevant sink:source relations of individual plant organs were studied. Furthermore, 142

a stress-induced phenotype was investigated by exposing rice seedlings to high 143

salinity, a major abiotic stress. The examination of the mode-of-action of herbicide 144

treatment further underlined the high potential of the technique to reliably quantify 145

metabolic variation. The developed technology provides plant metabolic engineers 146

with a sophisticated tool for fast screening and metabolic profiling of distinct 147

phenotypes, which perfectly complements more demanding isotopically non-148

stationary metabolic flux analysis (Szecowka et al., 2013; Ma et al., 2014) to get a 149

comprehensive picture of plant metabolic functions. 150

151

Results 152

Construction of labelling reactors and experimental design. Three sizes and 153

types of labelling reactor were designed, constructed and validated to evaluate their 154

suitability for in vivo 13C labelling studies (Fig. 1): two tube reactors for 13CO2 studies 155

with soil-grown adult plants (250 L) and seedlings (100 L), respectively, and a box 156

reactor for combined 13CO2 and 15NH4NO3 labelling studies with hydroponic 157



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seedlings (125 L). For all reactors, the used wall material allowed full transmission of 158

light (Fig. S1) and temperature and humidity could be maintained at desired values 159

(Fig. S2). Hence, the reactors allowed plants to be labelled under the same light, 160

temperature and humidity regimen that they were exposed to during growth in a 161

research plant growth cabinet (phyto chamber). Immediate replacement of ambient 162

CO2 by an equimolar level of 13CO2 was realized by an absorber unit connected to 163

the reactor. A first set of experiments with soil-grown rice seedlings was conducted 164

to identify the optimum conditions regarding supply of tracer (400 µL L-1, 700 µL L-1 165 13CO2) and the time period of incubation with 13CO2 (10, 60, 180 min) (Fig. S3). 166

Short incubation times of 10 minutes at ambient levels of 13CO2 (400 µL L-1) were 167

sufficient to allow precise estimation of assimilated carbon, due to the high precision 168

of the EA-C-IRMS measurement (Fig. S3A). Labelled under these conditions, the 169

shoot of rice seedlings showed marked 13C enrichment, i.e. a delta value of 170 ± 170

6‰. The low deviation underlines that the assimilation was quantified with excellent 171

reproducibility, particularly considering the high complexity of the studied plant 172

system. Enrichment values were in an equal range after simultaneous labelling of 173

one, three, six or twelve plants in the same reactor for 60 minutes, indicating that 174

even larger sets of plants and longer incubation times did not result in CO2 limitation 175

(Fig. S3B). In order to examine diurnal effects on photosynthesis and CO2 176

assimilation, isotopic labelling studies with seedlings were conducted every hour in 177

the timeframe of 2.5 to 9.5 hours after sunrise. Labelling of plants at different 178

daytime did not reveal significant difference from plants labelled at midday (6.5 179

hours after sunrise) (Fig. S3C). Accordingly, the routine workflow was as follows: 180

Oryza sativa plants were grown in a phyto chamber under ambient air, until they 181

were placed inside the enclosure shortly before the labelling experiment. Ambient 182

CO2 was then removed from the reactor within 30 seconds and replaced by an 183

equimolar amount of 13CO2 (400 µL L-1). After 10 minutes of incubation in this 184

atmosphere, plants were removed from the reactor and either directly harvested for 185

assessment of carbon assimilation or cultivated further on in the phyto chamber for 186

assessment of carbon translocation, respectively. For simultaneous tracing of 15N, 187

roots of hydroponically grown seedlings were supplied with 15NH4NO3. The isotopic 188

enrichment of harvested plant material and extracted amino acids was determined 189

using EA-C-IRMS and GC-C-IRMS, respectively. 190

191

Combined assessment of carbon and nitrogen metabolism in rice seedlings. 192

The developed approach was next used for combined 13CO2 and 15NH4NO3 labelling 193

of hydroponically grown rice seedlings, in order to obtain an integrated picture of 194



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carbon and nitrogen metabolism (Fig. 2). Isotopically labelled ammonium nitrate 195

was provided to the roots, while at the same time, 13CO2 was supplied to the shoot 196

of a rice seedling, using the designed box reactor (Fig. 1C). Immediately after the 197

pulse, maximum 13C enrichment was detected in the shoot (450 ± 45‰) (Fig. 2A), 198

while 15N labelling was highest for the root (4130 ± 25‰) (Fig. 2C). However, 199

transport of carbon and nitrogen seemed fast, because significant 15N enrichment at 200

this time point was already found in the shoot (190 ± 25‰) (Fig. 2D). Likewise, the 201

root contained slight amounts of 13C (15 ± 5‰) (Fig. 2B). Within two hours after 202

assimilation, 15N and 13C levels were evenly equilibrated. During the ongoing chase 203

period, 13C and 15N enrichments continuously decreased in root and shoot. By 204

integration of the measured 13C and 15N enrichment data, it was now possible to 205

determine the percent reallocation of label within two hours after the labelling pulse 206

(Fig. 3), thereby providing fast and quantitative access to relative carbon and 207

nitrogen fluxes in rice plants. The root-to-shoot ratio, calculated from the labelling 208

data via Equation (4) was 0.173. This seemed a proper estimate according to 209

previously reported values for rice between 0.05 – 0.3 (Yoshida, 1981). The majority 210

of assimilated nitrogen (85%) was transported to the shoot (Fig. 3A), whereas only 211

15% remained in the roots. Regarding assimilated carbon, the major fraction (69%) 212

was retained in the shoot, whereas only 7% was translocated into the roots. A total 213

of 76% of assimilated carbon was thus recovered inside the plant, two hours after 214

assimilation, which indicated a loss of 24% via respiration. The retainment of carbon 215

in the shoot was slightly higher than that for maize plants, in which 53% of 13C is 216

recovered inside the shoot at elongation (Meng et al., 2013). The same calculation, 217

using labelling data from samples, taken 24 hours after the pulse, i.e. including a 218

dark period, revealed an increased loss of carbon through respiration by 52% (data 219

not shown), which agreed well with corresponding data obtained from the 220

measurement of dry matter production, photosynthesis and respiration (Tanaka and 221

Yamaguchi, 1968). 222

223

Impact of salt stress on assimilation and translocation of carbon and nitrogen 224

in rice seedlings. Hydroponically grown rice seedlings were exposed to 100 mM 225

sodium chloride for six days, prior to the labelling experiment. Untreated plants 226

served as a control. Immediately after the labelling pulse, root 15N enrichment was 227

4190 ± 25‰ in the control plant and only 2490 ± 160‰ in the stressed plant, 228

corresponding to a decreased ammonium uptake of 40% (Fig. 2). In addition, the 229

translocation of nitrogen from root to shoot was strongly impaired, leading to 230

significantly less enrichment (43% to 62%) in the shoot of stressed plants, compared 231



9

to control plants at all sampling time points. In contrast, carbon assimilation in the 232

shoot was rather unaltered (Fig. 2A). As described above for untreated control 233

plants, the distribution of carbon and nitrogen was inferred for a stressed plant by 234

integrating 13C and 15N labelling data. The root-to-shoot ratio estimated via Equation 235

(4) was only slightly increased under stress conditions (0.165 ± 0.01 for control 236

plants compared to 0.173 ± 0.03 for stressed plants). Relative carbon distribution did 237

not change in plants exposed to stress (Fig. 3). Nitrogen distribution, however, 238

changed significantly, leading to the recovery of 30% of the assimilated nitrogen in 239

roots, compared to 15% in control plants. The amount of labelled nitrogen 240

transported to the shoot was accordingly decreased, resulting in 69% compared to 241

86% in control plants (Fig. 3B). 242

243

Quantitative assessment of carbon assimilation in adult rice plants. In 244

flowering and grain-filling stage, rice plants exhibit different leaf types, i.e. normal 245

leaves and flag leaves. The flag leaf is the uppermost leaf on a culm and the main 246

carbon provider of the panicle when fully developed (Rawson and Hofstra, 1969). 247

Assimilation patterns of plants in different developmental stages, sampled 248

immediately after a 10-minute labelling pulse, were compared (Fig. 4). Most of the 249

label was found in the leaves. Plants in the flowering stage showed similar 13C 250

enrichment in normal leaves (260 ± 40‰) and flag leaves (240 ± 50‰) (Fig. 4B). 251

This was also observed for the early grain-filling stage. During late grain filling, 252

however, the flag leaf was more important for the assimilation of 13CO2, indicated by 253

significantly higher enrichment (170 ± 10‰ in normal leaves, compared to 270 ± 254

30‰ in flag leaves), which is similar to previous findings for wheat (Rawson and 255

Hofstra, 1969) and consistent with its function as major source organ for carbon 256

transport into the panicle. The stem did not exhibit any enrichment, while the panicle 257

showed low 13C accumulation during early grain-filling (10 ± 5‰) (Fig. 4B). 258

259

Quantitative assessment of carbon translocation in adult rice plants. In order 260

to assess carbon translocation, plants were post-cultivated in the phyto chamber 261

after a labelling period of 10 minutes. Samples taken after distinct chase periods 262

provided a time-resolved 13C sequestration pattern. Immediately after the 13CO2 263

pulse, most of the label was recovered in the leaves (Fig. 4D). Within two hours of 264

further growth, the 13C enrichment of flag leaves and normal leaves declined by 45% 265

and 41%, respectively, while the enrichment in the stem and panicle increased. This 266

trend continued until a maximal enrichment was reached after 24 hours for the 267

panicle (100 ± 20‰) and after 48 hours for the stem (50 ± 15‰) (Fig. 4D). As for the 268



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seedling experiments, the data for the adult plants showed high precision and 269

reproducibility. 270

271

Quantification of 13C and 15N amino acid enrichment using GC-C-IRMS. Using 272

GC-C-IRMS, the measurement of labelling enrichment was extended to amino 273

acids. For each amino acid, eluting from the GC column, the 13C and 15N enrichment 274

was given by the ion intensity at a mass to charge ratio of m/z = 45 and m/z = 29, 275

reflecting 13CO2 and 14N15N, respectively, formed by combustion in the instrument. 276

For 16 amino acids, satisfying signal quality was generally obtained and provided 277

precise estimates of their labelling status. Hereby, the amino acid pairs 278

glutamate/glutamine and aspartate/asparagine were each quantified as lumped 279

pools, due to conversion of the carboxamides asparagine and glutamine into their 280

corresponding acids during the protein hydrolysis step of sample processing 281

(Wittmann, 2007). Four amino acids were not accessible, because they were 282

degraded (cysteine, methionine, tryptophan, arginine) during this treatment 283

(Wittmann, 2007). Generally, 5 mg of lyophilized material was sufficient to provide 284

high quality data, independent from the type of tissue processed. The conditions 285

used for extraction, precipitation and derivatisation of protein from lyophilized plant 286

material was crucial with regard to yield and purity of the obtained amino acids. In 287

contrast to extraction in TRIS buffer (pH 8.8), extraction in hot water (100 °C, 15 288

min) did yield much less protein (data not shown). Similarly, precipitation of the 289

extracted protein in ice-cold 10% TCA was less efficient than precipitation in ice-cold 290

acetone (data not shown). Additional tests with alternative derivatisation agents, 291

revealed that tri-methyl-silyl derivates of the amino acids, obtained e.g. with 292

trimethylsilyl-trifluoroacetamide, were not fully separated by gas chromatography. 293

Even a set of variations in the temperature profile did not allow full baseline 294

separation for the amino acids methionine/aspartate, isoleucine/proline and 295

glutamate/phenylalanine. Full baseline separation was, however, necessary as the 296

combustion of analytes into CO2 and N2 prior to detection does not allow to 297

discriminate between overlapping analyte peaks. Derivatisation with methyl-t-298

butyldimethylsilyl-trifluoroacetamide into t-butyl-dimethyl-silyl derivates finally led to 299

full baseline separation of the target analytes. Some of the seedling samples, 300

however, did not provide an unambiguous signal for tyrosine, probably due to matrix 301

overlay. Due to the fact that interference with background noise or matrix effects 302

leads to false results in isotope experiments (Wittmann, 2007), this amino acid was 303

partly excluded from further interpretation. It also turned out that the addition of 304

dimethylformamide, commonly used to process microbial samples (Wittmann, 305



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2007), was not compatible with the used GC-C-IRMS instrument, because the 306

solvent was largely transferred into the combustion chamber. Accordingly, 307

derivatisation was conducted without addition of solvents. Tests with different 308

incubation times (30, 60, 90, 120 min) and temperatures (80, 90, 100 °C) revealed 309

that the combination of 60 minutes and 80 °C provided the optimum signal-to-noise 310

ratio. 311

312

Isotope distribution patterns – dynamic incorporation of carbon into protein 313

amino acids. The developed protocol was now used to quantify 13C distribution 314

patterns in rice related to amino acid metabolism (Fig. 5). A first study with seedlings 315

revealed that enrichment increased with time, as 13C was continuously incorporated 316

into cell protein. Amino acids strongly differed with regard to label incorporation, 317

which seemed to correlate to their biosynthetic origin. Particularly, tyrosine and 318

phenylalanine, stemming from intermediates of the EMP pathway 319

(phosphoenolpyruvate) and of the non-oxidative PP pathway (erythrose 4-320

phosphate), were enriched rather fast and to a greater extent than all other amino 321

acids and contributed up to 9% and 15% of the entire enrichment, respectively (Fig. 322

5A). Immediately after the pulse, significant 13C incorporation was also observed for 323

amino acids stemming from pyruvate, another intermediate of the EMP pathway, i.e. 324

alanine, serine, glycine, valine and leucine. In contrast, labelling enrichment was 325

delayed for amino acids, synthesized from 2-oxoglutarate and oxaloacetate, 326

intermediates of the tricarboxylic acid (TCA) cycle (Fig. 5A). Generally, highest 327

enrichments were detected 24 hours after the labelling pulse. After 48 hours, the 328

enrichment declined for most amino acids, probably due to a dilution with 12CO2 329

taken up during the post-labelling incubation. The 13C labelling profile of glycine and 330

serine was similar, indicating that they originate from the same metabolic precursor, 331

3-phosphoglycerate (Wittmann, 2007). The same trend was also found for other 332

amino acid families, like the aspartate family of amino acids with threonine, lysine, 333

isoleucine and aspartate itself. In comparison to rice seedlings, the general amino 334

acid enrichment was, on average, eight times lower in the leaf of an adult plant 335

during the late grain filling stage (Fig. 5A). This was interesting to note, because the 336

total assimilation of carbon of both tissue types was in the same range (Fig. S3 and 337

Fig. 4B) and perfectly matches with the changing role of leaves from a strong sink 338

during development to a major source during reproduction, assimilating but not 339

incorporating carbon dioxide (Thrower, 1962; Turgeon, 1989). Low enrichment was 340

equally observed for normal leaves (60 ± 10‰ total amino acid enrichment), flag 341

leaves (70 ± 10‰ total amino acid enrichment) and stem (40 ± 25‰ total amino acid 342



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enrichment) within one day of label translocation (Fig. 5B). In contrast, the panicle of 343

adult rice plants was much more active regarding amino acid metabolic pathways 344

(280 ± 30‰ total amino acid enrichment). Here, highest enrichment was detected 345

for phenylalanine (39 ± 3‰) and tyrosine (30 ± 2‰), followed by alanine (28 ± 4‰), 346

glutamate (23 ± 2‰) and leucine (22 ± 3‰), which was in accordance to the pattern 347

detected for rice seedlings. The other amino acids showed lower enrichment (Fig. 348

5B). 349

Isotope distribution patterns - combined 13C and 15N incorporation into protein 350

amino acids. Amino acids of the shoot were analysed for their 13C and 15N 351

enrichment from combined 13CO2 and 15NH4NO3 labelling experiments with 352

hydroponically grown rice seedlings (Fig.6). For six selected amino acids, i.e. 353

alanine, glycine, proline, serine, aspartate and glutamate, root-based data with 354

satisfying quality could be derived, which allowed a tissue-specific examination, at 355

least for these molecules (Fig. 6). Immediately after labelling, strong 15N enrichment 356

was detected for serine, aspartate and glutamate of root protein. At the same time, 357

alanine, glycine and serine, extracted from shoot protein, revealed significant 13C 358

enrichment (Fig. 6). Within two hours, labelled compounds were distributed inside 359

the plant, leading to combined 13C and 15N enriched amino acids in shoot and root. 360

Although all amino acids exhibited significantly different 13C and 15N enrichment, 361

strongest differences were found for shoot amino acids. Alanine, and serine 362

exhibited higher 13C enrichment, whereas proline, aspartate and glutamate were 363

more strongly enriched with 15N. Four hours after the labelling pulse, similar amino 364

acid enrichment patterns of shoot and root indicated the equilibration of label 365

between these organs (Fig. 6). Amino acid enrichment patterns were similar for soil-366

grown and hydroponically grown rice seedlings (Fig. S4), indicating that hydroponic 367

cultivation did not significantly influence at least this part of metabolism. 368

369

Mode-of-action analysis - effect of imazapyr treatment on rice seedlings. 370

Herbicide treatment was used as proof of concept to demonstrate the potential of 371

the established technology for mode-of-action studies. Imazapyr was chosen as a 372

widely used herbicide, with a well described mechanism of action, i.e. the inhibition 373

of acetolactate synthase (ALS) in branched chain amino acid biosynthesis. The 374

studies were conducted using 12-day old, soil-grown rice plants, which were 375

exposed to imazapyr treatment or to a control treatment. Plants were pulse-labelled 376

with 13CO2, four hours after herbicide application (Fig. 7). At the time-point of the 377

labelling experiment, no phenotypic alterations of plant morphology, as compared to 378

the control plants, were observed (data not shown). The overall carbon assimilation 379



13

at this time point was not disturbed, as indicated by equal 13C shoot enrichment of 380

stressed and control plants, namely 586 ± 26‰ and 595 ± 16‰, respectively (Fig. 381

7A). However, strongly diminished label incorporation was detected in proteinogenic 382

amino acids, which was particularly pronounced for the branched-chain amino acids 383

(BCAAs), 2 hours after the labelling pulse (Fig. 7B). Amino acid enrichment of 384

stressed plants reached 19 to 75% of the enrichment detected in control plants, 385

except for the branched-chain amino acids, which did only reach 4 to 11%. On 386

average, the enrichments were 2.7 times lower in imazapyr-treated plants than in 387

control plants, with the exception of BCAAs, which exhibited 7 to 26 times less 13C 388

enrichment. Observable phenotypic effects became evident seven days after 389

imazapyr application, comprised inhibition of growth, chlorosis of aboveground plant 390

parts, as well as a dieback of young leaves (Fig. 7C). 391

392 Discussion 393

The quantitative analysis of pathway function and regulation is key to understand 394

and engineer plant physiology (Maliga and Graham, 2004). Here, we developed a 395

cost-effective, high-throughput approach to assess whole plant metabolic 396

phenotypes in vivo. As shown, we coupled 13CO2 and 15NH4NO3 pulse studies under 397

precisely controlled physiological conditions with ultra-precision GC-C-IRMS for 398

parallel 13C and 15N labelling analysis in different plant tissues and even individual 399

molecular compounds to elucidate plant metabolic traits. Different tube reactor 400

layouts enabled 13CO2 isotope experiments with soil grown seedlings and adult 401

plants, up to an height of about one metre (Fig. 1A, Fig. 1B), whereas parallel 13CO2 402

and 15NH4NO3 labelling with hydroponic plant cultures could be conducted in a 403

specific box reactor (Fig. 1C). In contrast to previous techniques (Tanaka and Osaki, 404

1983; Nouchi et al., 1994; Römisch-Margl et al., 2007), our methodology minimizes 405

potential alterations of the studied plant during the experiment due to an atmosphere 406

with ambient CO2 levels, controlled temperature, humidity and illumination and 407

incubation times of only 10 minutes. The careful experimental layout provided data 408

with high precision and reproducibility among replicates, independent of the 409

developmental stage of the analysed plants. Assimilation and translocation of 410

carbon in different tissues (Fig. 3, Fig. 4) and even individual molecules (Fig. 5) 411

could be quantified at deviations below 20% for adult plants. Given the fact that 412

plants in advanced developmental stages are rather complex and subject to a 413

certain biological variation, due to differentiation into specific organs and cell types, 414

precision and reproducibility can be regarded excellent. For seedlings, they were 415

partially even higher (Fig. 6, Fig. 7). This allowed to accurately discriminate 416



14

metabolic properties, differing only slightly, which seems a valuable characteristic of 417

our approach. 418

419

Assessment of important characteristics of carbon metabolism. Beyond 420

technical precision and accuracy, it was further important to validate to which extent 421

the method could assess key properties of plant physiology. A catalogue of 422

experiments addressed this issue. Grain yield, the most prominent characteristic of 423

crop plants, is strongly dependent on the source-sink relationship between plant 424

parts (Kato et al., 2004), whereby the operational mode of a distinct plant organ, as 425

source or sink, changes throughout development (Meng et al., 2013). Pioneering 426

studies with rice plants, using radioactive 14CO2 at high dosage had revealed 427

translocation of assimilated carbon into the panicle during grain filling (Cock and 428

Yoshida, 1972). This was quantitatively assessed here, however, by much safer and 429

easier handling using stable 13CO2. Most of the assimilated carbon was recovered 430

inside the rice panicle, 24 hours after the pulse (Fig. 4D and Fig. 5B). In line, a 90% 431

decrease of 13C in the assimilating tissue of plants from the late grain filling stage 432

was detected during this chase period (Fig. 4D), which is in the range of values 433

reported for other plants (Leake et al., 2006). During development from flowering to 434

late grain filling, the relative contribution of different leaves to carbon assimilation 435

probably corresponds to changing metabolic requirements (Meng et al., 2013). 436

During late grain filling, the lower activity of carbon assimilation in mature leaves, 437

relative to the flag leaf, indicated mechanisms of senescence (Fig. 4). In senescing 438

leaves, the RuBisCO content and, as a consequence hereof, the photosynthetic 439

activity rapidly decreases. Therefore, mature leaves cannot assimilate as much CO2 440

as younger leaves (Makino et al., 1984). At night, 13C was further lost by respiration. 441

Additional carbon loss might have resulted from a combination of translocation to 442

tissues not analysed, e.g. the roots of plants grown on soil, and dilution of the label 443

by overall plant biomass increase during the chase period (Leake et al., 2006). 444

445

Integrated analysis of carbon and nitrogen metabolism. The set-up furthermore 446

allowed combined labelling studies with 13CO2 and 15NH4NO3, which are interesting 447

due to the close connection of carbon and nitrogen metabolism in plants, but have 448

been conducted only rarely (Cliquet et al., 1990; Dyckmans et al., 2000). The 449

studies highlighted fast interorgan distribution of carbon and nitrogen in seedlings 450

within two hours after assimilation (Fig. 2), whereby the shoot operated as major 451

sink and exhibited a ten-fold and 6-fold higher demand for carbon and nitrogen 452



15

compounds, respectively, as compared to the root (Fig. 3A), which reflects sufficient 453

supply with water and nutrients, especially nitrogen (Wilson, 1988; Peuke et al., 454

1994). Obviously, the examined seedlings received all essential macro- and 455

micronutrients, and were exposed to optimal breeding conditions, concerning light, 456

temperature and humidity, so that carbon and nitrogen were mainly used for shoot 457

growth and development. The relative flux maps for carbon and nitrogen, giving the 458

relative distribution among the different tissues on basis of the isotope enrichment 459

data, provide a straightforward snapshot of plant metabolism (Fig. 3). Given the 460

available instrumentation, such insights can be easily provided within one day after 461

an isotope experiment and thus allow for a fast evaluation, e.g. to study 462

environmental stresses as demonstrated for salt-stressed rice (Fig. 2, Fig. 3B). In 463

light of breeding stress tolerant plant lines, an important area of application is 464

metabolic phenotyping in order to identify protective mechanisms (Cramer et al., 465

2011) and changes in sink-source relations (Roitsch, 1999; Albacete et al., 2014). 466

Our data reflect these features for plants treated with salt, a major abiotic factor, 467

particularly affecting growth and productivity of salt sensitive crops (Roy et al., 468

2014). Salt stress resulted in strong perturbation of nitrogen uptake by the root and 469

transport to the shoot, whereas carbon assimilation and translocation was not 470

significantly affected. Stressed plants kept relatively more nitrogen in the root, as 471

compared to non-stressed plants (Fig. 3), probably to support the supply with N-472

containing compatible solutes (Wang et al., 2012). Enhanced retention of nitrogen 473

compounds in the root might furthermore be due to adaptive mechanisms to ensure 474

adequate water and nutrient acquisition from the rhizosphere (Sharp et al., 2004). 475

476

Labeling dynamics of amino acids provide qualitative insight into metabolic 477

pathways. The coupling of isotope-ratio combustion mass spectrometry with gas 478

chromatographic separation, together with the development of suitable protocols for 479

sampling and sample processing, provided time-resolved enrichment data for 480

protein-derived amino acids across different tissues of rice. Amino acids are the 481

analytes of choice for microbial pathway analysis, because they are much more 482

abundant in cell extracts and protein than their precursors and provide extensive 483

labelling information (Wittmann, 2007). On basis of the underlying biosynthetic 484

precursor amino acid relationship it is easy to deduce the labelling patterns of the 485

precursor metabolites from labelling patterns of the corresponding amino acids. The 486 13C labelling of amino acids from the same biosynthetic family was similar and 487

obviously reflected the enrichment of their common precursor (Fig. 5A). In the 488

seedling, amino acids stemming from precursors of the EMP pathway and the non-489



16

oxidative PP pathway exhibited a fast and strong 13C enrichment (Fig. 5A, upper 490

panels), examples being phenylalanine, tyrosine, serine, glycine and histidine. In 491

contrast, glutamate, proline, aspartate and threonine, originating from TCA cycle-492

based precursors, were labelled much slower and weaker. Altough this does not 493

directly provide quantitative flux rates, the 13C enrichment data reveal a fast and 494

strong influx of 13C into the EMP pathway and the non-oxidative PP pathway, 495

indicating high activities of these routes. The rather low enrichment of TCA-cycle 496

related amino acids most likely reflects a downregulation of the cycle in the light 497

(Tcherkez et al., 2005). In addition, the slow dynamics could be an indication, that 498

glutamate, aspartate and amino acids derived therefrom, are not formed in the 499

shoot, but are rather synthesized in the root, followed by transport into the shoot. 500

This is indeed taking place, which is discussed below on basis of integrated 13C and 501 15N labelling data (Fig. 6). The 13C enrichment in the shoot of a seedling was about 8 502

to 10 fold higher than that in the leaf of an adult rice plant (Fig. 5A, lower panels). 503

Adult leaves assimilated the provided 13CO2 to a high extent (Fig. 4), but 504

incorporated only little of it into protein. This matches with the changing role of 505

leaves from sink to source during reproduction, assimilating but not incorporating 506

carbon dioxide (Thrower, 1962; Turgeon, 1989). 507

508

Labeling dynamics of amino acids indicate tissue specific metabolism. The 13C 509

labelling of amino acids differed largely between individual tissues. For rice at late 510

grain filling, leaf, flag leaf and stem incorporated only little carbon into protein 511

(Fig. 5B). The panicle showed the highest 13C enrichment among all tissues. Most 512

assimilated carbon was hence translocated into the panicle, where it was 513

incorporated into proteinogenic amino acids. The panicle exhibited an active de-514

novo protein biosynthesis, reflecting that filling of the grains results in a strong 515

demand for protein precursors (Cock and Yoshida, 1972). A compound-oriented 516

view, based on statistical significance of labelling patterns, groups amino acids into 517

coloured ellipses according to their labelling similarity (Fig. 5D). This immediately 518

highlights specific metabolic fingerprints for all tissues of rice. Leaf and flag leaf 519

differed only in a few amino acids, whereas stem and panicle revealed drastically 520

altered patterns and evidence for a tissue specific carbon metabolism. This type of 521

visualization further highlighted strong differences between the carbon metabolism 522

of an adult leaf and a young shoot. 523

524

Labeling dynamics provide spatial resolution of amino acid metabolism. 525

Combined 13C and 15N labelling of hydroponic rice seedlings showed an immediate 526



17

occurrence of 15N labelled glutamate/glutamine and aspartate/asparagine in the 527

root, whereas the 13C labelled forms appeared much later (Fig. 6C). Obviously, 528

these amino acids were formed from carbon precursors in the root through 15NH4 529

assimilation and transamination (Lam et al., 1995), which explains the exclusive 530

enrichment with 15N (Fig. 6A and Fig. 6C). Subsequently, they were transported into 531

the shoot (Funayama et al., 2013) to serve as amino group donors for the 532

biosynthesis of other amino acids (Kiyomiya et al., 2001). Glutamate with its rather 533

high 15N and low 13C enrichment, synthesized in the root and transported to the 534

shoot (Fig. 6B, 2 hour time point), is the precursor for de novo synthesis of proline, 535

exhibiting a similar labelling pattern. 536

The immediate 13C enrichment (Fig. 6B, time point zero) indicates a fast 537

biosynthesis of alanine, glycine and serine in the shoot. For glycine and serine this 538

may be due to photorespiration, which typically leads to high turnover rates for these 539

amino acids (Gauthier et al., 2010). Overall, this provides a spatially resolved picture 540

of amino acid metabolism (Fig. 6), which explains the different dynamics of 13C and 541 15N enrichment. From similar effects after simultaneous labelling of rape plants with 542 13C and 15N it has been hypothesized that the incorporation of assimilated 13C into 543

amino acids is not tightly connected to nitrogen assimilation (Gauthier et al., 2010). 544

This seems to also hold for rice. 545

546

Response of rice to the herbicide imazapyr comprises impaired biosynthesis 547

of branched-chain amino acids and enhanced protein turnover. Upon treatment 548

with imazapyr, biosynthesis of valine, leucine and isoleucine was strongly inhibited 549

(Fig. 7B), observable already six hours after treatment. The overall carbon 550

assimilation of the treated plant was, however, unaffected (Fig. 7A). This distinct 551

phenotype perfectly matches with the known mode-of-action of imazapyr. The 552

herbicide is highly target-specific. The enzyme acetohydroxyacid synthase, a key 553

step in branched-chain amino acid biosynthesis, is the only site of action of this 554

herbicide (Tan et al., 2005). In the longer term, imazapyr causes dysfunction of cell 555

growth, as well as disruption of DNA and protein biosynthesis and increased protein 556

turnover to recycle branched-chain amino acids (Shaner and Reider, 1986b; 557

Scarponi et al., 1995; Royuela et al., 2000). As there was no more de novo 558

synthesis, valine, leucine and isoleucine exhibited lowest enrichment (3 ± 3‰ to 10 559

± 3‰) amongst all amino acids. In addition, our analysis demonstrates that 560

metabolic changes at this early time point were not restricted to branched-chain 561

amino acids as primary target. In fact, metabolism was affected much more globally. 562

Newly assimilated 13C was incorporated into protein to a lesser extent in herbicide-563



18

treated plants than in control plants (Fig. 7B). Growth defects, were evident seven 564

days after imazapyr application (Fig. 7C), indicating a slow rate of plant death, which 565

is related to the amount of intracellularly stored amino acids (Shaner and Singh, 566

1991). In this regard, our profiling toolbox appears valuable to study the mode-of-567

action of synthetic compounds at the initial level of plant phenotyping, the first level 568

of a three-tiered approach for mode-of-action identification (Tresch, 2013). 569

570

Conclusions 571

Taken together, the developed approach is suitable to conduct stable isotope 572

labelling experiments for in vivo whole plant metabolic profiling. The high technical 573

data quality achievable under physiologically relevant conditions seems particularly 574

promising to be applied to (i) stress response studies, (ii) phenotypic screening of 575

plant lines, (iii) mode-of-action studies and (iv) integrated analysis of carbon and 576

nitrogen metabolism, among others. The underlying tracer studies require little time 577

and low effort as compared to model-based approaches and are potent as 578

screening tool (Schwender, 2008). Clearly, this type of analysis does not, per se, 579

provide quantitative intracellular fluxes through individual reactions and pathways, 580

but can infer metabolic activities, i.e. reallocation profiles or metabolic fingerprints. In 581

this regard, our approach provides a useful complementation to more demanding 582

approaches of isotopically non-stationary metabolic flux analysis (INST-MFA) 583

(Szecowka et al., 2013; Ma et al., 2014). The latter offer the greatest potential for 584

quantitative resolution of metabolic fluxes in autotrophic plants, but involve extreme 585

experimental and computational effort, high cost and low throughput to derive flux 586

information. In this regard, future combinations of both technologies for two-tiered 587

complementary analysis could provide plant physiologists with a sophisticated 588

toolbox for initial screening of several distinct phenotypes, thereby identifying the 589

most promising ones for more comprehensive analysis. The high-precision GC-C-590

IRMS analysis, demonstrated here for amino acids, might be easily widened to e.g. 591

fatty acids (Meier-Augenstein, 2002; Richter et al., 2010; Panetta and Jahren, 2011), 592

sterols (Jones et al., 1991), monosaccharides (Docherty et al., 2001; Derrien et al., 593

2003) and lignin (Goñi and Eglinton, 1996), which are all accessible via such an 594

instrumentation. This promises to extend the approach to other pathways of primary 595

metabolism, e.g. lipid, sugar and cell wall biosynthesis, as well as to pathways of 596

secondary metabolism, involving e.g. phenol, isoprenoid and alkaloid biosynthesis. 597

598



19

Materials and Methods 599

Plants. O. sativa L. ssp. japonica Nipponbare was obtained from CropDesign N.V. 600

(Zwijnaarde, Belgium). 601

602

Chemicals. As tracer, 13CO2 (> 99 atom% 13C) was purchased from Eurisotop 603

(Saarbrücken, Germany). Labelled ammonium nitrate (15NH4NO3, > 98 atom% 15N) 604

was purchased from Sigma-Aldrich (Steinheim, Germany). 605

606

Media. Plants were grown either on soil (Einheitserde Type-GS90, 70% organic 607

fiber peat, 30% clay, pH 5.5-6, Einheitserde- und Humuswerke Gebr. Patzer, 608

Altengronau, Germany) or on hydroponic medium (1.43 mM ammonium nitrate, 1 609

mM calcium chloride hexahydrate, 0.18 mM magnesium sulfate heptahydrate, 1.32 610

mM potassium sulfate, 0.32 mM monosodium phosphate, 1 mM ferric 611

ethylendiaminetetraacetic acid, 8 µM manganese (II) chloride tetrahydrate, 0.15 µM 612

zinc sulfate heptahydrate, 0.15 µM copper (II) sulfate pentahydrate, 0.075 µM 613

ammonium heptamolybdate, 1.39 µM boric acid, based on (Ritte, 2010)). In isotope 614

experiments, naturally labelled NH4NO3 was replaced by an equimolar amount of 615 15NH4NO3. 616

617

Plant growth conditions. Rice seeds were germinated on moist filter paper in a 618

Petri dish for four days at 26°C in the dark. The seeds were transferred into light 619

(500 µmol m-2 s-1 photosynthetically active radiation (PAR)), one day before they 620

were either transplanted into 0.7 dm3 pots used for further cultivation on soil or into 621

hydroponic boxes. Prior to sowing, pots were soaked with deionized water 622

containing 0.15% of the fungicide proplant (Stähler, Stade, Germany). Seeds were 623

subjected to hot water treatment (60°C, 10 min) to prevent sheath rot. Rice plants 624

were then grown under 13/11 h day/night cycles at an average irradiance of 500 625

µmol m-2 s-1 PAR during the light phase (Powerstar HQI-BT 400W, Osram, Munich, 626

Germany), temperature cycles of 26/21°C and a relative humidity of 60%. During the 627

first 14 days of development, plants were irrigated two times per day with deionized 628

water. During the first three weeks, plants were watered via top-irrigation, later via 629

sub-irrigation. Between weeks three and ten, plants were fertilized with ‘Hakaphos-630

Blau’ solution (0.3% in deionized water, Compo, Münster, Germany) twice per week, 631

replacing one deionized water treatment, respectively. Plants in different 632

developmental stages were used for 13CO2 labelling experiments. Rice seedlings 633

were generally used for experimental purposes after 12 days of cultivation. 634



20

Flowering plants, as well as plants from the early and late grain filling stages were 635

examined at an age of 68, 75 and 88 days, respectively. For hydroponic cultures, 636

plants were grown in hydroponic containers (27x17x12 cm), covered with a 637

perforated styrofoam plate. Plastic meshes were placed inside the holes (2 cm 638

diameter) on which pre-germinated seedlings were cultivated with their roots freely 639

suspended in the hydroponic medium. Rice seedlings were generally used for 640

experimental purposes after 12 days of cultivation. The hydroponic cultures were 641

incubated under the same conditions regarding light, temperature and humidity as 642

soil-grown plants. 643

644

High salt treatment. In salt stress experiments, hydroponically growing seedlings 645

were subjected to high salt treatment for six days. For that purpose, 100 mM NaCl 646

was added to the growth medium. 647

648

Imazapyr treatment. Prior to the labelling experiment, soil-grown seedlings were 649

subjected to imazapyr treatment, a non-selective herbicide of the imidazolinone 650

group. The imazapyr solution (0.3 mM imazapyr (BASF SE, Ludwigshafen, 651

Germany), 0.1% (v/v) dimethyl sulfoxide (DMSO), 0.1% (v/v) Dash® E.C. (BASF 652

SE, Ludwigshafen, Germany)) was applied with an airbrush, to reflect a dosis of 653

62.5 g ha-1. Control plants were subjected to a solution containing only the used 654

solvents (0.1% (v/v) DMSO, 0.1% (v/v) Dash® E.C.). Labelling experiments were 655

conducted four hours after herbicide application. 656

657

Isotopic labelling experiments with 13CO2. The labelling experiments were 658

conducted in specifically constructed labelling reactors (Fig. 1). A large tube reactor 659

(0.5 m diameter, 1.3 m height, 255 L volume) was designed for 13CO2 isotope 660

experiments with soil-grown, adult plants (Fig. 1A), and a small tube reactor (0.5 m 661

diameter, 0.5 m height, 98 L volume) served for 13CO2 isotope experiments at the 662

seedlings stage (Fig. 1B). The tube reactors were built from Plexiglas® acrylic 663

sheets (5 mm thickness, Hans Keim Kunststoffe, Rottweil, Germany). The material 664

allowed full spectral transmission of sunlight at wavelengths between 400 nm and 665

900 nm, containing the essential spectral interval for plant growth (Fig. S1). EPDM 666

rubber (ethylene propylene diene monomer, Mercateo, Munich, Germany) was used 667

as sealing material, because of its high flexibility and endurance. The rubber sealing 668

was agglutinated to the plexiglas or polycarbonate sheets with solvent-free glue 669

(Loctite 406 Henkel, Düsseldorf, Germany). The tube was conglutinated to the lid 670

with a two-component adhesive (Pattex Stabilit, Henkel, Düsseldorf, Gemany). For 671



21

maintenance of a constant temperature, a cooling system with a water-cooled 672

ventilator (peltier cooler/heater, 380W, 24V, Uwe Electronic, Unterhaching, 673

Germany), connected to an external cryostat (Lauda RMT20, Lauda Dr. R Wobser, 674

Lauda-Königshofen, Germany) was installed. The ventilator and the connectors 675

were attached to the bottom plate of the reactor. To keep the humidity level at or 676

above 60% of saturation during the experiments, water-soaked cloth was placed in a 677

glass beaker inside the enclosure. Temperature and relative humidity were 678

monitored on-line by a humidity and temperature logger (Voltcraft DL-120 TH, 679

Conrad Electronic SE, Hirschau, Germany). In addition, the CO2 concentration was 680

measured (Voltcraft CM-100, Conrad Electronic SE, Hirschau, Germany). All 681

reactors allowed a precise adjustment of the 13CO2 level. For this purpose, they 682

contained two perforated pipes, one in the upper back part (exhaust air) and one in 683

the lower back part (supply air). These were connected to a CO2 adsorption unit, 684

consisting of a high power pump (6000 L/min, Bravo 2000, 220V, Scoprega Spa, 685

Cassano d/Adda, Italy), a fine dust filter (Filter Cartridge A Kärcher, Gelsenkirchen, 686

Germany) and a CO2 adsorber (5 L, Drägersorb® 800+, Drägerwerk, Lübeck, 687

Germany). All power supplies, except for the external absorber pump, had 24V D.C. 688

to allow safe handling. All labelling reactors were installed inside the phyto chamber 689

(Svalöf Weibull, Sweden), directly beside the benches, where rice plants were 690

grown at ambient air prior to and after the labelling experiments, respectively. For 691

the labelling studies, plants were placed inside the enclosure. Hereby, the soil of the 692

plant pots was covered with plastic wrap to avoid potential interference of CO2 693

respired from soil with the defined gas atmosphere. The ambient CO2 was removed 694

(< 20 µl L-1) by adsorption for a short time period of about 30 seconds as described 695

above. Immediately after purging, the desired amount of 13CO2 was injected through 696

a valve (screw cap with silicone diaphragm), positioned in the lid of each enclosure 697

and the plants were then incubated for a defined labelling period. Afterwards, the 698

plants or specific parts of it were directly harvested or further cultivated in the phyto 699

chamber under ambient air, prior to analysis. All harvested plants or plant tissues 700

were immediately deep-frozen in liquid nitrogen to stop metabolic activity. At each 701

sampling time point, at least three biological replicates were obtained. In the case of 702

seedling experiments, the whole shoot was harvested. Roots were collected from 703

hydroponically grown plantlets and treated equally. Of a full-grown plant, five tillers 704

were harvested, whereby flag leaf, leaf, stem and panicle were separated, followed 705

by immediate quenching in liquid nitrogen. The individual tissues originating from the 706

five tillers were pooled. The outermost, photosynthetically active leaves were 707



22

removed from the stem prior to further treatment. Experiments were generally 708

performed in the timeframe of four and eight hours after sunrise. 709

710

Combined 13C and 15N labelling experiment. A box reactor (C/N reactor, 711

0.5x0.5x0.5 m, 125 L volume) was developed for combined 13CO2 and 15NH4NO3 712

labelling with hydroponic rice cultures (Fig. 1C). Ammonium nitrate was selected, 713

because it generally serves as nitrogen source and is taken up by the roots. Rice 714

prefers ammonium over nitrate, as demonstrated by a higher uptake rate. Compared 715

to nitrate, its uptake is less dependent on light intensity and O2 concentration at root 716

site (Sasakawa and Yamamoto, 1978). The reactor was built from polycarbonate 717

(5 mm thickness, Hans Keim Kunststoffe, Rottweil, Germany), which allowed full 718

spectral transmission of sunlight (Fig. S1). Plants were pre-grown in the phyto 719

chamber as hydroponic cultures. Prior to the experiment, cultures were transferred 720

from naturally labelled growth medium to a container with 15NH4NO3 medium. The 721

container was then placed inside the reactor on a perforated plate (polyvinylchloride, 722

5 mm, Hans Keim Kunststoffe, Rottweil, Germany) and the enclosure was closed 723

tightly via fixation clamps. Immediately afterwards, the 13CO2 pulse was applied, as 724

described above. Monitoring and control of temperature, humidity and 13CO2 level 725

was done as described for the tube reactors (see above). At the end of the labelling 726

incubation period, the box reactor was opened to ambient air and the plants were 727

either directly harvested or re-transferred into naturally labelled growth medium after 728

washing of the roots with naturally labelled growth medium. Sampling and sample 729

processing was done as described above. Experiments were generally performed in 730

the timeframe of four and eight hours after sunrise. 731

732

Quantification of isotopic 13C and 15N enrichment. Shortly, deep-frozen plant 733

material was freeze-dried (Christ Gamma 2-16 LSC, Martin Christ 734

Gefriertrocknungsanlagen, Osterode am Harz, Germany) and ground to fine powder 735

in a ball mill (3-5 min, 30 Hz, Retsch MM300, Retsch, Haan, Germany). A sample 736

(0.8-0.9 mg dry weight) was then transferred into a tin capsule (3.5x5 mm, 737

HEKAtech, Löbau, Germany). The isotopic enrichment was determined using an 738

elemental analyser (FLASH 2000 Elemental Analyser, Thermo Scientific, Waltham, 739

USA-MA) coupled to an isotope-ratio mass spectrometer (Delta V Plus Isotope Ratio 740

MS, Thermo Scientific, Waltham, USA-MA). The gas flow was set to 300 mL/min 741

and the column temperature was kept at 41°C. 742

743



23

Quantification of isotopic 13C and 15N enrichment of proteinogenic amino 744

acids. Deep-frozen plant material was freeze-dried (Christ Gamma 2-16 LSC, 745

Martin Christ Gefriertrocknungsanlagen, Osterode am Harz, Germany) and ground 746

to fine powder in a ball mill (3-5 min, 30 Hz, Retsch MM300, Retsch, Haan, 747

Germany). Protein extraction was carried out as described previously (Hurkman and 748

Tanaka, 1986), involving slight modifications as outlined below. Samples of 749

approximately 5 mg dry weight were mixed with 400 µL extraction buffer (0.175 M 750

tris(hydroxymethyl)aminomethane/HCl, pH 8.8, 5% (w/v) sodium dodecylsulfate, 751

15% (v/v) glycerol, 0.3 M dithiothreitol), followed by centrifugation (13,000 xg, 10 752

min, room temperature). The supernatant was mixed with 1.6 mL ice-cold acetone 753

and incubated for precipitation of cell protein for 1 h at -20°C). After centrifugation 754

(13,000 xg, 10 min, 4°C), the protein pellet was washed two times with 80% 755

acetone, air-dried and hydrolysed into the amino acids for 12 hours (125 µL, 6 M 756

HCl, 100 °C). The hydrolysate was purified (Millipore, centrifugal filter units, 757

Ultrafree-MC, Durapore-PVDF 0.22 µm, Sigma-Aldrich, Steinheim, Germany). A 758

volume of 50 µL of the hydrolysate was mixed with 50 µL internal standard (1.2 mM 759

α-aminobutyric acid) and evaporated under a nitrogen stream. Amino acids were 760

derivatised by addition of 100 µl N-methyl-N-t-butyldimethylsilyl-trifluoroacetamide 761

(Macherey-Nagel, Düren, Germany) followed by incubation for 1 hour at 80°C. The 762

isotopic composition of the amino acids was quantified by GC-C-IRMS (Trace GC 763

Ultra Gas Chromatograph, Delta V Plus Isotope Ratio MS, Thermo Scientific, 764

Waltham, USA-MA). A sample volume of 0.5 µL was injected via the PTV-inlet 765

(250°C) at a split ratio of 1:20. Helium was used as carrier gas at a constant flow 766

rate of 1 mL/min. Analytes were separated on a fused silica capillary column (HP-767

5MS, 30 m x 25 mm, 0.25 µm, Agilent, Waldbronn, Germany) and then transferred 768

to an oxidizing combustion reactor (1000°C). The initial oven temperature of 120°C 769

was kept for 2 minutes. Afterwards, the temperature was increased at a rate of 770

8°C/min until 200°C. In a second gradient step, the temperature was raised to 771

300°C at 10°C/min followed by a temperature hold for 5 minutes. The GC-C-IRMS 772

profile of the MBDSTFA-derivatised amino acids was obtained in selective ion 773

monitoring mode via mass isomers of formed CO2 (m/z 44, 45, 46) and N2 (at m/z 774

28, 29) at their corresponding retention time. Metabolite identification was achieved 775

by GC-MS (7890A GC-System, 7000 GC/MS Triple Quad, 7693 Autosampler, 776

Agilent Technologies, Waldbronn, Germany) measurements of single amino acids 777

and their mixture (10 µM each) in full-scan acquisition mode, followed by a NIST 778

mass spectral search (NIST MS search 2.0) and comparison of the chromatographic 779

pattern with the one of the corresponding GC-C-IRMS measurement. Data 780



24

acquisition and evaluation was conducted using the Software Isodat NT (Thermo 781

Scientific, Waltham, USA-MA). Analytical accurateness was a pre-condition for 782

further data evaluation. Data points, for which peak integrity was corrupted were 783

omitted from graphical data representation. 784

785

Calculation of 13C and 15N enrichment. The δ values (‰) are expressed relative to 786

international standards as: 787

788

δ =

Rsample - Rstandard

Rstandard*1000 (Eq. 1)

789

where R is the ratio of 13C/12C or 15N/14N. The 13C and 15N measurement was 790

calibrated against Vienna Pee Dee Belemnite (VPDB) and atmospheric nitrogen, 791

respectively, using the international reference materials cellulose (IAEA-CH-3) and 792

ammonium sulphate (IAEA-N-1) as secondary standards. Typical values for δ13C of 793

unlabelled C3 plant material are between -34 and -22‰ (Richter et al., 2010) (Meier-794

Augenstein, 1999a). Enrichment values were also expressed as atom percent (AP), 795

i.e. the percentage of 13C or 15N atoms relative to the total amount of C or N atoms 796

in the sample. Atom percent enrichment was derived via Equation 2. 797

798

AP =

100 * Rsample

1 + Rsample (Eq. 2)

799

Atom percent excess (APE), the absolute value for isotopic enrichment, was 800

calculated by subtracting the enrichment of the control from the enrichment of the 801

sample: 802

803

APE = APsample- APcontrol (Eq. 3)

Data correction for natural isotopes. Naturally occurring isotopes of the analyte 804

and of derivative groups were considered (Wittmann, 2007) and data correction 805

following GC-C-IRMS measurement was done as previously described (Metges and 806

Daenzer, 2000) (Docherty et al., 2001) (Heinzle et al., 2008). Shortly, δ values were 807

normalized to their respective unlabelled equivalents by subtracting values of the 808

unlabeled control from the corresponding value of the labelled sample: 809



25

810

δcorr = δsample - δcontrol (Eq. 4)

811

Where δcorr is the labelled compound, δsample is the derivatized labelled compound 812

and δcontrol is the derivatized unlabelled compound. For each experiment, unlabelled 813

control plants were harvested (at least three biological replicates) that were exposed 814

to the exact same breeding conditions as the labelled plants, i.e., that were grown 815

on the same batch of soil or hydroponic medium, respectively. Furthermore, 816

unlabelled controls were subjected to the same sample processing steps like 817

labelled samples. 818

For the amino acid pathway illustrations (Fig. 5A and Fig. 5B), the corrected δ 819

values were normalized to 100%. Therefore, the highest δcorr value of the respective 820

dataset was set to 100%. The normalized value of any number x (Xnorm) of the 821

original dataset was calculated by the following equation: 822

823

Xnorm = x * 100 δmax

(Eq. 5),

824

where δmax was the highest δcorr value. 825

826

Determination of root-to-shoot ratio and translocation flux. To set up a flux map 827

for a rice seedling, it was important to derive the root-to-shoot ratio of the analysed 828

plantlets. It was assumed that the decrease of 15N enrichment in the root within two 829

hours of tracing is only due to translocation of label to the shoot. With this 830

assumption, the root-to-shoot ratio was derived via the following formula: 831

832

Mshoot* δ15Nshoot, t2- δ15Nshoot, t0 = Mroot* δ15Nroot, t0- δ15Nroot, t2 (Eq. 6)

833

Where M is the mass of shoot and root, respectively. A root:shoot ratio of 1:6 was 834

obtained for twelve day old seedlings. This value was used to estimate the percent 835

enrichment of individual plant parts after two hours of tracing. Considering that shoot 836

biomass was six times as much as root biomass, it follows that 15N enrichment of 837

the shoot was diluted by a factor of six, upon translocation to the shoot, whereas 13C 838

enrichment accumulated 6-fold upon translocation to the root. Accordingly, δ15N 839

values of the shoot were multiplied by six, whereas δ13C values of the root were 840



26

divided by six. Shoot and root enrichment values of 13C as well as 15N labelling, at 841

time point zero, were summed, displaying 100% uptake, respectively. On this basis, 842 13C and 15N percent enrichments were estimated for root and shoot. The amount of 843 13C labelling that could not be recovered in plant tissue was assumed to be lost by 844

respiration. 845

846

Statistical analysis. The statistical significance of differences between mean 847

values were determined using Student`s t-test or one-way ANOVA followed by a 848

post-hoc Tukey`s test. Differences were considered significant, when the P-value 849

was below 0.05.850



27

Supplementary Data 851

Supplementary Fig. S1: Absorption spectra of material used for the construction of 852 labelling reactors. 853 Supplementary Fig. S2: Profiles of temperature and relative humidity inside the 854 different reactor housings. 855 Supplementary Fig. S3: Influence of magnitude and duration of 13CO2 labelling 856 pulse, number of plants in the enclosure and daytime on the enrichment of 857 seedlings. 858 Supplementary Fig. S4: Simplified pathway illustration of shoot amino acid 13C 859 enrichment of rice seedlings raised on soil compared to hydroponic culture. 860 Supplementary Table S1: Raw data of Figure 2 and Figure 3A, combined 13C and 861 15N enrichment of seedlings. 862 Supplementary Table S2: Raw data of Figure 2 and Figure 3B, combined 13C and 863 15N enrichment of seedlings exposed to salt stress. 864 Supplementary Table S3: Raw data of Figure 4B, 13C enrichment of plants in the 865 developmental stages flowering, grain filling early and grain filling late. 866 Supplementary Table S4: Raw data of Figure 4D, 13C enrichment of the different 867 tissue types of plants in the late grain filling stage. 868 Supplementary Table S5: Raw data of Figure 5A, 13C amino acid enrichment of a 869 seedling shoot compared to the leaf of a plant in the late grain filling stage. 870 Supplementary Table S6: Raw data of Figure 5B, tissue specific 13C amino acid 871 enrichment of plants in the late grain filling stage. 872 Supplementary Table S7: Raw data of Figure 5C, statistical significance between 873 individual amino acid 13C enrichments of different tissue types. 874 Supplementary Table S8: Raw data of Figure 6, 13C and 15N enrichment of shoot 875 and root. 876 Supplementary Table S9: Raw data of Figure 7A, 13C assimilation of imazapyr-877 treated rice seedlings. 878 Supplementary Table S10: Raw data of Figure 7B, 13C amino acid enrichment of 879 imazapyr-treated rice seedlings. 880 Supplementary Table S11: Raw data of Figure S2, displaying temperature and 881 humidity profiles of the labelling reactors. 882 Supplementary Table S12: Raw data of Figure S3, validation of labelling system. 883 Supplementary Table S13: Raw data of Figure S4, 13C labelling enrichment of 884 seedlings grown on soil and such grown on hydroponic medium. 885

886



28

Acknowledgements 887

The authors gratefully thank Enrico Peter for his input regarding experimental design 888

and troubleshooting, and Olaf Woiwode for cultivation of plants, maintenance of 889

equipment and assistance with preparation and execution of experiments. Our 890

sincere thanks also go to Jürgen Kastler and René Müller for IRMS analyses and 891

data evaluation.892



29

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1109



35

Figure Legends 1110

1111

Figure 1: Equipment designed and constructed for in vivo 13C and 15N labelling studies: 1112

Large tube reactor (0.5 m diameter, 1.3 m height, 255 L volume) for 13CO2 labelling of soil-1113

grown adult rice plants (A); Small tube reactor (0.5 m diameter, 0.5 m height, 98 L volume) 1114

for 13CO2 labelling of soil-grown rice seedlings (B); Box reactor (0.5 x 0.5 x 0.5 m, 125 L 1115

volume) for simultaneous 13CO2 and 15NH4NO3 labelling of hydroponic rice seedlings (C). All 1116

reactors were equipped with a temperature control, comprising a water-cooled ventilator at 1117

the bottom plate of the reactor and an external cryostat. In addition, an external CO2 1118

adsorption unit consisted of a high power pump, an adsorber and a fine dust filter. Prior to 1119

the experiments, the chosen plants were placed into the reactor, which were then closed gas 1120

tight by a rubber sealing. Ambient CO2 was removed from the reactor within 30 seconds. 1121

Experiments were started by injecting desired amounts of 13CO2 through an injection valve in 1122

the lid of each reactor. 1123

1124

Figure 2: Impact of salt stress on carbon and nitrogen assimilation and translocation of 1125

hydroponically grown rice seedlings. The data reflect 13C (A) and 15N enrichment (B) in the 1126

shoot, and 13C (C) and 15N enrichment (D) and in the root. The data comprise mean values ± 1127

SD (n = 3) for stressed seedlings (100 mM NaCl for six days, white bars) and untreated 1128

controls (grey bars). At the age of 12 days, rice seedlings were simultaneously labelled with 1129 13CO2 (400 µL L-1) through the reactor gas phase and with 15NH4NO3 (1.43 mM), supplied via 1130

the hydroponic growth medium. The labelling pulses were applied for 10 minutes, after which 1131

plants were either directly harvested to assess assimilation, or were further cultivated at 1132

ambient air and in non-labelled medium up to 48 hours for tracing of label translocation. The 1133 13C and 15N enrichment of freeze-dried plant material was analysed by combustion isotope 1134

ratio mass spectrometry, coupled to elemental analysis. Asterisks indicate significant 1135

differences between mean values (P ≤ 0.05, Student`s t-test). n.s., not significant. The full 1136

data set is given in Table S4. 1137

1138

Figure 3: Relative fluxes of assimilated carbon and nitrogen in hydroponically grown rice 1139

seedlings under control conditions (A) and exposed to salt stress (100 mM NaCl for six days) 1140

(B), calculated from 13C and 15N enrichment data, obtained 2 hours after the labelling pulse 1141

(Fig. 2). The root-to-shoot ratio for seedlings under control conditions (0.173) and seedlings 1142

exposed to high salinity (0.165) was calculated from the 15N label distribution using Eq. 4 and 1143

Eq. 6. Based on this ratio, the relative re-allocation of label between shoot and root was 1144

determined. The total amount of assimilated carbon and nitrogen at time point zero was set 1145

to 100% carbon and nitrogen uptake, respectively, in order to provide relative data. The 1146



36

seedlings were analyzed at the age of 12 days. The full data sets are given in Table S3 and 1147

Table S4, respectively. 1148

1149

Figure 4: Carbon assimilation and translocation in adult rice plants, assessed by 13CO2 1150

isotope experiments and labelling analysis by combustion isotope ratio mass spectrometry, 1151

coupled to elemental analysis. Morphology of the studied plants with sampled leaf, flag leaf, 1152

stem and panicle (A); Tissue-specific 13C assimilation of rice at flowering stage (68 days), at 1153

early grain filling stage (75 days) and at late grain filling stage (88 days), for which soil-grown 1154

plants were labelled with 400 µL L-1 13CO2 for 10 minutes and directly harvested for 1155

assessment of 13C enrichment (B); Morphology of the studied plants with identified carbon 1156

assimilation routes (C); Time-resolved carbon assimilation and translocation of rice plants at 1157

late grain filling stage (88 days), for which soil-grown plants were labelled with 400 µL L-1 1158 13CO2 for 10 minutes and directly harvested, or further cultivated at ambient air for 2, 4, 24 1159

and 48 hours prior to harvesting (D). In all cases, 13C enrichment of freeze-dried plant 1160

material is displayed as δ13C (‰), corrected for natural labelling. Mean values ± SD (n = 3) 1161

are shown. Different letters (a, b, c) indicate significant differences between means (P ≤ 0.05, 1162

one-way ANOVA with Tukey`s test) of sampled organs at the respective time points. The full 1163

data sets of these experiments are given in Table S1 and Table S2. 1164

1165

Figure 5: Incorporation of 13C into protein amino acids upon 13CO2 labelling. Enrichment of 1166

extracted amino acids was analysed by GC-C-IRMS. Time-resolved pattern of a rice seedling 1167

(upper panels, age of 12 days) and an adult rice plant at late grain filling (lower panels, age 1168

of 88 days), for which soil-grown plants were labelled with 400 µL L-1 13CO2 for 10 minutes 1169

and then directly harvested, or further cultivated at ambient air for 2, 4, 24 and to 48 hours 1170

prior to harvesting. Statistical analysis was conducted using the Student`s t-test, whereby 1171

significant differences (P ≤ 0.05) between seedling and adult leaf are marked with an asterisk 1172

(A); Tissue-resolved pattern of an adult rice plant at late grain filling, for which plants were 1173

labelled with 400 µL L-1 13CO2 for 10 minutes, followed by 24 hour cultivation at ambient air 1174

prior to harvesting of leaf, flag leaf, stem and panicle. Statistical analysis was done by one-1175

way ANOVA with Tukey`s test, whereby different letters (a, b, c) indicate significant 1176

differences between means of the different tissues (B); Tissue specific amino acid 1177

metabolism, visualized as Venn diagram, which displays the relation of amino acids, based 1178

on the statistical significance between measured 13C enrichments. Significant differences 1179

between means of amino acid 13C enrichments (P ≤ 0.05) were determined by one-way 1180

ANOVA with Tukey`s test. Amino acids that do not show significantly different 13C 1181

enrichment, are located in equally coloured ellipses (C). The enrichment data are provided 1182

as mean values (n = 3) and reflect atom percent excess (APE), corrected for natural 1183



37

isotopes. The full data sets are given in Table S5, Table S6 and Table S7, respectively. To 1184

facilitate comparison, the data are normalised for the highest enrichment of the respective 1185

data set, which was set 100% and visualized by a color code between yellow (0%) and red 1186

(100%). Abbreviations: SDL (seedling shoot), G6P (glucose 6-phosphate), RU5P (ribulose 1187

1,5-bisphosphate), R5P (ribose 5-phosphate), E4P (erythrose 4-phosphate), F6P (fructose 6-1188

phosphate), GAP (glyceraldehyde 3-phosphate), 3PG (3-phosphoglycerate), PEP 1189

(phosphoenolpyruvate), PYR (pyruvate), OAA (oxaloacetate), CIT (citrate), 2OG (2-1190

oxoglutarate), SUC (succinate), FUM (fumarate), MAL (malate). Amino acid abbreviations 1191

are according to the three letter code. 1192

1193

Figure 6: Integrated analysis of carbon and nitrogen metabolism by combined labelling of 1194

hydroponically-grown rice seedlings with 13CO2 and 15NH4NO3. Tissue specific enrichment of 1195

extracted amino acids was quantified by GC-C-IRMS. Integrated view on transport and 1196

biosynthetic routes of Ala, Gly, Ser, Glu/Gln, Asp/Asn and Pro regarding assimilated 13C 1197

(light grey) and 15N (dark grey) labelling (A), assessed in shoot (B) and root (C) is 1198

represented by bar graphs over the first four hours of tracing. The data reflect mean values ± 1199

SD (n = 3). At the age of 12 days, rice seedlings were simultaneously labelled with 400 µl L-1 1200 13CO2 and 1.43 mM 15NH4NO3 for 10 minutes and then either harvested directly for 1201

assessment of label assimilation, or further cultivated at ambient air for 2 to 4 hours for 1202

assessment of label translocation. Asterisks indicate significant differences between mean 1203

values at P ≤ 0.05 (Student`s t-test). n.s., not significant. The full data set is given in Table 1204

S8. 1205

1206

Figure 7: Mode-of-action analysis on the effect of the herbicide imazapyr on rice seedlings 1207

using 13CO2 labelling in combination with EA-C-IRMS to assess carbon assimilation (A) and 1208

with GC-C-IRMS to assess 13C enrichment of extracted proteinogenic amino acids (B). The 1209

experimental set-up contained seedlings at the age of 12 days, subjected to imazapyr (62.5 g 1210

ha-1 active ingredient) or control treatment (62.5 g ha-1 of control solution). Four hours after 1211

the treatment, seedlings were labelled for 10 minutes with 400 µL L-1 13CO2. The assimilation 1212

of 13C, determined immediately after the labelling pulse from freeze-dried plant material, is 1213

expressed as δ13C (‰), corrected for natural isotopes. The enrichment of extracted amino 1214

acids was determined after two hours of further cultivation at ambient air. The δ13C-values of 1215

the amino acids of imazapyr-treated rice seedlings were normalized to those of the control 1216

seedlings. The phenotype of rice seedlings, seven days after treatment with the control 1217

solution (left plant) and the imazapyr solution (right plant) is shown in (C). Asterisks indicate 1218

significant differences between mean values of imazapyr-treated and control plants at P ≤ 1219



38

0.05 (Student`s t-test). n.s., not significant. Mean values ± SD (n = 3) are shown. The full 1220

data sets are given in Table S9 and Table S10. 1221

















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Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective.BMC Plant Biol 11: 163


Derrien D, Balesdent J, Marol C, Santaella C (2003) Measurement of the 13C/12C ratio of soil-plant individual sugars by gaschromatography/combustion/isotope-ratio mass spectrometry of silylated derivatives. Rapid Commun Mass Spectrom 17: 2626-2631


Derrien D, Marol C, Balesdent J (2004) The dynamics of neutral sugars in the rhizosphere of wheat . An approach by 13C pulse-labelling and GC/C/IRMS. Plant Soil 267: 243-253


Docherty G, Jones V, Evershed RP (2001) Practical and theoretical considerations in the gas chromatography/combustion/isotoperatio mass spectrometry delta13C analysis of small polyfunctional compounds. Rapid Commun Mass Spectrom 15: 730-738


Dyckmans J, Flessa H, Shangguan Z, Beese F (2000) A dual 13C and 15N long term labelling technique to investigate uptake andtranslocation of C and N in beech (Fagus sylvatica L .). Isotopes Environ Health Stud 36: 63-78


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http://scholar.google.com/scholar?as_q=Determination of d13C values of sedimentary straight chain and cyclic alcohols by gas chromatography/isotope ratio mass spectrometry&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jones&as_ylo=1991&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Phytochemistry%5BTitle%5D%29 AND 68%5BVolume%5D AND 2232%5BPagination%5D AND Junker BH%2C Lonien J%2C Heady LE%2C Rogers A%2C Schwender J%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Photosynthesis and dry-matter production during ripening stage in a female-sterile line of rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kato&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=Real time visualization of 13N-translocation in rice under different environmental conditions using positron emitting tracer imaging system&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kiyomiya&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

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Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field13CO2 pulse-labelling in an upland grassland. Appl Soil Ecol 33: 152-175


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Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-1,5-bisphosphate carboxylase in rice leaves fromemergence through senescence. Plant Cell Physiol 25: 429-437


Maliga P, Graham I (2004) Plant biotechnology: Molecular farming and metabolic engineering promise a new generation of high-tech crops. Curr Opin Plant Biol 7: 149-151


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http://scholar.google.com/scholar?as_q=Network flux analysis: impact of 13C-substrates on metabolism in Arabidopsis thaliana cell suspension cultures&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=Network flux analysis: impact of 13C-substrates on metabolism in Arabidopsis thaliana cell suspension cultures&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kruger&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biochimie%5BTitle%5D%29 AND 91%5BVolume%5D AND 697%5BPagination%5D AND Kruger NJ%2C Ratcliffe RG%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kruger NJ, Ratcliffe RG (2009) Insights into plant metabolic networks from steady-state metabolic flux analysis. Biochimie 91: 697-702

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kruger&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Insights into plant metabolic networks from steady-state metabolic flux 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

http://scholar.google.com/scholar?as_q=Insights into plant metabolic networks from steady-state metabolic flux analysis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kruger&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis%5BTitle%5D%29 AND 7%5BVolume%5D AND 887%5BPagination%5D AND Lam H%2C Coschigano K%2C Schultz C%2C Melo%2DOliveira R%2C Tjaden G%2C Ngai N%2C Hsieh M%2C Coruni G%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lam H, Coschigano K, Schultz C, Melo-Oliveira R, Tjaden G, Ngai N, Hsieh M, Coruni G (1995) Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis. 7: 887-898

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http://scholar.google.com/scholar?as_q=Use of Arabidopsis mutants and genes to study amide amino acid biosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lam&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28J Exp Bot%5BTitle%5D%29 AND 63%5BVolume%5D AND 2363%5BPagination%5D AND Lattanzi FA%2C Ostler U%2C Wild M%2C Morvan%2DBertrand A%2C Decau ML%2C Lehmeier CA%2C Meuriot F%2C Prud%27Homme MP%2C Sch�ufele R%2C Schnyder H%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Lattanzi FA, Ostler U, Wild M, Morvan-Bertrand A, Decau ML, Lehmeier CA, Meuriot F, Prud'Homme MP, Sch�ufele R, Schnyder H (2012) Fluxes in central carbohydrate metabolism of source leaves in a fructan-storing C3 grass: Rapid turnover and futile cycling of sucrose in continuous light under contrasted nitrogen nutrition status. J Exp Bot 63: 2363-2375

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lattanzi&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Fluxes in central carbohydrate metabolism of source leaves in a fructan-storing C3 grass: Rapid turnover and futile cycling of sucrose in continuous light under contrasted nitrogen nutrition status&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=Fluxes in central carbohydrate metabolism of source leaves in a fructan-storing C3 grass: Rapid turnover and futile cycling of sucrose in continuous light under contrasted nitrogen nutrition status&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lattanzi&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Appl Soil Ecol%5BTitle%5D%29 AND 33%5BVolume%5D AND 152%5BPagination%5D AND Leake JR%2C Ostle NJ%2C Rangel%2DCastro JI%2C Johnson D%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Appl Soil Ecol 33: 152-175

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Leake&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland&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=Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Leake&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Proc Natl Acad Sci U S A%5BTitle%5D%29 AND 111%5BVolume%5D AND 16967%5BPagination%5D AND Ma F%2C Jazmin LJ%2C Young JD%2C Allen DK%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ma F, Jazmin LJ, Young JD, Allen DK (2014) Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation. Proc Natl Acad Sci U S A 111: 16967-16972

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ma&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation&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=Isotopically nonstationary 13C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ma&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Relation%5BTitle%5D%29 AND 1%5BVolume%5D AND 5%5BPagination%5D AND Makino A%2C Mae T%2C Ohira K%5BAuthor%5D&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Makino A, Mae T, Ohira K (1984) Relation between nitrogen and ribulose-1,5-bisphosphate carboxylase in rice leaves from emergence through senescence. Plant Cell Physiol 25: 429-437

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Makino&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Makino&as_ylo=1984&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Opin Plant Biol%5BTitle%5D%29 AND 7%5BVolume%5D AND 149%5BPagination%5D AND Maliga P%2C Graham I%5BAuthor%5D&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Physiol%5BTitle%5D%29 AND 136%5BVolume%5D AND 3245%5BPagination%5D AND Nogu�s S%2C Tcherkez G%2C Cornic G%2C Ghashghaie J%5BAuthor%5D&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Nouchi I, Ito O, Harazono Y, Kouchi H (1994) Acceleration of 13C labelled photosynthate partitioning from leaves to panicles in rice plants exposed to chronic ozone at the reproductive stage. Environ Pollut 88: 253-260

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nouchi&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Rapid Commun Mass Spectrom%5BTitle%5D%29 AND 25%5BVolume%5D AND 1373%5BPagination%5D AND Panetta RJ%2C Jahren AH%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ratcliffe&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Aust J Biol Sci%5BTitle%5D%29 AND 22%5BVolume%5D AND 321%5BPagination%5D AND Rawson BHM%2C Hofstra G%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Rawson&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Richter&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Characterization of rapeseed (Brassica napus) oils by bulk C, O, H, and fatty acid C stable isotope analyses&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=Characterization of rapeseed (Brassica napus) oils by bulk C, O, H, and fatty acid C stable isotope analyses&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Richter&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant J%5BTitle%5D%29 AND 39%5BVolume%5D AND 668%5BPagination%5D AND Roessner%2DTunali U%2C Liu J%2C Leisse A%2C Balbo I%2C Perez%2DMelis A%2C Willmitzer L%2C Fernie AR%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Kinetics of labelling of organic and amino acids in potato tubers by gas chromatography-mass spectrometry following incubation in 13C labelled isotopes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Roessner-Tunali&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=%28Curr Opin Plant Biol%5BTitle%5D%29 AND 2%5BVolume%5D AND 198%5BPagination%5D AND Roitsch T%5BAuthor%5D&dopt=abstract

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Yousfi S, Serret MD, Márquez AJ, Voltas J, Araus LJ (2012) Combined use of d13C, d18O and d15N tracks nitrogen metabolism andgenotypic adaptation of durum wheat to salinity and water deficit. New Phytol 194: 230-244


Zhu C, Zhu J, Cao J, Jiang Q, Liu G, Ziska LH (2014) Biochemical and molecular characteristics of leaf photosynthesis and relativeseed yield of two contrasting rice cultivars in response to elevated CO2. J Exp Bot 65: 6049-6056



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Plant Physiology Preview. Published on March 10, 2016, as ...€¦ · 2016-03-10 · 54 Katina Kiep: Evonik Industries AG, Essen, Germany 55 • Corresponding author: Christoph Wittmann,