Proline accumulation is regulated by transcription factors … · 2017. 8. 1. · 78 The glutamate-derived pathway is the most important for proline biosynthesis in plants, and is

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Short title 2

PHR1 and PHL1 controls proline biosynthesis. 3

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Authors 5

Dávid Aleksza, Gábor V. Horváth, Györgyi Sándor, László Szabados* 6

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Title 8

Proline accumulation is regulated by transcription factors associated with phosphate starvation 9 10

Affiliation 11

Institute of Plant Biology, Biological Research Centre, Temesvári krt. 62, 6726-Szeged, Hungary 12

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Short summary 14

Proline accumulation and activation of the P5CS1 gene is an ABA-dependent molecular 15

response to phosphate starvation in Arabidopsis, and is controlled by the PHR1 and PHL1 16

transcription factors. 17

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Key Words 19

Arabidopsis, phosphate starvation, P5CS1, proline, PHR1, PHL1, ABA 20

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Author contribution 22

D.A. performed most of the experiments, G.V.H. and L.Sz. designed and supervised the 23

experiments, G.S. provided technical assistance. 24

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Funding 26

Research was supported by OTKA-NN110962, OTKA-K7623, OTKA-K109719, GINOP 2.3.2-27

15-2016-00001 and NTP-EFÖ-P-15-0157 grants. 28

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* Corresponding author. 30

Email: [email protected] 31

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Plant Physiology Preview. Published on August 1, 2017, as DOI:10.1104/pp.17.00791

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Abstract 35

Proline accumulation in plants is a well-documented physiological response to osmotic stress 36

caused by drought or salinity. In Arabidopsis thaliana the stress and ABA-induced Δ1-37

PYRROLINE-5-CARBOXYLATE SYNTHETASE 1 (P5CS1) gene was previously shown to 38

control proline biosynthesis in such adverse conditions. To identify regulatory factors which 39

control the transcription of P5CS1, yeast one hybrid (Y1H) screens were performed with a 40

genomic fragment of P5CS1, containing 1.2 kB promoter and 0.8 kB transcribed regions. The 41

MYB-type transcription factors PHOSPHATE STARVATION RESPONSE 1 (PHR1) and PHR1-42

LIKE 1 (PHL1) were identified to bind to P5CS1 regulatory sequences in the first intron, which 43

carry a conserved PHR1-binding site (P1BS) motif. PHR1 and PHL1 binding to P1BS was 44

confirmed by Y1H, electrophoretic mobility assay (EMSA) and chromatin immune precipitation 45

(ChIP). Phosphate starvation led to gradual increase in proline content in wild type Arabidopsis 46

plants as well as transcriptional activation of P5CS1 and PROLINE DEHYDROGENASE 2 47

(PDH2) genes. Induction of P5CS1 transcription and proline accumulation during phosphate 48

deficiency was considerably reduced by phr1 and phl1 mutations and was impaired in the ABA 49

deficient aba2-3 and ABA insensitive abi4-1 mutants. Growth and viability of phr1phl1 double 50

mutant was significantly reduced in phosphate-depleted medium, while growth was only 51

marginally affected in the aba2-3 mutants, suggesting that ABA is implicated in growth 52

retardation in such nutritional stress. Our results reveal a previously unknown link between 53

proline metabolism and phosphate nutrition, and show that proline biosynthesis is target of 54

crosstalk between ABA signaling and regulation of phosphate homeostasis through PHR1 and 55

PHL1-mediated transcriptional activation of the P5CS1 gene. 56

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Key words 58

Arabidopsis, phosphate starvation, P5CS1, proline, PHR1, PHL1, abscisic acid 59

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3

Introduction 62

63

Proline is known to accumulate to high levels in numerous plant species at low water 64

potential caused by drought and salinity (Kemble and MacPherson, 1954; Szabados and 65

Savoure, 2010; Verslues and Sharma, 2010). Furthermore, several reports describe proline 66

accumulation in response to other types of stress provoked by heavy metals (Schat, 1997; Jiang 67

et al., 2012), oxidative agents (Yang et al., 2009; Ben Rejeb et al., 2015), or certain pathogens 68

(Fabro et al., 2004; Senthil-Kumar and Mysore, 2012). Different protective functions were 69

attributed to proline, suggesting that it acts as osmoprotectant, stabilizing cellular structures and 70

enzymes, scavenging reactive oxygen species (ROS), and maintain redox equilibrium in 71

adverse conditions (Csonka, 1981; Delauney, 1993; Hoque et al., 2008; Székely et al., 2008; 72

Szabados and Savoure, 2010; Verslues and Sharma, 2010; Sharma et al., 2011; Zouari et al., 73

2016). Besides the much-studied osmoprotective function, proline has been implicated in the 74

regulation of plant development including flowering, pollen, embryo and leaf development 75

(Székely et al., 2008; Mattioli et al., 2009). 76

Proline content is regulated by the balance between its biosynthesis and degradation. 77

The glutamate-derived pathway is the most important for proline biosynthesis in plants, and is 78

composed of two consecutive steps catalyzed by the bifunctional enzyme Δ1-pyrroline-79

carboxylate synthetase (P5CS), that synthetizes glutamate semialdehyde (GSA) from glutamate 80

(Hu et al., 1992; Yoshiba et al., 1995; Funck et al., 2008). GSA is spontaneously converted to 81

pyrroline-5-carboxylate (P5C) and is subsequently reduced to proline by P5C reductase (P5CR) 82

(Delauney and Verma, 1990; Funck et al., 2012). The whole process is controlled by the first 83

and rate-limiting step, mediated by the feed-back regulated P5CS enzyme, which in Arabidopsis 84

is encoded by two genes, P5CS1 (AT2G39800) and P5CS2 (AT3G55610) (Zhang et al., 1995; 85

Strizhov et al., 1997; Székely et al., 2008; Szabados and Savoure, 2010). The production of 86

proline from ornithine represents an alternative biosynthetic pathway and is mediated by 87

ornithine--aminotransferase (OAT, AT5G46180) (Delauney et al., 1993). The importance of 88

this pathway in proline accumulation has however been questioned, as stress-induced proline 89

accumulation was not affected in knockout oat mutants (Funck et al., 2008). P5CS2 is 90

considered to be a housekeeping gene with constitutive expression throughout the plant, while 91

the stress-induced P5CS1 responds to hyperosmotic stress and is regulated by ABA-dependent 92

and independent signals (Savouré et al., 1997; Strizhov et al., 1997; Székely et al., 2008) 93

(Sharma and Verslues, 2010). While P5CS2 can be activated by incompatible plant-pathogen 94

interactions associated with hypersensitive response (Fabro et al., 2004), P5CS1 induction was 95



4

shown to depend on light (Abraham et al., 2003) and respond to ROS signals (Ben Rejeb et al., 96

2015). Besides ABA and light, calcium and lipid signals were implicated in regulation of P5CS 97

genes and proline biosynthesis (Thiery et al., 2004; Parre et al., 2007). The P5CS1 promoter 98

contains sequence motifs that are conserved in related Brassicaceae species and can be 99

binding sites for bZIP, MYB, MYC, AP2/ERBP, C2H2_Zn type transcription factors (Figure S1) 100

(Fichman et al., 2015). A recent ChIP-seq study suggest that several ABA-regulated TFs can 101

bind to the promoter region of the P5CS1 gene (Figure S2) (Song et al., 2016). 102

Proline degradation is an oxidative process, mediated by the rate limiting proline 103

dehydrogenase (PDH) and P5C dehydrogenase (P5CDH) enzymes, both localized in the 104

mitochondria, encoded by two and one genes, respectively (Kiyosue et al., 1996; Deuschle et 105

al., 2001; Servet et al., 2012). Similar to the P5CS genes, the Arabidopsis PDH1 and PDH2 106

genes have remarkable differences in their transcriptional regulation (Funck et al., 2010). PDH1 107

is induced by proline or low osmolarity during stress release and was shown to be controlled by 108

the basic leucine zipper (bZIP) transcription factors (Satoh et al., 2004; Weltmeier et al., 2006). 109

Binding of S-type bZIP factors to the ACTCAT cis-acting element of the PDH1 promoter was 110

demonstrated and shown to be essential for hypo osmolarity-dependent induction of this gene 111

(Satoh et al., 2004; Weltmeier et al., 2006). In contrast, no transcription factors have been 112

characterized which regulates P5CS1. 113

Phosphorus is an essential constituent of biomolecules such as phospholipids, nucleic 114

acids, ATP and is important for reversible protein modification. Soluble phosphate is limited in 115

many soils due to insoluble complex formation with different metals or by microbial consumption 116

converting inorganic phosphate into organic one, which is not available to plants. Phosphate 117

deficiency affects 70% of cultivated land and seriously reduces crop yields, turning phosphate 118

fertilization one of the essential elements of modern agriculture (Lynch, 2011; Herrera-Estrella 119

and Lopez-Arredondo, 2016). Phosphate deficiency generates a complex stress in plants, 120

reduces shoot growth and root elongation, but enhances formation of lateral roots and root 121

hairs, which facilitates phosphate acquisition (Lynch, 2011). Plants take up phosphorus as 122

inorganic orthophosphate (Pi), mediated by high and low affinity phosphate transporters which 123

are influenced by root system architecture, organic acid exudation and soil microbes, mainly 124

arbuscular mycorrhizal fungi (Lopez-Arredondo et al., 2014). Physiological response to 125

phosphate starvation includes changes in glycolysis and mitochondrial electron transport, 126

excretion of several organic acids, enhancement of enzyme activities facilitating phosphate 127

recycling and transport, anthocyanine accumulation and leaf bleaching (Plaxton and Tran, 128

2011). Comprehensive metabolic profiling of phosphate-starved Arabidopsis plants revealed 129



5

massive changes in primary and secondary metabolites, such as organic acids, sugars, 130

glucosinolates, flavonoids and amino acids, including proline (Morcuende et al., 2007; Pant et 131

al., 2015; Valentinuzzi et al., 2015). 132

Regulation of phosphate homeostasis requires complex signaling network coordinating 133

uptake, transport and metabolism of this essential nutrient (Doerner, 2008; Rouached et al., 134

2010). Genome-wide transcript profiling allowed the identification of large sets of phosphate-135

regulated genes and define the most important regulons responding to phosphate deprivation in 136

shoots and roots (Morcuende et al., 2007; Muller et al., 2007; Bustos et al., 2010; Woo et al., 137

2012). The MYB-type PHOSPHATE STARVATION RESPONSE 1 (PHR1) and PHR1-LIKE 1 138

(PHL1) factors are the most important transcriptional regulators, which control the expression of 139

target genes and define metabolic and developmental responses to phosphate deficiency 140

(Rubio et al., 2001; Nilsson et al., 2007; Pant et al., 2015). PHR1 was shown to be essential for 141

adaptation to light stress and to maintain photosynthesis during Pi starvation (Nilsson et al., 142

2012). PHR1 was reported to regulate common transcriptional responses during phosphate 143

starvation and hypoxia under light (Klecker et al., 2014). PHR1 is apparently a key regulator of 144

metabolic changes during phosphorus limitation controlling amino acid pools and lipid 145

remodeling, a dramatic response to phosphate deficiency (Pant et al., 2015; Pant et al., 2015). 146

Starvation-regulated genes are enriched for the PHR1 binding site (P1BS) motif in their 147

promoters, which binds both PHR1 and PHL1 factors. P1BS is important for high level induction 148

of PHR1 target genes during phosphate starvation (Rubio et al., 2001; Karthikeyan et al., 2009; 149

Bustos et al., 2010). Interestingly, PHR1 and PHL1 genes are not induced by phosphate 150

deprivation, but are essential for transcriptional activation of the downstream target genes 151

(Bustos et al., 2010). 152

In this study we report the identification of PHR1 and PHL1 transcription factors as 153

positive regulators of P5CS1 transcription during phosphate starvation. We demonstrate that 154

proline accumulation is a consequence of phosphate starvation, and is controlled by PHR1 and 155

PHL1, which are essential for the enhanced expression of the P5CS1 gene in such conditions. 156

Our results suggest that ABA-dependent signals regulate the proline biosynthetic pathway not 157

only during salt and osmotic stress, but also in phosphate-starved plants. Our results reveals an 158

important connection between proline metabolism and phosphate nutrition and shows that 159

proline accumulation is part of a large-scale metabolic response that is triggered by phosphate 160

starvation. 161

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6

Results 164

165

Phosphate starvation response factors identified by a yeast one-hybrid screen 166

167

To identify the transcription factors that bind to the regulatory region of P5CS1 gene, 168

yeast one-hybrid screens were performed using the 1.95 kb long genomic fragment of P5CS1 169

as bait. The promoter and 5’ UTR region of the P5CS1 gene contains most conserved cis 170

elements, which were predicted as potential TF binding sites (Figure S1,S2) (Fichman et al., 171

2015; Song et al., 2016). Besides the 5’ regulatory region, introns have been reported to carry 172

regulatory elements with capacity to enhance transcription in a number of genes (Lohmann et 173

al., 2001; Casas-Mollano et al., 2006; Gallegos and Rose, 2015), including the high-affinity 174

phosphate transporter AtPht1;4 (Karthikeyan et al., 2009). Therefore we decided to include a 175

1.2 kb 5’ region (promoter and 5’UTR) and a 0.8 kb transcribed region (two exons and the first 176

intron) in the bait genomic fragment (Figure 1A). 86 yeast colonies were identified which grew 177

on selective medium and contained cDNA inserts of different lengths. cDNAs were rescued and 178

their nucleotide sequence was determined to identify the encoded proteins by sequence 179

homology search. One yeast colony carried the full length cDNA of the MYB-type transcription 180

factor Phosphate Starvation Response 1 (PHR1, AT4G28610), and four independent colonies 181

contained cDNAs encoding the closely-related PHR1-like 1 factor (PHL1, AT5G29000), known 182

regulators of the Arabidopsis thaliana phosphate starvation response (Bustos et al., 2010). 183

Analysis of the P5CS1 bait sequence identified a conserved PHR1 binding site (P1BS, 184

GAATATTC) (Karthikeyan et al., 2009) in the first intron of the P5CS1 gene (Figure 1A, S1), 185

suggesting that this motif might be responsible for binding the identified TFs. 186

Binding of PHL1 and PHR1 to the bait was verified by re-transformation of the bait-187

containing yeast strain with cloned factors, by electrophoretic mobility shift assay (EMSA) and in 188

vivo chromatin immunoprecipitation (ChIP) assays. Bait-containing yeast cells were able to 189

proliferate on selective medium when they were expressed either the PHR1 or PHL1 cDNAs, 190

cloned in the pGAD424 vector, but failed to grow with the empty pGAD424 vector (Figure 1B). 191

Interaction of the identified PHR1 and PHL1 factors with P5CS1 genomic sequences was 192

subsequently tested by in vitro (EMSA) and in vivo (ChIP) protein-DNA binding assays. EMSA 193

was performed with purified PHR1 and PHL1 proteins. A 700bp P5CS1 genomic fragment, 194

containing the conserved P1BS motif, a 700bp fragment with mutated P1BS motif (GAATATTC 195

was changed to TCCGCGGA) and a 400bp deletion derivative, missing the P1BS sequence, 196

was incubated with purified PHR1 and PHL1 proteins and assayed with EMSA. Increasing 197



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amount of PHR1 and PHL1 proteins led to gradual enhancement in the electrophoretic mobility 198

shift of the 700bp genomic fragment on agarose gels. This gel shift was however not observed 199

with the 400bp fragment, which lacked the predicted P1BS site (Figure 1C,D). Electrophoretic 200

mobility of the mutated 700bp fragment, in which the P1BS motif was eliminated by point 201



8

mutagenesis, was unchanged when it was coincubated with PHR1 or PHL1 proteins, 202

suggesting that this sequence element was essential for protein binding (Figure 1D). The EMSA 203

assay therefore confirmed that the P1BS motif of the P5CS1 first intron is essential and 204

sufficient for binding of both PHR1 and PHL1 proteins. 205

To confirm the interaction of PHR1 factor with P5CS1 genomic sequenced, chromatin 206

immunoprecipitation was performed, using phosphate-starved Arabidopsis plants expressing 207

the PHR1:HA gene fusion. Immunoprecipitation of the isolated chromatin was carried out with 208

anti-HA microbeads, while Anti-GFP microbeads were employed as control. Quantitative PCR 209

was employed to amplify the target DNA as well as non-specific DNA fragments from unrelated 210

chromosomal regions. After background subtraction and normalisation to control PCR reactions, 211

specific enhancement of HA-immunoprecipitated target DNA was detected when compared to 212

mock samples (Figure 1E). Experiments were repeated three times with similar results. ChIP 213

experiment could therefore confirm that interaction of the PHR1 transcription factor and target 214

DNA in the P5CS1 gene occurs in plant cells. 215

216

Proline accumulates during phosphate starvation 217

Proline accumulation during osmotic and salt stress is a well documented metabolic 218

response, which was shown to be controlled by both ABA-dependent and independent 219

regulatory pathways (Yoshiba et al., 1995; Savouré et al., 1997; Strizhov et al., 1997; Abraham 220

et al., 2003; Sharma and Verslues, 2010). Binding of the PHR1 and PHL1 transcription factors 221

to P5CS1 sequences suggested that proline metabolism can also be influenced by phosphate 222

levels. Proline contents and transcription of key genes in proline metabolism were therefore 223

tested under phosphate deficiency. Phosphate deprivation in our experimental system caused 224

retardation of rosette growth, root elongation, accumulation of anthocyanine and hydrogen 225

peroxide, enhanced lipid peroxidation and more than thousand fold induction of IPS1 gene 226

(AT3G09922), known to be responsive to phosphate starvation (Figure S3) (Martin et al., 2000). 227

When wild type Arabidopsis plants were cultured on medium lacking inorganic phosphate, 228

proline concentration started to increase after 7 days of starvation and after 14 days it was 7 229

times higher than in control, containing 2.5 mM phosphate (Figure 2A). When culture medium 230

was supplemented by additional phosphate (10 mM), proline levels were not affected (Figure 231

2A). Expression of genes which are known to control proline metabolism was considerably 232

altered by phosphate starvation. P5CS1 expression increased 3 to 5 fold, while PDH2 233

expression was enhanced by 4 to 6 fold in shoots and roots under phosphate starvation Figure 234



9

2B,3A). Expression of the other tested genes (P5CS2, P5CR, PDH1, P5CDH) was not or only 235

slightly changed (Figure 2B,3B). Nevertheless, transcript levels of the induced P5CS1 and 236

PDH2 genes were still lower than the related P5CS2 or PDH1 genes, respectively, which were 237

not influenced by phosphate levels (Figure 2B). 238



10

To study spatial and temporal changes in P5CS1 protein levels during phosphate 239

starvation, fluorescence of the GFP-tagged P5CS1 was monitored in transgenic Arabidopsis 240

plants harboring the genomic P5CS1-GFP gene fusion (Székely et al., 2008). GFP-derived 241

fluorescence in roots of transgenic plants was weak and was detectable only close to the root 242

tips of plants cultured on standard 1/2MS culture medium. GFP-derived fluorescence was 243

however well visible in P5CS1-GFP plants on plates lacking phosphate. Enhanced fluorescence 244

was detectable in root elongation zone as early as 4 days after transfer to phosphate-deprived 245

medium, when other phenotypic alterations were not yet visible (Figure 2C). Root proliferation is 246

a characteristic developmental response of phosphate-starved plants, which facilitates 247

phosphate uptake from Pi deficient soils (Lynch, 2011). GFP-derived fluorescence was strong in 248

proliferating lateral roots also, which was typical in plants after 7 days or longer phosphate 249

starvation (Figure 2C, S4). Intracellular localization of P5CS1-GFP fusion protein was similar in 250

leaf cells in phosphate-starved and control plants (not shown). Western hybridization with anti-251

GFP antibody detected the P5CS1-GFP protein in phosphate-starved transgenic plants, but not 252

in the plants grown on standard culture medium, containing 2.5mM Pi. Similar Western signal 253

was obtained in plants which were treated by moderate salt stress, known to enhance P5CS1 254

transcription (Figure 2D) (Strizhov et al., 1997). These results demonstrate that P5CS1 is 255

activated during phosphate starvation, and suggest that the enhanced proline biosynthesis 256

leads to proline accumulation under these conditions. 257

PHR1 and PHL1 transcription factors regulate proline accumulation. 258

To test the role of PHR1 and PHL1 factors in regulation of proline metabolism, proline 259

accumulation in phr1, phl1 and phr1phl1 double mutants were compared to wild type plants 260

under phosphate starvation. Proline levels in these mutants were similar to wild type plants in 261

standard culture conditions, but were 50% lower than in Col-0 plants during phosphate 262

starvation (Figure 3A). Salt and ABA are known to enhance free proline content in most plants 263

(Lehmann et al., 2010; Szabados and Savoure, 2010). Proline content was enhanced by salt 264

and ABA treatments in phr1 and phl1 single mutants similar to wild type plants, but were 265

significantly lower in the phr1phl1 double mutant (Figure 3A). These results suggest that PHR1 266

and PHL1 factors are important for proline accumulation in phosphate-starved plants, and can 267

play a minor role in salt or ABA-induced proline accumulation as well. To test the effect of phr1 268

and phl1 mutations on the expression of genes which control proline biosynthesis and 269

catabolism, transcript levels of P5CS1, P5CS2, P5CR, PDH1, PDH2 and P5CDH were 270

monitored in phosphate-starved mutants. While P5CS1 and PDH2 were induced 3 to 6 times by 271



11

phosphate deprivation in wild type plants, activation of the P5CS1 gene was minimal in phr1 272

and phr1phl1 mutants and was considerably reduced in phl1. Transcript levels of PDH2 were 273

similar to wild type plants in leaves of these mutants, and reduced in roots, while expression of 274

the other pro-related genes was not altered during phosphate starvation (Figure 3B). Our results 275



12

are supported by gene expression data, available in supplementary files of transcript profiling 276

experiments (Bustos et al., 2010). Although P5CS1 and P5CS2 transcripts were not 277

distinguished in the Affymetrix 22.5K ATH1 chip commonly used in microarray-based transcript 278

profiling, phosphate starvation considerably enhanced P5CS1/P5CS2 and PDH2 transcript 279

levels, reduced PDH1 expression but did not affect other genes in proline metabolism (P5CR, 280

P5CDH, �AT) (Figure S5) (Bustos et al., 2010). When compared to wild type plants, transcript 281

levels of P5CS1/P5CS2 and PDH2 were clearly reduced in phr1 and phr1,phl1 mutants (Figure 282

S5). While PHR1 and PHL1 genes themselves are not induced in phosphate-starved plants, the 283

encoded transcription factors are necessary for the activation of P5CS1 and PDH2 genes which 284

are direct targets of PHR1 during phosphate deprivation (Figure 3B, S6, S7) (Bustos et al., 285

2010). 286

Abscisic acid regulates proline accumulation during phosphate starvation. 287

In our experimental system phosphate deprivation reduced growth of wild type 288

Arabidopsis plants by nearly 50%. Rosette growth of phr1, phl1 and phr1phl1 mutants was 289

similar to wild type plants in standard, phosphate-containing medium, while in the absence of 290

phosphate, phr1 and phr1phl1 mutants were significantly smaller than wild type (Figure 4A,B). 291

Rosette growth of aba2-3 mutant was however less reduced by phosphate starvation, than wild 292

type plants or prl1 and phl1 mutants, as it was only 10% smaller in Pi- conditions than in 293

standard medium (Figure 4A,B). Bleaching and leaf necrosis indicate an accumulation of 294

reactive oxygen species, oxidative damage and cell death, which inversely correlates with plant 295

viability (Giacomelli et al., 2007; Laloi and Havaux, 2015). During phosphate strarvation wild 296

type plants were smaller but did not produce bleached leaves, while 60% of phr1phl1 double 297

mutants and 70% of aba2-3 mutants had necrotic leaves in such conditions (Figure 4A,C). 298

These results suggest, that ABA is implicated in the restriction of rosette growth and 299

maintenance of viability in a phosphate-limiting enviroment. 300

Proline accumulation during salt and osmotic stress was shown to be controlled by both 301

ABA-dependent and independent pathways (Savouré et al., 1997; Strizhov et al., 1997) 302

(Sharma and Verslues, 2010). To investigate whether proline accumulation is regulated by ABA-303

dependent signals in phosphate-starved plants, proline content and transcript levels of proline 304

metabolic genes were tested in the aba2-3 mutant, in which ABA biosynthesis is blocked (Leon-305

Kloosterziel et al., 1996) and in abi4-1 and abi5-1 mutants, in which key ABA signaling 306

pathways are impaired (Finkelstein et al., 1998; Lopez-Molina and Chua, 2000). While 307



13

phosphate deprivation enhanced free proline content 3 to 4 times in wild type plants and in the 308

abi5-1 mutant, it was only slightly increased in the phosphate-starved aba2-3 in abi4-1 mutants 309

(Figure 5A). When compared to wild type plants, Pi starvation-dependent activation of P5CS1 310

was reduced by 50% in aba2-3 and in abi4-1 mutants, while it was less affected in shoots and 311



14

more reduced in roots of abi5-1 (Figure 5B). Expression of PDH2 was not affected in shoots of 312

these mutants, while in roots of abi4-1 and abi5-1 it was higher and lower than wild type, 313

respectively (figure 5C). ABA biosynthesis is controlled by the drought-induced NCED3 gene, 314

which encodes the rate limiting 9-cis-epoxycarotenoid dioxygenase enzyme (Iuchi et al., 2001). 315



15

NCED3 expression was induced by phosphate starvation (Figure S7A,B), suggesting that ABA 316

biosynthesis is enhanced in such conditions. These results suggest that proline accumulation 317

and P5CS1 activation during phosphate starvation is at least partially controlled by ABA-318

dependent signals. 319

To study whether damage of phosphate-starved plants is related to senescence, 320

expression of known senescence induced genes, the senescence-associated cysteine 321

proteases SAG12 (Lohman et al., 1994), the glutamine synthetase (GSR2) (Peterman and 322

Goodman, 1991) and methallothionein 1 (MT1) (Zhou and Goldsbrough, 1994), was tested. 323

While expression of the IPS1 marker gene was induced more than two thousand times by 14 324

days of phosphate deprivation, transcript levels of the senescence-related SAG12 were 325

enhanced five times, MT1A and GSR2 genes were only slightly induced in such conditions 326

(Figure S7A). Expression data of microarray experiments showed, that these genes are not or 327

only slightly induced in the absence of phosphate (Figure S7B). Detrimental effects of 328

phosphate starvation can therefore be associated with senescence-related processes. 329

330

Role of proline metabolism in phosphate starvation. 331

Proline accumulation in the p5cs1-1 mutant was completely abolished in phosphate 332

limiting conditions, suggesting that the P5CS1 gene encodes the rate-limiting enzyme of proline 333

biosynthesis under such conditions (Figure 6A). Proline concentration in the pdh1-4 mutant was 334

similar to wild type plants, while it was 30% higher in the pdh2-2 mutant under phosphate 335

starvation (Figure 6A). The function of proline metabolism in phosphate starvation was 336

subsequently tested by monitoring growth of the p5cs1-1, pdh1-4 and pdh2-2 mutants in the 337

presence or absence of inorganic phosphate. Rosette growth of these mutants was similar to 338

wild type in both standard and phosphate limiting conditions (Figure S8). Root growth of the 339

mutants was similar to wild type plants on Pi containing medium, while in the absence of 340

phosphate, p5cs1-1 mutant roots were slightly but significantly shorter than wild type (Figure 341

6B). In the p5cs1-1 mutant transcriptional response of other proline metabolic genes to 342

phosphate starvation was similar to wild type, while in pdh1-4 and pdh2-2 mutants transcript 343

levels of PDH2 and PDH1 genes were reduced, respectively (Figure S9). Exogenously supplied 344

proline (1 mM and 10 mM) reduced rosette and root growth of wild type and phr1phl1 double 345

mutants on phosphate-containing medium. In the absence of phosphate, size of phr1phl1 plants 346

was smaller than wild type ones, and was not influenced significantly by proline (Figure S10). 347



16

These results suggest, that enhanced proline biosynthesis is important to maintain root 348

elongation during phosphate starvation but has no effect on rosette growth, while growth defects 349

cannot be alleviated by externally supplied proline. 350

351

352



17

Discussion 353

Proline accumulation during osmotic and salt stress is a well-documented phenomenon 354

in higher plants and is considered as an important metabolic response to such conditions 355

(Szabados and Savoure, 2010; Verslues and Sharma, 2010). Information on the effect of 356

nutrients and particular nutrient starvation on proline metabolism is however scarce. Our studies 357

revealed that free proline content is increased in Arabidopsis plants during phosphate starvation 358

(Figure 2). These results correlate with recent metabolomic data, revealing that proline 359

accumulation is one of the consequences of phosphorus deficiency in several plant species 360

(Pant et al., 2015; Valentinuzzi et al., 2015). Proline accumulation in phosphate-starved plants is 361

driven by enhanced expression of P5CS1, encoding the key enzyme in the proline biosynthetic 362

pathway. Besides P5CS1, one of the proline catabolic genes, PDH2 was induced by phosphate 363

starvation (Figure 2,3). Although transcripts of the Arabidopsis P5CS1 and P5CS2 genes 364

cannot be distinguished in the most commonly used Affymetrix 22.5K ATH1 chip, microarray-365

based transcript profiling detected enhanced P5CS1/2 and PDH2 transcript levels in phosphate-366

starved plants (Figure S5) (Morcuende et al., 2007; Muller et al., 2007; Bustos et al., 2010). 367

Proline contents were reduced in the p5cs1-1 mutant and enhanced in the pdh2-2 mutant, 368

suggesting that these two genes determine proline levels in this type of stress (Figure 6). The 369

function of proline in the adaptation to phosphate deficiency is however ambiguous, as plant 370

growth was not or was only slightly affected in these mutants, and externally supplied proline 371

had no visible influence on plant growth on medium lacking phosphate (Figure 6, S10). By 372

contrast, deficient proline accumulation in p5cs1 knockout mutants caused salt and drought 373

hypersensitivity (Székely et al., 2008; Sharma et al., 2011), indicating that proline is important 374

for protection in such stresses. Elevated P5CS1 and PDH2 expression suggests that enhanced 375

proline turnover might take place in phosphate-starved plants. Such scenario can be beneficial 376

by regulating NADP/NADPH ratio and cellular redox status during and after stress, consuming 377

reducing power during proline biosynthesis and/or supplying energy for mitochondrial electron 378

transport through proline oxidation (Kiyosue et al., 1996; Sharma et al., 2011; Servet et al., 379

2012; Bhaskara et al., 2015). 380

381

Both PHR1 and PHL1 factors were identified in our yeast one hybrid (Y1H) screen, using 382

a 2 kb fragment of the P5CS1 gene, where the conserved P1BS sequence element was 383

identified in the first intron (Figure 1,S1). Sequence specific binding of both PHR1 and PHL1 384

proteins to this motif could be demonstrated by EMSA and in vivo binding of PHR1 was 385



18

confirmed by ChIP assays. It is intriguing, that the PHR1 and PHL1-binding P1BS motif was 386

localized in the first intron of the P5CS1 gene. Transcription-enhancing features of introns have 387

been described in a number of genes, specially when they are close to the transcription initiation 388

site (Lohmann et al., 2001; Casas-Mollano et al., 2006; Karthikeyan et al., 2009; Gallegos and 389

Rose, 2015). For example, the transcription factors LEAFY and WUSCHEL cooperate in 390

activating the expression of AGAMUS gene by recognizing specific binding sites in the first 391

intron of AG (Lohmann et al., 2001). Promoter analysis of the high-affinity phosphate transporter 392

AtPht1;4 gene has identified a P1BS motif in the first intron of the 5’ UTR region, which was 393

shown to be essential for high level of expression in roots during phosphate deprivation 394

(Karthikeyan et al., 2009). PDH2 is also induced by phosphate starvation (Figure 3), and 395

similarly to AtPht1;4 and P5CS1, has a conserved P1BS motif in its first intron (Figure S11). 396

Earlier transcript profiling data suggest, that P5CS1 and PDH2 genes can be regulated by 397

PHR1 (Figure S5,S6) (Bustos et al., 2010). These data suggest, that PHR1 binding motifs can 398

be located in introns of several genes, which can be important for transcriptional activation 399

during phosphate deficiency. A recent ChIP-seq study revealed that ABA-induced transcription 400

factors can bind to one or multiple sites of 5’ upstream region of the P5CS1 gene, but none of 401

these sequence motifs was located in introns (Figure S2) (Song et al., 2016). PHR1 was 402

recently reported to regulate epigenetic marks and DNA methylation near to cis regulatory 403

elements in the promoters of Pi responsive genes (Yong-Villalobos et al., 2016). Methylation 404

was however not predicted in the vicinity of P1BS motif in the intron of P5CS1 405

(http://neomorph.salk.edu/epigenome/epigenome.html), therefore epigenetic regulation of this 406

gene during phosphate starvation is unlikely. 407

Proline accumulation was attenuated in the phr1phl1 mutant, when plants were exposed 408

phosphate starvation as well as to salt or ABA treatments (Figure 3). ABA was shown to 409

regulate proline accumulation and P5CS1 activation during salt or osmotic stress (Savouré et 410

al., 1997; Strizhov et al., 1997; Szabados and Savoure, 2010). Proline and P5CS1 transcript 411

levels were lower in the ABA deficient aba2-3 and in the ABA insensitive abi4-1 mutant during 412

phosphate deprivation (Figure 5). ABI4 is an AP2-type transcription factor which controls the 413

expression of large set of ABA-regulated genes and is implicated in sugar signaling (Finkelstein 414

et al., 1998; Finkelstein, 2013). These results suggest, that ABA-dependent signals activate the 415

proline biosynthetic pathway not only during dehydration but also during phosphate insufficiency 416

(Figure 7). Connection between ABA regulation and phosphate starvation is however not limited 417

to proline metabolism. Mining of transcript profiling datasets revealed, that a number of ABA-418

regulated target genes are also induced by phosphate deprivation such as RD29A, RAB18, 419



19

RD20, RD22, P5CS1/2, XER2, including NCED3, a key regulator of ABA biosynthesis (Figure 420

S12) (Bustos et al., 2010). Transcription of NCED3 was indeed enhanced by phosphate 421

starvation in our conditions also (Figure S7). Several ABA signaling genes (eg. ABI1, ABI2, 422

HAB1, ST1, ABF3, MYB2, MYC2, RAP2.12) were induced by phosphate deprivation, which 423

was attenuated in phr1 and phr1phl1 double mutants (Figure S12) (Bustos et al., 2010), 424

suggesting that a segment of the ABA regulon is controlled by the PHR1 and PHL1 transcription 425

factors. Transcript profiling data revealed, that PHL1 can be induced by salinity, osmotic stress 426

and ABA as well (Figure S13) (Kilian et al., 2007). On the other hand a number of phosphate-427

responsive genes are also regulated by other stresses such as cold, drought or salinity, some 428

pathogens and hormones like ABA or ethylene (Woo et al., 2012), and senescence-induced 429

genes can be upregulated by phosphate deprivation (Figure S7) (Lohman et al., 1994). These 430



20

results suggest, that there is an intimate relationship between starvation, senescence-related 431

pathways and ABA signaling, which regulates responses to phosphate deficiency. ABA triggers 432

defenses during drought or high soil salinity and mediate growth inhibition (Finkelstein, 2013) 433

(Rowe et al., 2016). We found that on phosphate-deficient medium rosette growth of the ABA 434

deficient aba2-3 mutant was less reduced than wild type, suggesting that ABA is implicated in 435

growth inhibition in such nutritional stress. Enhanced leaf bleaching of the aba2-3 mutant 436

however indicates, that ABA is needed to maintain viability during phosphate starvation. In 437

contrast to aba2-3, both growth and viability was reduced in the phr1phl1 double mutant under 438

phosphate limitation (Figure 4). Reduced proline accumulation in these mutants is probably not 439

responsible for compromised growth or leaf bleaching, as p5cs1-1 mutants with low proline 440

levels had no similar symptoms (Figure 5, 6, S8). Blocking of ABA biosynthesis was reported to 441

release inhibition of root growth under moderate osmotic stress (Rowe et al., 2016), supporting 442

our finding that ABA is implicated in growth control during stress. Growth restriction during 443

osmotic stress can be mediated by growth-repressing DELLA proteins, which are stabilized by 444

ABA, but are promoted to degradation by gibberellins (Achard et al., 2006; Golldack et al., 445

2013). 446

Our results reveal a previously unknown connection between phosphate and proline 447

metabolism. The P5CS1 gene controls proline biosynthesis and seem to be the target of 448

crosstalk between ABA sigaling and regulation of phosphate homeostasis, controlled by the 449

MYB-type transcription factors PHR1 and PHL1 (Figure 7). 450

451

452

Materials and Methods 453

Plant material and growth conditions 454

All Arabidopsis plants used in this study, including mutants were based on the Columbia 455

0 accession (Col-0). p5cs1-1, pdh2-2 and pdh1-4 mutants were obtained from the SALK 456

collection (SALK_058000, SALK_108179, SALK_119334 respectively) (Székely et al., 2008). 457

The phr1, phl1 and phr1phl1 mutants were kindly provided by Dr. J. Paz-Ares (Centro Nacional 458

de Biotecnologica, Madrid, Spain) (Bustos et al., 2010). The aba2-3, abi4-1 and abi5-1 lines are 459

from the ABRC stock (ABRC stock numbers: CS3834, CS8104, CS8105). Plants were grown as 460

described earlier (Székely et al., 2008). Seeds were surface sterilized and germinated on 461

medium solidified with 0.8% (w/v) phytoagar containing 5 mM KNO3, 2.5 mM KH2PO4 (adjusted 462



21

to pH 5.5 with KOH), 2 mM MgSO4, 2 mM Ca(NO3)2, 50 µM Fe-EDTA, 70 µM H3BO3, 14 µM 463

MnCl2, 0.5 µM CuSO4, 1 µM ZnSO4, 0.2 µM NaMoO4, 10 µM NaCl, and 0.01 µM CoCl2, 2.5 mM 464

MES [2-(N-morpholino)-ethanesulfonic acid]-KOH (pH 5.5), 0.5% (w/v) Sucrose. Standard 465

culture medium contained 2.5 mM KH2PO4 and was referred to +Pi medium. For -Pi medium, 466

KH2PO4 was omitted (Ticconi et al., 2001). For phosphate starvation, 5 day-old seedlings, 467

germinated on standard (+Pi) medium, were transferred to –Pi or +Pi medium and grown for 14 468

days. Salt and ABA treatments were applied by transferring 14 days-old in vitro grown plants to 469

media containing 75 or 150 mM NaCl or 50 μM ABA for 1 to 3 days. Results shown were 470

obtained with at least 6 technical and 3 biological replicates. 471

472

Real Time Quantitative RT-PCR 473

RNA isolation was performed as described (Gombos, 2016). First-strand cDNA 474

synthesis of 2 μg of total RNA in a final volume of 20 μL was carried out with RevertAid M-MuLV 475

Reverse Transcriptase (Fermentas), using random hexamers. Real-time PCR was carried out 476

with the ABI 7900 Fast Real Time System (Applied Biosystems) with the following protocol: 45 477

cycles at 95 °C for 15 s, followed by 60 °C for 1 min. The specificity of the amplifications was 478

verified at the end of the PCR run through use of the ABI SDS software. The normalized relative 479

transcript levels were obtained by the 2-ΔΔCt method (Livak and Schmittgen, 2001). To reveal the 480

possible gene expression changes in the proline metabolism pathway we examined the 481

transcript abundance of the following genes: P5CS1 (AT2G39800), P5CS2 (AT3G55610), 482

P5CR (AT5G14800), P5CDH (AT5G62530), PDH1 (AT3G30775), PDH2 (AT5G38710). The 483

actin gene (AT2G37620) was used as an inner control and IPS1 (AT3G09922) was employed to 484

check the stringency of the phosphate starvation. To reveal possible interactions between 485

phosphate starvation, senescence and ABA signals, expression of SAG12 (AT5G45890), MT1A 486

(AT1G07600), GSR2 (AT1G66200), NCED3 (AT3G14440), PHR1 (AT4G28610) and PHL1 487

(At5G29000) were tested in phosphate-starved and control plants. Primers used in this study 488

are listed in Figure S14. 489

490

Yeast ne-hybrid screening 491

The yeast one-hybrid screen was performed principally as described (Ouwerkerk and 492

Meijer, 2001). A 1.95 kbp long P5CS1 genomic fragment was cloned into pHis3NB vector 493

which has the His3 reporter gene construct. The HIS3 reporter construct was integrated at the 494

nonessential PDC6 locus of Y187 yeast strain (Clontech) using the integrative vector, pINT1. 495

The transformation was carried out as described (Gietz and Woods, 2002). To identify DNA 496



22

binding proteins, two Arabidopsis cDNA libraries were used for Y1H screening. The pGAD10 497

expression library (MATCHMAKER cDNA Library, Clontech) was prepared from 3 weeks old 498

green vegetative tissues of Arabidopsis (Col-0). The pACT2 library was the Kim & Theologis 499

lambda-ACT 2-hybrid library 500

(https://www.arabidopsis.org/servlets/TairObject?type=library&id=23). Transformation of the 501

yeast reporter strain with the two libraries generated 86 independent transformed colonies, 502

which were plated on selective medium to permit proliferation of transformed yeast cells on high 503

stringency conditions. 504

505

Electrophoretic mobility shift assay 506

The non-radioactive EMSA assay was based on protocols which used ethidium bromide 507

staining to visualize gel mobility shifts (Ibarra et al., 2003; Forster-Fromme and Jendrossek, 508

2010). In order to achieve strong P1BS binding of the PHR1 and PHL1 factors, truncated 509

proteins containing the C-terminal DNA-binding sites were used (Bournier et al., 2013). 510

Corresponding DNA fragments were PCR amplified (primers in Supplement) inserted into the 511

pET28a+ vector (Invitrogen) and transformed into E. coli BL21 DE3 Rosetta cells (New England 512

Biolabs). Proteins were purified on His-Select Nickel affinity gel (SIGMA). For electromobility 513

shift assay (EMSA), a 415 bp and 705 bp fragments of the P5CS1 gene were generated by 514

PCR, and purified by EZ-10 Spin column PCR purification kit (Biobasic). Protein binding 515

reactions were performed in a buffer containing 137 mM NaCl, 2.7 mM KCl, 4.3 mM Na2HPO4, 516

1.5 mM KH2PO4, pH 7.4 (Alves, 2012). The reaction was perfomed at room temperature for 30 517

min prior to load onto a 1,5% TAE agarose gel (pH 8.5). Separation and detection of the 518

fragments was made as described (Alves, 2012). Electrophoresis was run for 4 h at 12oC, and 519

gels were stained with ethidium bromide (1,5 μg/ml, aquaeus solution) for 40 min, eliminating 520

the need of radiolabelling of the DNA fragment. Images were recorded with UVIDOC HD2 521

(Uvitech, Cambridge) system. 522

523

Chromatin Immunoprecipitation 524

Chromatin Immunoprecipitation (ChIP) was used to verify in planta the interaction of 525

PHR1 protein and the P1BS site localized in p5cs1 gene. The chromatin was isolated from 526

transgenic plants expressing the epitope-tagged PHR1:HA protein, as described (Reimer and 527

Turck, 2010). The immunoprecipitation was carried out with μMACS HA Isolation Kit (Miltenyi 528

Biotec). Control ChIP experiment was carried out with Anti-GFP beads (Miltenyi Biotec), which 529

does not bind HA-tagged proteins. The reverse crosslinking and DNA purification was carried 530



23

out by the ABCAM ChIP protocol (based on the description of Werner Aufsatz). Fragments of 531

immunoprecipitated DNA were amplified by quantitative PCR using P5CS1 specific primers, 532

flanking the P1BS motif in intron 1 (P5CS1-IPfw, P5CS1-IPrev, 133 bp fragment), and control 533

primers amplifying a 178 bp fragment on chromosome 4 (13519698-13519876) (Figure 1, 534

Figure S14). Results were calculated with the „background subtraction” method, as described 535

(Haring et al., 2007). 536

537

Proline, hydrogen-peroxide and malondialdehyde determination 538

The ninhydrin-based colorimetric assay was used to determine the proline level in 539

Arabidopsis seedlings as described (Abraham et al., 2010). The lipid peroxidation assay was 540

carried out as reported (Heath and Packer, 1968), the hydrogen peroxide level was determined 541

by the KI-method (Velikova et al., 2000). 542

Monitoring expression of GFP-tagged P5CS1 gene 543

Gene fusions were previously made by inserting the eGFP reporter gene into the 3’ end 544

of the P5CS1 gene (Székely et al., 2008), and transgenic lines expressing the eGFP-tagged 545

P5CS1 were employed to study spatial and kinetic regulation of the P5CS1 gene. Fluorescence 546

of the transgenic lines was monitored and images were recorded with Olympus SZ12X stereo 547

microscope. 548

549

Bioinformatic analysis 550

Public transcriptomic data were compiled from AtGenExpress Visualization Tool 551

(http://jsp.weigelworld.org/expviz/expviz.jsp) (Kilian et al., 2007). Putative cis elements on 552

P5CS1 genomic sequences were determined by AthaMap tool (http://www.athamap.de) 553

(Steffens et al., 2005), and Promomer tool (http://bar.utoronto.ca/ntools/cgi-554

bin/BAR_Promomer.cgi) as described (Fichman et al., 2015). 555

556

557



24

Supplemental figures 558

Figure S1: Sequence elements on the P5CS1 promoter, 5’UTR, exon 1, intron 1 and exon 2. 559

Figure S2: Binding sites of 21 transcription factors on genomic regions of the P5CS1 gene. 560

Figure S3: Response of Arabidopsis plants to phosphate starvation. 561

Figure S4: P5CS1-GFP fluorescence in root tips of transgenic Arabidopsis plants. 562

Figure S5: Transcript profiles of proline genes during phosphate starvation. 563

Figure S5: Growth of phr1, phl1, phr1phl2 and aba2-3 mutants in the absence of Pi. 564

Figure S6: Activation of proline metabolic genes by PHR1. 565

Figure S7: Expression of marker genes in phosphate-starved Arabidopsis plants. 566

Figure S8: Growth of p5cs1-1, pdh1-4 and pdh2-2 mutants on Pi+ and Pi- media. 567

Figure S9: Expression of proline metabolism genes in p5cs1-1, pdh1-4 and pdh2-2 mutants. 568

Figure S10: Effect of externally supplied proline on plant growth. 569

Figure S11: Sequence elements on the PDH2 gene. 570

Figure S12: Transcript profiles of selected ABA-related genes during phosphate starvation. 571

Figure S13: Transcript profiles of PHR1 and PHL1 genes in response to salt and ABA. 572

Figure S14: Primers used in this study, and their nucleotide sequence. 573

574

Acknowledgements 575

The authors are grateful to János Györgyey (BRC, Szeged) for financial and technical support, 576

James Smart and Csaba Koncz for revision of the manuscript, Javier Paz-Ares (Centro 577

Nacional de Biotecnologia, Madrid, Spain) for providing seeds of phr1, phl1 and phr1phl1 578

mutants and PHR1.KA expressing transgenic lines, and to Annemarie H. Meijer (Leiden 579

University, Leiden, The Netherlands) for providing yeast one-hybrid vectors. 580

581

582



25

Figures 583

Figure 1. PHR1 and PHL1 factors bind to P5CS1 regulatory sequences. A) Schematic map of 584

the P5CS1 regulatory region, including promoter (-1.2 kb), 5’ UTR, first and second exons and 585

the first intron, to +0.8 kb. Schematic map was adapted from a previous report (Fichman et al., 586

2015). Positions of promoter, 5’UTR, exons and 1st intron, and predicted ABRE and P1BS 587

motifs are indicated. Fragments used for yeast one hybrid screen (Y1H, fragment 1), EMSA 588

(fragments 2-4) and ChIP amplification (fragment 5) are shown. B) Y1H test of PHR1 and PHL1 589

factors and P5CS1 genomic fragment as bait. C) Electrophoretic mobility assay (EMSA) of 590

purified PHR1 and PHL1 factors with 0.7 kb and 0.4 kb genomic fragments of the P5CS1 gene 591

(Fragments 2 and 4). Note, that increasing amount of PHR1 and PHL1 protein enhance the high 592

mobility complex with the 0.7 kb fragment. D) EMSA with wild type (Fragment 2), mutated 593

(Fragment 3) and deletion derivative (Fragment 4) of the region containing the P1BS site with 1 594

g purified PHR1 or PHL1 protein. Note, that electromobility shift can be observed only when 595

Fragment 2 was used, which contained the wild type P1BS sequence, but not with the mutated 596

or deleted version (Fragments 3 and 4, respectively). E) Chromatin Immunoprecipitation (ChIP) 597

assay. Normalized quantitative PCR data are shown, where the amount of P1BS-containing 598

PCR product (fragment 5) was related to PCR product obtained from a non-specific intergenic 599

region. HA: samples precipitated with anti-HA beads. GFP: samples precipitated by anti-GFP 600

beads. Input: qPCR data with samples without immunoprecipitation. Bars on diagrams indicate 601

standard error of three biological replicates. 602

Figure 2. Phosphate starvation leads to proline accumulation and P5CS1 activation in 603

Arabidopsis plants. A) Proline levels in wild type Arabidopsis plants grown with or without 604

phosphate for 14 days. B) Expression profiles of genes which control proline biosynthesis 605

(P5CS1, P5CS2, P5CR), or proline catabolism (P5CDH, PDH1, PDH2) in wild type Arabidopsis 606

plants grown with or without phosphate for 14 days. Values were normalized to transcript levels 607

of actin gene. C) GFP-derived fluorescence of P5CS1-GFP construct under phosphate 608

starvation. 5 days-old seedlings expressing the genomic P5CS1-GFP fusion (Székely et al., 609

2008) were transferred to standard culture medium (+Pi), or medium deprived of phosphate (-610

Pi), and GFP-derived fluorescence was recorded in 3-4 day intervals. Note the enhanced GFP 611

signals and proliferation of lateral roots in –Pi medium. D) Western detection of P5CS1-GFP 612

protein in phosphate-starved (14 days on Pi deficient medium) or salt-induced plants (14 days-613

old plants, treated with 75mM NaCl for 24 hours). Scale bar: 500μm. 614



26

Figure 3. Proline metabolism in phr1 and phl1 mutants. A) Proline levels in wild type (Col-0) 615

phr1, phl1 and double phr1phl1 mutants subjected to phosphate starvation for 14 days or 616

treated by 150 mM NaCl or 50 μM ABA for three days, after having grown on standard culture 617

medium for 14 days. B) Transcript levels of genes controlling proline metabolism in wild type 618

and mutant plants, growth with or without phosphate for 14 days. Relative transcript levels are 619

shown, normalized to transcript data of plants grown on +Pi medium (2,5 mM Pi). Bars on 620

diagrams indicate standard error, * and ** show significant differences to Col-0 wild type (A) or 621

to Pi+ medium (B) at p<0.05 and p<0.005, respectively (Student t-test). 622

Figure 4. Growth and viability of phr1, phl1 and aba2-3 mutants under phosphate starvation. A) 623

Wild type and mutant plants grown on standard (+Pi) and phosphate deficient (-Pi) culture 624

media for 14 days. B) Average rosette sizes of wild type and mutant plants after 14 days of 625

culture. C) Percentage of plants with bleaching leaves indicating cell death, after culture on 626

phosphate containing and deficient media for 14 days. Note, that wild type plants had no leaves 627

with necrotic symptoms. Bars on diagrams indicate standard error, * and ** show significant 628

differences to wild type at p<0.05 and p<0.005, respectively (Student t-test). 629

Figure 5. Abscisic acid regulates proline accumulation during phosphate starvation. A) Proline 630

levels of wild type (Col-0), an ABA-deficient mutant (aba2-3) and two ABA insensitive mutants 631

(abi4-1, abi5-1), which were cultured on media with or without phosphate (Pi+, Pi-) for 14 days. 632

Normalized values are shown, where 1 corresponds to proline levels of non-starved plants. B,C) 633

Expression of P5CS1 ( B ) and PDH2 ( C ) genes in shoots and roots of wild type (Col-0), aba2-634

3, abi4-1 and abi5-1 mutants. Relative expression is shown, normalized to transcript data of 635

plants grown on Pi-containing medium. Bars on diagrams indicate standard error, * and ** show 636

significant differences to not-treated (A) or wild type (B,C) plants at p<0.05 and p<0.005, 637

respectively (Student t-test). 638

Figure 6. Effect of proline accumulation on plant growth during phosphate starvation. A) Proline 639

levels are shown in Col-0 wild type, p5cs1-1, pdh1-4 and pdh2-2 mutants. B) Root elongation of 640

wild type and mutant plants grown in the presence or absence of 2,5 mM phosphate (+Pi and –641

Pi, respectively). Bars on diagrams indicate standard error, ** show significant differences to 642

wild type at p<0.05 (Student t-test). 643

Figure 7. Regulation of proline metabolism during osmotic stress and phosphate starvation. 644

During osmotic stress, proline accumulation takes place, controlled by the induction of P5CS1 645

and repression of PDH1 genes, respectively. P5CS1 activation in this process is controlled by 646



27

ABA signals, possibly through the ABRE cis acting motif in the promoter. Phosphate starvation 647

induces PHR1 and PHL1, which activates P5CS1 through binding to its P1BS motif. PDH2 is 648

also induced by PHR1 and PHL1 and Pi deficiency. NCED3 is induced during Pi deprivation, 649

which can enhance ABA levels. ABA signals restrict plant growth and activate numerous stress-650

related genes, incuding PHL1 and P5CS1. 651

652



28

653



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http://www.ncbi.nlm.nih.gov/pubmed?term=Achard P%2C Cheng H%2C De Grauwe L%2C Decat J%2C Schoutteten H%2C Moritz T%2C Van Der Straeten D%2C Peng J%2C Harberd NP %282006%29 Integration of plant responses to environmentally activated phytohormonal signals%2E Science 311%3A 91%2D94&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Doerner P %282008%29 Phosphate starvation signaling%3A a threesome controls systemic P%28i%29 homeostasis%2E Curr Opin Plant Biol 11%3A 536%2D540&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fabro&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fabro&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Fichman Y%2C Gerdes SY%2C Kovacs H%2C Szabados L%2C Zilberstein A%2C Csonka LN %282015%29 Evolution of proline biosynthesis%3A enzymology%2C bioinformatics%2C genetics%2C and transcriptional regulation%2E Biol Rev Camb Philos Soc 90%3A 1065%2D1099&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Forster%2DFromme K%2C Jendrossek D %282010%29 AtuR is a repressor of acyclic terpene utilization %28Atu%29 gene cluster expression and specifically binds to two 13 bp inverted repeat sequences of the atuA%2DatuR intergenic region%2E FEMS Microbiol Lett 308%3A 166%2D174&dopt=abstract

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Methods Enzymol 350: 87-96Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Golldack D, Li C, Mohan H, Probst N (2013) Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorableconditions. Plant Cell Rep 32: 1007-1016


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Haring M, Offermann S, Danker T, Horst I, Peterhansel C, Stam M (2007) Chromatin immunoprecipitation: optimization, quantitativeanalysis and data normalization. Plant Methods 3: 11


Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. ArchBiochem Biophys 125: 189-198


Herrera-Estrella L, Lopez-Arredondo D (2016) Phosphorus: The Underrated Element for Feeding the World. Trends Plant Sci 21: 461-463


Hoque MA, Banu MN, Nakamura Y, Shimoishi Y, Murata Y (2008) Proline and glycinebetaine enhance antioxidant defense andmethylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol 165: 813-824


Hu CA, Delauney AJ, Verma DP (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps inproline biosynthesis in plants. Proc Natl Acad Sci U S A 89: 9354-9358


Ibarra JA, Villalba MI, Puente JL (2003) Identification of the DNA binding sites of PerA, the transcriptional activator of the bfp and peroperons in enteropathogenic Escherichia coli. J Bacteriol 185: 2835-2847


Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulationof drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis inArabidopsis. Plant J 27: 325-333


Jiang ZF, Huang SZ, Han YL, Zhao JZ, Fu JJ (2012) Physiological response of Cu and Cu mine tailing remediation of Paulownia fortunei(Seem) Hemsl. Ecotoxicology 21: 759-767


Karthikeyan AS, Ballachanda DN, Raghothama KG (2009) Promoter deletion analysis elucidates the role of cis elements and 5'UTRintron in spatiotemporal regulation of AtPht1;4 expression in Arabidopsis. Physiol Plant 136: 10-18


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http://www.ncbi.nlm.nih.gov/pubmed?term=Heath RL%2C Packer L %281968%29 Photoperoxidation in isolated chloroplasts%2E I%2E Kinetics and stoichiometry of fatty acid peroxidation%2E Arch Biochem Biophys 125%3A 189%2D198&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hoque MA%2C Banu MN%2C Nakamura Y%2C Shimoishi Y%2C Murata Y %282008%29 Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl%2Dinduced damage in cultured tobacco cells%2E J Plant Physiol 165%3A 813%2D824&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Hu CA%2C Delauney AJ%2C Verma DP %281992%29 A bifunctional enzyme %28delta 1%2Dpyrroline%2D5%2Dcarboxylate synthetase%29 catalyzes the first two steps in proline biosynthesis in plants%2E Proc Natl Acad Sci U S A 89%3A 9354%2D9358&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Iuchi S%2C Kobayashi M%2C Taji T%2C Naramoto M%2C Seki M%2C Kato T%2C Tabata S%2C Kakubari Y%2C Yamaguchi%2DShinozaki K%2C Shinozaki K %282001%29 Regulation of drought tolerance by gene manipulation of 9%2Dcis%2Depoxycarotenoid dioxygenase%2C a key enzyme in abscisic acid biosynthesis in Arabidopsis%2E Plant J 27%3A 325%2D333&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jiang ZF%2C Huang SZ%2C Han YL%2C Zhao JZ%2C Fu JJ %282012%29 Physiological response of Cu and Cu mine tailing remediation of Paulownia fortunei %28Seem%29 Hemsl%2E Ecotoxicology 21%3A 759%2D767&dopt=abstract

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AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stressresponses. Plant J 50: 347-363


Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, anenzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8: 1323-1335


Klecker M, Gasch P, Peisker H, Dormann P, Schlicke H, Grimm B, Mustroph A (2014) A Shoot-Specific Hypoxic Response ofArabidopsis Sheds Light on the Role of the Phosphate-Responsive Transcription Factor PHOSPHATE STARVATION RESPONSE1.Plant Physiol 165: 774-790


Laloi C, Havaux M (2015) Key players of singlet oxygen-induced cell death in plants. Front Plant Sci 6: 39Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39: 949-962Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Leon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JA, Koornneef M (1996) Isolation andcharacterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10: 655-661


Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T))Method. Methods 25: 402-408


Lohman KN, Gan SS, John MC, Amasino RM (1994) Molecular Analysis of Natural Leaf Senescence in Arabidopsis-Thaliana. PhysiologiaPlantarum 92: 322-328


Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floralpatterning in Arabidopsis. Cell 105: 793-803


Lopez-Arredondo DL, Leyva-Gonzalez MA, Gonzalez-Morales SI, Lopez-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition:improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65: 95-123


Lopez-Molina L, Chua NH (2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol 41:541-547


Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156: 1041-1049


Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de La Pena A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on theexpression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559-567

Pubmed: Author and Title https://plantphysiol.orgDownloaded on May 21, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

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http://search.crossref.org/?page=1&rows=2&q=Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8: 1323-1335

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http://search.crossref.org/?page=1&rows=2&q=Lohman KN, Gan SS, John MC, Amasino RM (1994) Molecular Analysis of Natural Leaf Senescence in Arabidopsis-Thaliana. Physiologia Plantarum 92: 322-328

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http://search.crossref.org/?page=1&rows=2&q=Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105: 793-803

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Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR (2007)Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85-112


Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome revealsinteraction of phosphate and sugar metabolism. Plant Physiol 143: 156-171


Nilsson L, Lundmark M, Jensen PE, Nielsen TH (2012) The Arabidopsis transcription factor PHR1 is essential for adaptation to highlight and retaining functional photosynthesis during phosphate starvation. Physiol Plant 144: 35-47


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http://search.crossref.org/?page=1&rows=2&q=Mattioli R, Falasca G, Sabatini S, Altamura MM, Costantino P, Trovato M (2009) The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiol Plant 137: 72-85

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http://search.crossref.org/?page=1&rows=2&q=Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143: 156-171

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http://www.ncbi.nlm.nih.gov/pubmed?term=Rouached H%2C Arpat AB%2C Poirier Y %282010%29 Regulation of phosphate starvation responses in plants%3A signaling players and cross%2Dtalks%2E Mol Plant 3%3A 288%2D299&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Savour� A%2C Hua XJ%2C Bertauche N%2C Van Montagu M%2C Verbruggen N %281997%29 Abscisic acid%2Dindependent and abscisic acid%2Ddependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana%2E Mol Gen Genet 254%3A 104%2D109&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Savour� A, Hua XJ, Bertauche N, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet 254: 104-109

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http://www.ncbi.nlm.nih.gov/pubmed?term=Schat H%2C Sharma%2C S%2ES%2E%2C and Vooijs%2C R%2E %281997%29 Heavy metal%2Dinduced accumulation of free proline in a metal%2Dtolerant and a nontolerant ecotype of Silene vulgaris%2E Physiol%2E Plant%2E 101%3A 477%2D482&dopt=abstract

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http://scholar.google.com/scholar?as_q=Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Yoshiba&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang CS%2C Lu Q%2C Verma DP %281995%29 Removal of feedback inhibition of delta 1%2Dpyrroline%2D5%2Dcarboxylate synthetase%2C a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants%2E J Biol Chem 270%3A 20491%2D20496&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zhang CS, Lu Q, Verma DP (1995) Removal of feedback inhibition of delta 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. J Biol Chem 270: 20491-20496

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou J%2C Goldsbrough PB %281994%29 Functional homologs of fungal metallothionein genes from Arabidopsis%2E Plant Cell 6%3A 875%2D884&dopt=abstract

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http://scholar.google.com/scholar?as_q=Functional homologs of fungal metallothionein genes from Arabidopsis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zouari M%2C Ben Ahmed C%2C Elloumi N%2C Bellassoued K%2C Delmail D%2C Labrousse P%2C Ben Abdallah F%2C Ben Rouina B %282016%29 Impact of proline application on cadmium accumulation%2C mineral nutrition and enzymatic antioxidant defense system of Olea europaea L%2E cv Chemlali exposed to cadmium stress%2E Ecotoxicol Environ Saf 128%3A 195%2D205&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Zouari M, Ben Ahmed C, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Ben Abdallah F, Ben Rouina B (2016) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Saf 128: 195-205

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zouari&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L&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=Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zouari&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1


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