Oxygen sensing and integrative stress signaling in plants132 retrograde signals in hypoxia has been partly investigated, for example mitochondrial ROS 133 signals were shown to impact

1

Short title: Integrative oxygen sensing and signaling in plants 1

Corresponding author: Joost T. van Dongen 2

RWTH Aachen University, 3

Institute of Biology I, 4

Worringerweg 1, 5

D-52074 Aachen, 6

Germany 7

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Full title: Oxygen sensing and integrative stress-signaling in plants 9

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Authors: Romy R. Schmidt, Daan A. Weits, Claudio FJ Feulner, Joost T. van Dongen 11

RWTH Aachen University, Institute of Biology I, Worringerweg 1, D-52074 Aachen, Germany 12

13

The research on abiotic stress responses in the van Dongen laboratory is financed by 14

RWTH Aachen University and the German Science Foundation. 15

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Summary statement: Integration of multiple cellular signals provides new opportunities in 17 understanding oxygen sensing and response mechanisms in plants. 18

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Author contribution: All authors contributed to conceiving and write the manuscript. 21

Plant Physiology Preview. Published on November 21, 2017, as DOI:10.1104/pp.17.01394

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Oxygen sensing and integrative stress-signaling in plants 22

23

Romy R. Schmidt, Daan A. Weits, Claudio FJ Feulner, Joost T. van Dongen 24

RWTH Aachen University, Institute of Biology I, Worringerweg 1, D-52074 Aachen, Germany 25

26

Introduction 27

Plants grow in a dynamic environment and continuously face numerous stress conditions in 28

parallel. This fluctuating environment pushed the evolution of extensive metabolic flexibility 29

(Sweetlove et al., 2010; van Dongen et al., 2011). Flooding is an example of an 30

environmental condition that combines many different stress factors simultaneously, 31

including limited gas diffusion (e.g. of oxygen, carbon dioxide and ethylene), temperature 32

stress, light quality and -quantity, osmotic and oxidative stress. Changes in the internal 33

concentration of oxygen, but also e.g. ethylene are crucial early signals for the initiation of 34

adaptation strategies to flooding (Sasidharan and Voesenek, 2015; Sasidharan et al., in 35

press). Initially, a plant cell responds to nearly all these different types of stresses by using 36

the same set of second messengers (such as ROS, calcium, NO and lipid molecules), and 37

by activating signalling cascades through kinases (Bjornson et al., 2010; Zhu, 2016). This 38

raises the question, how do cells detect and differentiate between stresses. 39

One fundamental aim in low-oxygen research is to unravel how organisms detect and react 40

to the lack of oxygen and respond to an impairment of their energy metabolism (Ratcliffe, 41

2013). In both plants (Licausi et al., 2011a; Gibbs et al., 2011; Weits et al., 2014; Gibbs et 42

al., 2014; White et al. 2017) and animals (Loenarz and Schofield, 2011; Ratcliffe, 2013; 43

Bishop and Ratcliffe 2014; Hamanaka et al., 2016) key transcriptional regulators have been 44

identified that regulate the hypoxic response via the integration of cellular signals that are 45

required for their activation (Box 1). Here, we discuss the nature and origin of these various 46

signals under hypoxia that initiate adaptation responses at the transcriptional and (post) 47

translational level and their potential integration points. In addition, we postulate that it is the 48

integration of different signal inputs that defines a response specific to oxygen limitation. 49

Further, we will discuss the state of current methods and technologies to measure plant 50

internal oxygen concentrations. 51

52

53



3

The concept of an integrative oxygen sensing mechanism 54

Abiotic stress perception appears not to rely on the detection of only one specific effector or 55

ligand. Despite all efforts to reveal the primary sensors for diverse abiotic stresses, 56

unequivocal identification remains arduous (Zhu et al., 2016). In Arabidopsis (Arabidopsis 57

thaliana), the N-end rule pathway of targeted proteolysis was shown to act as a mechanism 58

which controls protein levels of ERFVII transcription factors by regulating their protein 59

turnover in an oxygen concentration dependent manner (Gibbs et al., 2011; Licausi et al., 60

2011a; Box 1). Remarkably, protein abundance of RAP2.12, an ERFVII member in 61

Arabidopsis, is also positively regulated by HYDRAULIC CONDUCTIVITY OF ROOT 1 62

(HCR1), a Raf-like MAPKKK which could phosphorylate RAP2.12 in vitro. This N-end rule-63

independent stabilization mechanism is proposed to allow the integration of cation 64

(specifically potassium) availability with the oxygen concentration in the soil (Shahzad et al., 65

2016). 66

Low-oxygen stress impairs diverse plant cellular functions, including those in the cytosol, 67

nucleus, mitochondria, and endoplasmic reticulum (ER). Actually, molecular oxygen is 68



4

among the most-utilized molecules in eukaryotic cellular metabolism (Raymond and Segré, 69

2006) with more than 350 oxygen-dependent reactions. Thus, decreasing oxygen levels 70

might be indirectly sensed due to an impairment of various metabolic pathways when the 71

cellular oxygen concentration changes around or below the Km for oxygen of the enzymes 72

involved As such, any oxygen-dependent enzyme has the potential to act as a kind of 73

sensor, suggesting simultaneous oxygen sensing at multiple sites of the cell. Then again, it 74

might well be that one or a few oxygen-concentration dependent enzymes evolved to 75

primarily monitor aerobic metabolism. 76

Taken together, three scenarios of cellular oxygen sensing can be discussed: (1) 77

decentralized sensing at many sites of the cell by e.g. oxygen-consuming enzymes, (2) a 78

primary 'oxygen sensor' detects a drop in oxygen to initiate all signalling cascades, and (3) a 79

combination of scenario (1) and (2). A primary oxygen sensor (scenario 2) would detect the 80

cellular oxygen concentration but not the oxygen availability. However, differentiation 81

between “concentration” and “availability” is important, since a low oxygen concentration can 82

result in a high flux of oxygen into the tissue and does not necessarily lead to low-oxygen 83

stress. The advantage of a decentralized oxygen sensing mechanism (scenario 1) would be 84

that it allows for fine-tuning the response to low oxygen conditions to a particular situation. 85

By adding up various oxygen-concentration related signals, such integrative signalling would 86

trigger hypoxic responses only when the actual oxygen concentration does indeed disturb 87

cellular homeostasis. The decentralized oxygen sensing model further suggests that 88

perturbations of processes in various organelles, at the plasma membrane and in the cytosol 89

can initiate low-oxygen stress signalling, and that these various triggers must be integrated 90

to activate appropriate transcriptional reprogramming and cellular adaptation responses. A 91

specific balance between multiple stress-induced signals could provide a mechanism - like a 92

‘cellular fingerprint’ – to discriminate between different stress types. 93

In this review, we summarize signalling pathways from different cellular compartments which 94

are initiated by low-oxygen stress and discuss potential integration points for the multiple 95

signal inputs resulting in hypoxia-specific adaptive responses. 96

97

N-end rule pathway 98

In Arabidopsis, members of the ERFVII transcription factor family (Box 1) contain a 99

conserved N-terminal domain which makes them oxygen- and nitric oxide (NO)-dependent 100

substrates of the N-end rule pathway of targeted proteolysis (Gibbs et al., 2016a). 101



5

While the N-end rule is acting as a safe-guard mechanism to limit ERFVII abundance under 102

aerobic conditions, several observations suggest that its control is limited to certain Met-Cys 103

proteins, environmental conditions and developmental phases of the plant. Arabidopsis N-104

end rule mutant seedlings show constitutive expression of about half of the core hypoxia-105

responsive genes (Gibbs et al., 2011), indicating that the other hypoxia genes are not 106

controlled by this pathway. In addition, introduction of a β-Glucoronisidase (GUS) reporter 107

driven by the ALCOHOL DEHYDROGENASE 1 (ADH1) promoter in Arabidopsis wildtype 108

seedlings or a proteolysis6 (prt6) mutant defective in ERFVII turnover revealed constitutive 109

activation of the promoter in certain tissues of the prt6 mutant, but not in all as compared to 110

the wildtype. Interestingly, in both the wildtype and the prt6 mutant an increased GUS signal 111

was observed after 6 hours of hypoxia (Gibbs et al., 2011). Thus, in N-end rule mutants, the 112

hypoxic response is not entirely disrupted, nor do mutations in this pathway affect all plant 113

tissues in a similar manner. While constitutive expression of a subset of hypoxic genes is 114

observed in N-end rule mutant seedlings, a recent report revealed that this constitutive 115

expression is less pronounced in adult mutant plants (Giuntoli et al., 2017). As submergence 116

of rosette-stage plants just prior to bolting still results in the activation of hypoxic genes, it 117

strongly argues for additional N-end rule-independent mechanisms that control either ERFVII 118

activity or alternative transcriptional cascades. In addition, at least one ERFVII, SUB1A from 119

rice, is not a target of the N-end rule pathway although it possesses the N-terminal 120

consensus sequence as found in Arabidopsis ERFVIIs (Gibbs et al., 2011). This further 121

suggests alternative regulatory pathways. 122

123

Mitochondrial dysfunction as trigger for hypoxia signalling 124

Limited oxygen availability affects respiration, which impacts on a whole palette of 125

mitochondrial parameters and processes (see Box 2), including reactive oxygen and 126

nitrogen species (ROS/RNS) homeostasis, redox status of NAD(P)H and antioxidant pools, 127

ATP/ADP ratio, the proton-motive force, calcium and metabolite levels, which in principle 128

could all trigger mitochondrial signalling (Schwarzlander and Finkemeier, 2013). Indeed, 129

roles for these diverse signals in mitochondrial retrograde responses have been established, 130

and are discussed by Wagner et al. (2018) in this Focus Issue. The role of mitochondrial 131

retrograde signals in hypoxia has been partly investigated, for example mitochondrial ROS 132

signals were shown to impact on anoxia tolerance (Chang et al., 2012). Likewise, in animals, 133

mitochondrial electron transport chain (mETC)-derived ROS signals appear to provoke 134

adaptation responses upon hypoxia (Hamanaka et al., 2016). Interestingly, complex III 135

inhibition under aerobic conditions by antimycin-A treatment in part causes induction of 136



6

hypoxia-responsive genes in Arabidopsis (Ng et al., 2013a), which could be due to disruption 137

of the ATP/ADP ratio and/or increased mitochondrial ROS production. Furthermore, 138

metabolic signals derived from mitochondria might be integrated into cellular reprogramming 139

during hypoxia. This is supported by the notion that overexpression of the mitochondrial 140

UNCOUPLING PROTEIN 1 (UCP1), which decreases stress-induced ROS production, 141

results in a hypoxic metabolic pattern and transcriptomic signature (Bareto et al. 2016). UCP 142

proteins in animals have been linked to the induction of hypoxic responses (Dromparis et al., 143

2013), suggesting a universal role of this protein family in controlling low-oxygen responses. 144

An important feature of plant mitochondria is that the proton-translocating complexes I, III 145

and IV (see Box 2) are capable of forming so-called super-complexes (Dudkina et al., 2005). 146

Remarkably, mitochondrial super-complex assembly is oxygen dependent, as in potato 147

tubers low oxygen promotes dissociation of complex I from the super-complex while re-148

assembly is observed under reoxygenation (Ramírez-Aguilar et al., 2011). Supplying 149

isolated mitochondria with succinate under a low pH also caused dissociation of complex I 150

as observed for low oxygen conditions. Substrate-dependent supercomplex formation was 151

also found in mouse cells, in which the plasticity of the mETC complexes appears to be used 152

to fine-tune respiration (Lapuente-Brun et al., 2013). That said, it still needs to be 153

demonstrated that supercomplex formation also affects respiration rates in plant 154

mitochondria. Taken together, the release of complex I from the super-complex does not 155

appear to be the initial trigger for hypoxic responses in plants, but is already part of the 156

adaptation response that is initiated by a drop in pH and a change in substrate availability. 157



7

158

When the oxygen concentration is reduced below a certain threshold, respiration is impaired 159

(Nikoloski and van Dongen 2011). However, it remains to be determined at what sub-cellular 160

oxygen concentration mitochondrial dysfunction is initiated. Precise determination of the 161

mitochondrial oxygen concentration is especially important as the afinity for oxygen of 162

Cytochrome c Oxidase likely depends on cellular conditions such as pH, redox status, and 163

oxygen concentration (Krab et al., 2011). Also, it is to be determined whether this respiratory 164

impairment is specific to hypoxia or if other abiotic stresses cause similar mitochondrial 165

constraints too? UCPs, TYPE II NAD(P)H DEHYDROGENASEs, and ALTERNATIVE 166

OXIDASE (AOX) as part of the mitochondrial energy dissipation pathways (see box 2; 167

Maxwell et al. 1999; Geisler et al. 2007; Millar et al. 2011) have roles in the response to 168

diverse abiotic and biotic stresses, which in general cause an energy crisis (Pu et al., 2015; 169

Zhu, 2016). Beyond that, mitochondrial ROS production with signalling function can be 170

observed under salt or drought stress (Hernandez et al., 1993; Pastore et al., 2007), 171

indicating that stress signals released upon mitochondrial dysfunction are not hypoxia-172

specific per se. A fundamental biological question that needs further attention is how cells 173

distinguish between hypoxia-induced mitochondrial signals and those induced by other 174

stresses. 175

176

The endoplasmic reticulum as signalling hub 177

Protein folding in the ER is essential for the stability and functionality of many secreted and 178

membrane-bound proteins. Although the ER employs different proteins and pathways for this 179

task, it is inevitable that some proteins get misfolded especially during stress (Hedge and 180

Ploegh, 2010). ER stress results in the activation of the unfolded protein response (UPR), 181

which enhances the function of the protein folding machinery and the protein quality control 182

system, see Liu and Howell (2016) for a detailed overview. The major pathway for oxidative 183

protein folding is present in the endoplasmic reticulum (ER) and relies on protein disulfide 184

isomerase (PDI) and ER thiol oxidase (ERO) proteins (Aller and Meyer; 2013). PDI oxidizes 185

proteins, and is regenerated by ERO through the transfer of electrons from PDI to molecular 186

oxygen. The Km of the ERO protein from yeast was found to be 4-10 µM for oxygen, which is 187

similar to that of AOX in plants (Gross et al., 2006). If plant ERO1 proteins display a similar 188

Km as their yeast counterpart for oxygen, then they would be functionally impaired under 189

hypoxia and might act as sensors for low-oxygen conditions. Interestingly, only the disulfide 190

bond formation during the folding phase in the ER involving EROs was shown to be oxygen-191

dependent in mammalian cells, while subsequent glycosylation, ER export, Golgi processing 192



8

and transit to the extracellular space were not (Koritzinsky et al., 2013). As oxygen-193

dependent folding is directly impaired upon low oxygen stress, it has been suggested that 194

the ER constitutes a cellular oxygen sensor in animals that contributes to signalling and 195

survival during hypoxic conditions (Wouters and Koritzinsky, 2008). Future work is required 196

to understand if this putative ER pathway also plays a role in plants. Of note, in 197

mitochondria, oxidative protein folding relies on a FAD-dependent thiol oxidase that acts in 198

an oxygen-dependent manner (Ang et al., 2014), suggesting that other protein folding 199

pathways might have a role in low-oxygen stress. 200

Interestingly, the ER also represents an important crossroad for mitochondrial stress signals. 201

Disturbance of mitochondrial function results in a signal to the nucleus, the so-called 202

mitochondrial retrograde regulation (MRR) (Rhoads and Subbaiah 2007). MRR relies on 203

both ROS and calcium signals and recently, several of the protein components of the 204

pathway were uncovered.Transmembrane-domain containing NO APICAL MERISTEM / 205

ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR / CUP-SHAPED COTYLEDON 206

(NAC) transcription factors were found to act as important modulators of the transcriptional 207

response during MRR (De Clercq et al. 2013; Ng et al., 2013b). Both ANAC013 and 208

ANAC017 mediate MRR responses but are located at the ER, indicating that mitochondrial 209

signals are received at the ER. In this case, the mitochondrial signal is proposed to activate 210

a yet unknown protease that releases the NAC transcription factors from the ER membrane, 211

which subsequently travel to the nucleus to modulate expression. Many of the MRR-induced 212

genes are also hypoxia responsive, including the ERFVII transcription factor gene HYPOXIA 213

RESPONSIVE ERF 2 (HRE2), encoding a regulator of anaerobic responses in Arabidopsis 214

(Licausi et al., 2010). Therefore, it would be worthwhile to analyse the contribution of ER-215

mediated MRR to low-oxygen tolerance in plants. 216

217

Energy signalling 218

The harmful character of low-oxygen stress lies in its impact on oxidative phosphorylation in 219

the mitochondrion, which delivers energy equivalents in the form of ATP (Millar et al. 2011). 220

However, a low local oxygen concentration does not necessarily lead to an energy crisis 221

when the flux of oxygen towards the mitochondria can keep pace with respiratory oxygen 222

consumption. Therefore, it is of importance that any changes in the ATP-producing 223

processes within mitochondria are communicated to other compartments to induce 224

appropriate adaptive responses. By doing so, differentiation is required between (a) an 225

energy crisis that is induced by mitochondrial dysfunction due to hypoxia, and (b) a low-226

energy status that is caused by high ATP consumption due to metabolic activity. Only 227



9

sensing cellular oxygen levels without taking into account the actual energy charge of the 228

cell could provoke cost-intensive adaptation responses in tissues with high respiratory 229

activity. For detailed discussion of mitochondrial energy signalling we would like to refer to 230

the Update of Wagner et al. (2018) in this Focus Issue. 231

Eukaryotic energy sensing is largely conserved and involves the two kinases sucrose 232

nonfermenting 1–related kinase 1 (SnRK1) and target of rapamycin (TOR) in both plants and 233

animals (Broeckx et al., 2016). Plant SnRK1 is activated in response to energy-depleting 234

stress conditions to promote plant survival. Loss of SnRK1 function impairs submergence 235

tolerance in plants (Cho et al., 2012). It is important to note that SnRK1 appears to sense the 236

AMP/ATP ratio and ADP/ATP ratio in cells, linking its activation directly to an energy crisis 237

(Hardie, 2011). Many different stresses can cause an energy crisis, not surprisingly, most of 238

the core anaerobic genes are not hypoxia specific (van Dongen and Licausi, 2015). 239

Stresses that provoke a cellular 'energy crisis' evoke translational repression, which has also 240

been observed during hypoxia (Branco-Price et al., 2008; Mustroph et al., 2009). In 241

eukaryotic cells, growth in response to energy availability is in part controlled by the TOR 242

protein kinase (Dobronel et al., 2016). TOR controls translation initiation and has been 243

shown to be inactivated in mammalian cells upon hypoxia (Wouters and Koritzinsky, 2008). 244

In plants, a picture has emerged in which TOR kinase is active under favourable energy 245

conditions, while SnRK1 is stimulated upon energy limitation (Tomé et al., 2014). Moreover, 246

TOR and SnRK1 appear to act antagonistically. So far, the function of SnRK1 under low 247

oxygen conditions in plants is well established, however, a role for TOR is still unexplored. 248

ROS signalling 249

Cellular imbalances as a result of abiotic stress cause a change in ROS homeostasis. In 250

addition, during initial stress exposure, a so-called oxidative burst is observed, which acts as 251

a signal to initiate adaptive responses (Schippers and Schmidt, 2016). Although 252

counterintuitive, mitochondrial ROS function in retrograde signalling during oxygen 253

deprivation to adjust energy management in yeast and animal cells (Guzy et al. 2007; 254

Hamanaka et al., 2016). Also in plants, a mitochondrial ROS burst is observed upon a drop 255

in oxygen levels (Chang et al., 2012). As application of antimycin-A mimics this burst, it is 256

suggested that superoxide (O2-) derived from complex III might act as a signalling molecule 257

during mitochondrial dysfunction upon oxygen deprivation. In order to prevent the build-up of 258

high levels of superoxide, mitochondria actively scavenge it by employing MANGENESE 259

SUPEROXIDE DISMUTASE (MnSOD). The hydrogen peroxide (H2O2) produced during this 260

reaction either oxidizes mitochondrial proteins or exits the organelle to induce downstream 261



10

signalling responses. To exit mitochondria, H2O2 would rely on aquaporins (Bienert et al., 262

2007). 263

Within the cytosol, ROS as signalling molecules are rather short-lived due to the high 264

antioxidant capacity. Moreover, to provide mitochondrial specificity to the ROS signal, the 265

sensing and translation of this signal is expected to occur near the mitochondrial surface. So 266

far, release of H2O2 by mitochondria during oxygen deprivation into the cytosol has been 267

linked to the activation of MPK3 and MPK6 in Arabidopsis (Chang et al., 2012). The fact that 268

these MPKs are involved in a broad range of biotic and abiotic stress pathways (Suarez-269

Rodriguez et al., 2010) implies that they are integrated into local sensory complexes to 270

maintain ROS-source information to activate stress-specific responses. As loss of function 271

mutants of either MPK3 or MPK6 do not largely affect the activation of anaerobic genes 272

(Chang et al., 2012), additional components in the mitochondrial ROS-signalling pathway 273

related to low-oxygen stress await to be uncovered. Here, it is of interest to note that 274

mitochondria are often in direct contact with the ER (Mueller and Reski, 2015), which 275

therefore might be involved in relaying or translating the mitochondrial ROS signal. 276

Next to the transient mitochondrial oxidative burst upon oxygen deprivation, a plasma 277

membrane-localized burst occurs through the activation of calcium-dependent NADPH 278

oxidases (Blokhina et al., 2001; Baxter-Burell, 2002). As RBOH-dependent ROS production 279

occurs during nearly every stress, it remains unclear how such signals can be rendered 280

specific for low oxygen stress. 281

Arabidopsis contains ten NADPH oxidases, called RESPIRATORY BURST OXIDASE 282

HOMOLOGS (RBOHs), of which three - RBOHD, RBOHbohF and RBOHI - have been 283

implicated in low-oxygen responses (Pucciariello et al., 2012; Liu et al., 2017; Lin et al., 284

2017). Although fermentative genes including ADH1 have been shown to depend on single 285

Rboh activity, the exact mechanism through which each Rboh contributes to low-oxygen 286

signalling needs further investigation. Recently, RbohI activity providing submergence 287

tolerance could be linked to auxin signalling (Lin et al., 2017). NADPH oxidases are 288

activated by RHO-LIKE SMALL G-PROTEIN OF PLANTS (ROP) and calcium-dependent 289

kinases (Baxter-Burell et al., 2002; Suzuki et al., 2011). ROP promotes the oxidative burst 290

during oxygen deprivation by activating NADPH oxidases. The burst is transient as H2O2 291

activates ROP GTPASE ACTIVATING PROTEIN 4 (RopGAP4), which deactivates ROP 292

signalling (Baxter-Burell et al., 2002). Plants lacking RopGAP4 show impaired low-oxygen 293

tolerance. Recently, it was found that the ERFVII transcription factor RAP2.12 activates the 294

expression of HYPOXIA RESPONSIVE UNIVERSAL STRESS PROTEIN 1 (HRU1), 295

which, like RopGAP4, acts to dampen NADPH oxidase activity (Gonzali et al. 2015). 296



11

Potentially, RopGAP4 and HRU1 not only limit the length of the initial apoplastic ROS burst, 297

but might be involved in protecting the plants from an oxidative burst upon reoxygenation. 298

Studies on mammalian cells suggest a feed-forward loop between the mitochondrial ROS 299

burst and the activation of NADPH oxidases (Kröller-Schön et al., 2014). So far, this concept 300

has not been studied in plant cells, but it would be intriguing to be investigated further. 301

302

Calcium signalling 303

NADPH oxidase-driven ROS production depends on calcium, while ROS in turn can 304

modulate calcium uptake into the cytosol (Mazars et al., 2010; Suzuki et al., 2011), which 305

lets both second messengers be part of a tightly linked signalling cross-talk. Stress induces 306

an increase in cytoplasmic calcium levels, which activates diverse calcium-binding proteins 307

that decode the calcium signal into a cellular and transcriptional response (Dodd et al, 2010). 308

Amongst these calcium-activated proteins are kinases, enzymes and transcription factors. 309

The increase in cytosolic calcium levels occurs through the release of calcium from the 310

apoplast and/or cellular organelles (Edel et al., 2017). 311

Early anoxia studies revealed a rise in cytosolic calcium levels by using an AEQUORIN-312

based reporter in Arabidopsis (Sedbrook et al., 1996). Upon oxygen deprivation, a biphasic 313

calcium response was observed, with a first initial short-lived calcium spike occuring within 314

minutes of anoxia, followed by a second, prolonged calcium response that lasted several 315

hours. In addition, the authors showed that inhibition of calcium fluxes by calcium channel 316

blockers resulted in a partial inhibition of ADH1 expression under anoxia. Also in maize, the 317

use of such blockers impairs the expression of ADH1 under low oxygen stress (Subbaiah et 318

al., 1994). Still, the extent to which calcium fluxes and signalling events influence anaerobic 319

gene expression is largely unexplored in plants. 320

Cytosolic calcium homeostasis is rapidly restored after a calcium spike by active transport 321

mechanisms (Sanders et al., 2002). In plants, energization relies either on calcium pumps 322

powered by ATP hydrolysis or by Ca2+/H+ antiporters powered by a proton-motive force 323

(Dodd et al., 2010). The energy-consuming transport of calcium is essential to obtain the 324

basal levels, against which calcium release channels operate transiently to elevate free 325

cytosolic calcium levels upon a stress stimulus. Thus, after the cytosolic calcium spike, pre-326

stress levels need to be restored to keep the system sensitive towards a follow-up transient 327

increase in calcium (Bose et al., 2011). These properties suggest that calcium signalling 328

might be restricted to the initial phase of low-oxygen stress, as increasing ATP constrains 329



12

and the pH change under prolonged stress conditions might impair calcium homeostasis 330

mechanisms. 331

The origin of calcium released into the cytosol under low-oxygen stress in plants is partly 332

explored. Both plasma membrane calcium channel blockers as well as intracellular calcium 333

channel blockers in part block calcium-dependent hypoxic responses (Sedbrook et al., 1996; 334

Yemelyanov et al., 2011). Potential intracellular calcium sources for the cytosolic spike 335

during oxygen deprivation might be the vacuole, the ER and mitochondria. Although roles for 336

ER and mitochondria in cytosolic calcium release have been described in mammalian cells 337

(Rizzuto et al., 2012; Wiel et al., 2014), it is still unclear to which extent these organelles 338

contribute to calcium signalling under abiotic stresses in plants. 339

In rice, CALCINEURIN B-LIKE INTERACTING PROTEIN KINASE 15 (OsCIPK15) has been 340

shown to be required for the expression of genes encoding glycolytic enzymes, including 341

ADH (Lee et al., 2009; Meyer et al., 2010). Excitingly, OsCIPK15 is activated by SnRK1, 342

linking it to the energy sensing network. Energy saving as an adaptation response to low-343

oxygen stress can be achieved by controlled selective translation of mRNA (Sorenson and 344

Bailey-Serres, 2014), a process which is regulated in a calcium-dependent manner. 345

CALMODULIN38 (CML38) from Arabidopsis acts as potential calcium sensor which co-346

localizes under low-oxygen stress to messenger RNA ribonucleoprotein particles including 347

stress granules. Latter are formed under hypoxia to serve as storage of translationally 348

inhibited mRNA (Lokdarshi et al., 2016). 349

Taken together, despite the unquestionably eminent role of calcium in the initial response to 350

low-oxygen stress, major gaps exist regarding the regulation of calcium fluxes, homeostasis 351

and the role of specific calcium sensor and signalling proteins in adaptation to hypoxia. 352

353

Measuring oxygen concentrations in plants 354

A major bottleneck for the research on low-oxygen stress is that accurate measurements of 355

in situ oxygen concentrations in plants are difficult. Tools and methods to resolve the 356

dynamic variation in oxygen levels with spatial and temporal resolution are needed for a 357

better understanding of low oxygen signaling at the cellular level. 358

Over the years, numerous methods for accurate measurement of oxygen have been 359

developed (Box 3). Invasive oxygen measurements using Clark-type oxygen electrodes and 360

optical oxygen sensors are commonly used, and led to our current understanding on the 361

dynamics and distribution of oxygen in plants. Still, the development of non-invasive oxygen 362

measurement methods in plants is largely lacking behind as compared the mammalian field, 363



13

were cancer research has driven the development of a broad range of methods for the 364

detection of hypoxia within animal tissue, such as soluble oxygen sensitive fluorescent dyes, 365



14

genetically encoded sensors, positron emission tomography (PET) and 18F nuclear 366

magnetic resonance (NMR) (Zhang et al., 2010; Dmitriev and Papkovsky, 2015; Fleming et 367

al., 2015). 368

Clark-type electrodes are based on the diffusion of oxygen through a membrane to the 369

oxygen-reducing cathode, which generates a current that is proportional to the oxygen 370

concentration (Clark et al., 1953). A disadvantage is that oxygen is consumed at the 371

cathode. For the measurements of oxygen in tissue, this drawback has been partially 372

overcome by the development of miniaturized microsensors which consume significantly 373

less oxygen. These sensors, for which commercially available models are available with a tip 374

diameter of 5-10 µm, are also significantly less invasive compared to larger models. Despite 375

the oxygen consumption and destructiveness of the Clark-type electrodes, they have been 376

widely used and have been employed to measure the oxygen concentration in numerous 377

plants such as rice, seagrass, green alga cultures and in the roots of several wetland plant 378

species (Melis et al., 2000; Visser et al., 2000; Binzer et al., 2005; Colmer and Pedersen, 379

2008). 380

Optical oxygen sensors are popular due to their wide possible applications and their lack of 381

oxygen consumption during the measurements. The majority of oxygen optodes are based 382

on the quenching of a luminescent probe by oxygen, called phosphorescence quenching, 383

resulting in increased phosphorescence when the oxygen concentration decreases. Oxygen 384

sensitive phosphorescent dyes can be coated on the inside of culture flasks or microplates 385

to measure the oxygen concentration in a sample over time. Another application includes the 386

creation of thin films coated with an oxygen sensitive fluorescent dye, which was 387

successfully used to map the oxygen concentration in plant roots (Rudolph et al., 2012). 388

Micro-optodes, which consist of an optical fiber with a tip coated by an oxygen sensitive 389

probe can be used to measure the oxygen concentration within plant tissue (Licausi et al., 390

2011a). However, insertion of micro-optodes into the tissue is destructive and facilitates 391

oxygen diffusion into the sample which can lead to faulty measurements. 392

Genetically encoded oxygen reporters provide a potential solution to overcome the drawback 393

associated with the invasiveness of Clark-type electrodes and micro-optode oxygen sensors 394

(Ast et al., 2012). Several genes have been identified which display specific and strong 395

upregulation upon low oxygen (Mustroph et al., 2010). The expression of these genes may 396

therefore be used as an indication of underlying hypoxic conditions. Activation of promoters 397

of hypoxia-inducible genes, including HYPOXIA RESPONSE ATTENUATOR 1 (HRA1), 398

PCO1 and PCO2 has been clearly demonstrated (Chung and Ferl, 1999; Giuntoli et al., 399

2014; Weits et al., 2014; Gasch et al., 2016). 400



15

401

Oxygen measurements in non-plant organisms 402

Oxygen sensitive phosphorescence probes are used to measure the intracellular oxygen 403

concentration in different animal tissues (Vikram et al., 2007). The probes are either directly 404

injected into the desired tissue or taken up by the tissue through passive self-loading 405

(Dmitriev and Papkovsky, 2015). Afterwards, the phosphorescence signal is imaged using a 406

fluorescent microscope to map the oxygen concentration. 407

Several parameters need to be examined before phosphorescent probes can be applied in 408

plants, e.g. sensitivity to pH, stability, toxicity and probe distribution. Systemic distribution is 409

another roadblock, as several dyes are injected intravenously in animals and rely on 410

transport via the cardiovascular system to the tissue. A red light–emitting iridium based 411

probe Ir(btp)2(acac) (BTP) was developed and used to image tumor hypoxia in vivo (Zhang 412

et al., 2010). The phosphorescence of the probe is quenched by oxygen, but when the 413

concentration drops below 5% v/v O2 the signal increases. However, cellular uptake of BTP 414

appears to be albumin-mediated, and its uptake into plant cells may therefore not occur 415

efficiently. Modification of these oxygen probes, such as the addition of hydrophilic groups or 416

domains which interact with transport proteins, may facilitate uptake by the cell. Importantly, 417

as chlorophyll displays red autofluorescence, phosphorescent oxygen probes for plants 418

should be chosen with distinct emission spectra. 419

For studying the oxygen concentration in bacteria, a genetically encoded fluorescent protein-420

based biosensor for oxygen (FluBO) was established (Potzkei et al., 2012). This FRET-421

based probe contains an oxygen sensitive yellow fluorescent protein (YFP) coupled with a 422

hypoxia insensitive flavin-binding fluorescent protein (FbFP). Maturation of the YFP 423

chromophore requires oxygen, and therefore FRET efficiency from the FbFP donor to the 424

YFP acceptor depends on the oxygen availability. Remarkably, the YFP/FbFP emission ratio 425

could be calibrated to the dissolved oxygen concentration in a range from 0 to 33%, allowing 426

a precise quantification of the intracellular oxygen concentration. 427

PET has been widely applied to image hypoxia within tumors in mammals. PET based 428

detection of oxygen is based on the imaging of 18F-containing imidazoles, which passively 429

diffuse in to cells and bind strongly to macromolecules of hypoxic cells (Fleming et al., 2015). 430

This can be combined with X-ray computed tomography to provide additional anatomical 431

information of the tissue, allowing precise mapping of the oxygen concentration within the 432

tissue (Krause et al., 2006). Another minimally invasive method to determine oxygen content 433

in mammalian tissues is 19F (NMR). This spectroscopic technique is based on the 434

measurement of the spin lattice relaxation rate of perfluorocarbons, which has a linear 435



16

relation to the tissue oxygen concentration. 19F NMR therefore allows imaging of the 436

absolute oxygen concentration in tissue (Yu et al., 2005). Imaging of the oxygen 437

concentration using PET or NMR is not limited by the thickness of the issue, and it therefore 438

represents an effective technique to map the oxygen concentration in a non-invasive manner 439

of thick or difficult to access tissue. PET and NMR-based oxygen measurements may also 440

prove useful for plants, however their use in mammals relies on the injection of probes in to 441

the blood stream, and their distribution in plant tissue must therefore be carefully tested. 442

443

Concluding remarks 444

Oxygen deprivation affects diverse organelles, which give rise to unique stress signals that 445

must be processed and integrated to initiate an appropriate adaptive response of the plant 446

cell. The diverse and widespread consequences of a drop in oxygen for cellular homeostasis 447

strongly support a view in which oxygen sensing does not occur through one primary sensor, 448

but happens decentralized and simultaneously at multiple sites in the cell (Figure 1). 449

At the transcriptional level, at least 120 transcription factors are differentially expressed upon 450

low-oxygen stress in Arabidopsis (Licausi et al., 2011b). Still, the roles for most of these 451

transcription factors, or the kind of signals they perceive upon low-oxygen stress, are 452

unknown. So far, it is unclear which signals activate ERFVIIs upon low-oxygen stress in 453

Arabidopsis. The non-N-end rule ERFVII target SUB1A of rice was shown to be a MPK 454

phosphorylation target, (Singh and Sinha, 2016), suggesting post-translational signal 455

integration. Interestingly, MPK3/6 activity in Arabidopsis is induced by a mitochondrial signal 456

upon oxygen deprivation (Chang et al., 2012). Also transcription factor targets of the SnRK1 457

kinase might play a crucial role in oxygen signalling (Baena-González et al., 2007). 458

Furthermore, mitochondrial- or ER-to-nucleus signalling was shown to rely on transcription 459

factors that need to be proteolytically activated (Iwata et al., 2008; De Clercq et al., 2013). 460

One of the main challenges in the future is to identify all transcription factors that act as 461

signal integration points during low-oxygen stress, to decipher the signals they perceive and 462

the mechanisms through which they act in a spatial and temporal manner. 463



17

To date, a number of retrograde signalling molecules have been described, including ROS, 464

calcium and diverse metabolites (Kmiecik et al., 2016). Still, it is hardly known how these 465

signals act during low-oxygen stress. That said, the oxidative burst observed in mitochondria 466

during oxygen deprivation was shown to activate MPKs (Chang et al., 2012). Potentially, 467

calcium and ROS might act in synergy to form an integrative signal, as observed during salt 468

stress (Evans et al., 2016). Organellar signalling does not only involve signalling to the 469

nucleus but also between organelles (Kleine and Leister, 2016). Here the question raises 470

whether low oxygen-induced signalling of one organelle can be prioritized over another. 471

Abiotic stresses in general impair energy metabolism and provoke mitochondrial 472

dysfunctioning, which cause the activation of SnRK and AOX. In addition, signalling 473

molecules like calcium and ROS are vital to sense all different kinds of stresses. Despite this 474

remarkable overlap in stress responses at the cellular and molecular level, cells can 475

differentiate between stresses and respond specifically. To be able to do so, plants might be 476

capable of reading stress signal signatures (i.e., ROS waves or calcium spikes) and sense 477

the temporal and spatial context. In yeast and human cell systems, it was shown that cellular 478

stress sensors act in scaffolds (Kang et al., 2004). In plants, the idea of signalling scaffolds 479

has only recently started to emerge (Demir et al., 2013,). Future research (see ‘Outstanding 480

questions’) should place emphasis on the multiple signalling pathways that are activated by 481

oxygen limitation, their downstream integration and cross-talk to reveal how the adaptation 482

to low oxygen stress is fine-tuned and adjusted to a particular situation encountered by 483

plants. This will also require the development of innovative methods to measure intracellular 484

molecular oxygen levels with a high spatial and temporal resolution. 485

486



18

Figure 1. Integration of multiple low-oxygen stress signalling pathways from diverse 487 cellular origins. According to this model, signalling to the nucleus occurs through various 488 different pathways. From left to right, low-oxygen stress results in an NADPH-oxidase 489 derived oxidative burst which eventually leads to post-translational activation of diverse 490 transcription factors (TFs). The influx of extracellular calcium stimulates a signalling cascade 491 involving CALCINEURIN-B-LIKE PROTEINs (CBLs) and CBL-INTERACTING PROTEIN 492 KINASEs (CIPKs) and the activation of NADPH oxidases, called RESPIRATORY BURST 493 OXIDASE HOMOLOGs (RBOHs). RBOHs are in addition stimulated to produce ROS by 494 interacting with RHO-LIKE SMALL G-PROTEINS OF PLANTS (ROP). The resulting ROS 495 burst is subsequently dampened through the action of ROP GTPase ACTIVATING 496 PROTEIN 4 (RopGAP4), which targets ROP, as well as by HYPOXIA-RESPONSIVE 497 UNIVERSAL STRESS PROTEIN 1 (HRU1), which forms a complex with ROP and RBOH. 498 Furthermore, oxygen limitation might hamper oxidative protein folding in the endoplasmic 499 reticulum (ER), through impairing the activity of ER THIOL OXIDASE (ERO), which 500 subsequently results in an unfolded protein response (UPR). In addition, low-oxygen stress 501 causes mitochondrial dysfunction, which is communicated to the ER via mitochondrial 502 retrograde regulation (MRR). Dormant NAC TFs at the ER are proteolytically released to 503 transduce the MRR signal to the nucleus. Further, impairment of the mitochondrial electron 504 transport chain (mETC) is followed by a mitochondrial oxidative burst and potentially an 505 efflux of stored calcium into the cytosol. The oxidative burst results in the activation of 506 MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) and MPK6, which may regulate 507 hypoxic gene expression by phosphorylation of transcriptional regulators. Disturbance of the 508 mETC further leads to a drop in ATP levels which is sensed by the kinases TARGET OF 509 RAPAMYCIN (TOR) and SUCROSE NONFERMENTING 1–RELATED KINASE 1 (SnRK1), 510 whereby TOR is inactivated while Snrk1 is induced under ATP limitation. Stabilization of 511 RELATED TO APETALA 2.12 (RAP2.12) and other subgroup VII ERF TFs occurs through 512 inactivation of the N-end rule pathway under hypoxic conditions. Under aerobic conditions, 513 this active degradation pathway involves oxygen-dependent oxidation of the TF proteins that 514 is catalysed by PLANT CYSTEINE OXIDASE (PCO). Additionally, RAP2.12 protein 515 abundance is increased by HYDRAULIC CONDUCTIVITY ROOT1 (HCR1), a Raf-like 516 MAPKKK which targets the TF under oxygen limiting and K+-sufficient conditions. Finally, 517 integration of the diverse subcellular signal inputs most likely occurs at the level of TFs, 518 which are potentially regulated by post-translational modification and induce transcriptional 519 reprogramming resulting in hypoxia adaptation. 520

521



19

522



ADVANCES

• Oxygen gradients and concomitant low-oxygen stress are recognized to occur commonly in plants.

• Oxygen limitation in plants was shown to create a compound stress that affects many essential cellular processes (such as the energy charge, cellular pH, redox status, ROS burst, and calcium spiking).

• Oxygen-concentration-dependent stabilization of transcription factors as described by the N-end rule was shown to be involved in the control of hypoxia tolerance responses in plants.

• Evidence accumulates that a multitude of oxygen-related signals from various sub-cellular compartments are integrated into the cellular response to improve tolerance to low-oxygen stress.

• Novel methods are arising that allow a more detailed mapping of oxygen gradients in tissues.



OUTSTANDING QUESTIONS

• Signals under hypoxia, e.g. calcium spikes and ROS burst, overlap with those induced by other stresses. What determines their specificity? How are these signals from different cellular compartments integrated to induce specific adaptive changes?

• Organelles must be able to communicate low oxygen stress. What is the signal identity? Which molecular players are involved? Is there organelle cross-talk?

• All different signals under hypoxia potentially converge at the transcript level. Which transcription factors act as integration points here?

• Flooding induces a combination of stresses, e.g. hypoxia and osmotic stress. Is any single stress pathway prioritized over another?



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http://www.ncbi.nlm.nih.gov/pubmed?term=De Clercq I%2C Vermeirssen V%2C Van Aken O%2C Vandepoele K%2C Murcha MW%2C Law SR%2C Inz� A%2C Ng S%2C Ivanova A%2C Rombaut D%2C van de Cotte B%2C Jaspers P%2C Van de Peer Y%2C Kangasj�rvi J%2C Whelan J%2C Van Breusegem F %282013%29 The membrane%2Dbound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis%2E Plant Cell 25%3A3472%2D90&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Dodd AN%2C Kudla J%2C Sanders D %282010%29 The language of calcium signaling%2E Annu Rev Plant Biol 61%3A593%2D620&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Dromparis P, Paulin R, Sutendra G, Qi AC, Bonnet S, Michelakis ED (2013) Uncoupling protein 2 deficiency mimics the effects of hypoxia and endoplasmic reticulum stress on mitochondria and triggers pseudohypoxic pulmonary vascular remodeling and pulmonary hypertension. Circ Res 113:126-36

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http://www.ncbi.nlm.nih.gov/pubmed?term=Edel KH%2C Marchadier E%2C Brownlee C%2C Kudla J%2C Hetherington AM %282017%29 The Evolution of Calcium%2DBased Signalling in Plants%2E Curr Biol 27%3AR667%2DR679&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Edel KH, Marchadier E, Brownlee C, Kudla J, Hetherington AM (2017) The Evolution of Calcium-Based Signalling in Plants. Curr Biol 27:R667-R679

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gonzali S%2C Loreti E%2C Cardarelli F%2C Novi G%2C Parlanti S%2C Pucciariello C%2C Bassolino L%2C Banti V%2C Licausi F%2C Perata P %282015%29 Universal stress protein HRU1 mediates ROS homeostasis under anoxia%2E Nat Plants 1%3A1515&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gross E%2C Sevier CS%2C Heldman N%2C Vitu E%2C Bentzur M%2C Kaiser CA%2C Thorpe C%2C Fass D %282006%29 Generating disulfides enzymatically%3A Reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p%2E Proc Natl Acad Sci U S A 103%3A 299%2D304&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Guzy RD%2C Mack MM%2C Schumacker PT %282007%29 Mitochondrial Complex III is required for hypoxia%2Dinduced ROS production and gene transcription in yeast%2E Antioxid Redox Signal 9%3A1317�??1328&dopt=abstract

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Schmidt R, Schippers JHM (2015) ROS-mediated redox signaling during cell differentiation in plants. Biochim Biophys Acta 1850:1497-508


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Suarez-Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-Activated Protein Kinase Signaling in Plants. Annu Rev Plant Biol 61:621–649


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van Dongen JT, Licausi F (2015) Oxygen sensing and signaling. Annu Rev Plant Biol 66:345-67Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Vikram DS, Zweier JL, Kuppusamy P (2007) Methods for Noninvasive Imaging of Tissue Hypoxia. Antioxid Redox Signal 9: 1745–1756Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitiousroots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant, Cell Environ 23: 1237–1245


Weits DA, Giuntoli B, Kosmacz M, Parlanti S, Hubberten H-M, Riegler H, Hoefgen R, Perata P, van Dongen JT, Licausi F (2014) Plantcysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun 5: 3425


White MD, Klecker M, Hopkinson RJ, Weits DA, Mueller C, Naumann C, O'Neill R, Wickens J, Yang J, Brooks-Bartlett JC, Garman EF,Grossmann TN, Dissmeyer N, Flashman E (2017) Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nat Commun. 8:14690


Wiel C, Lallet-Daher H, Gitenay D, Gras B, Le Calvé B, Augert A, Ferrand M, Prevarskaya N, Simonnet H, Vindrieux D, Bernard D (2014)Endoplasmic reticulum calcium release through ITPR2 channels leads to mitochondrial calcium accumulation and senescence. NatCommun 5:3792


Wouters BG, Koritzinsky M (2008) Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer8:851-64


Yemelyanov VV, Shishova MF, Chirkova TV, Lindberg SM (2011) Anoxia-induced elevation of cytosolic Ca2+ concentration depends ondifferent Ca2+ sources in rice and wheat protoplasts. Planta 234:271-80


Zhang S, Hosaka M, Yoshihara T, Negishi K, Iida Y, Tobita S, Takeuchi T (2010) Phosphorescent light-emitting iridium complexes serveas a hypoxia-sensing probe for tumor imaging in living animals. Cancer Res 70: 4490–4498


Zhu JK (2016) Abiotic Stress Signaling and Responses in Plants. Cell 167:313–324Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title


http://www.ncbi.nlm.nih.gov/pubmed?term=van Dongen JT%2C Gupta KJ%2C Ram�rez%2DAguilar SJ%2C Ara�jo WL%2C Nunes%2DNesi A%2C Fernie AR %282011%29 Regulation of respiration in plants%3A a role for alternative metabolic pathways%2E J Plant Physiol 168%3A1434%2D43&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Vikram DS%2C Zweier JL%2C Kuppusamy P %282007%29 Methods for Noninvasive Imaging of Tissue Hypoxia%2E Antioxid Redox Signal 9%3A 1745�??1756&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Vikram DS, Zweier JL, Kuppusamy P (2007) Methods for Noninvasive Imaging of Tissue Hypoxia. Antioxid Redox Signal 9: 1745?1756

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

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http://search.crossref.org/?page=1&rows=2&q=Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant, Cell Environ 23: 1237?1245

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http://scholar.google.com/scholar?as_q=Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

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http://www.ncbi.nlm.nih.gov/pubmed?term=Weits DA%2C Giuntoli B%2C Kosmacz M%2C Parlanti S%2C Hubberten H%2DM%2C Riegler H%2C Hoefgen R%2C Perata P%2C van Dongen JT%2C Licausi F %282014%29 Plant cysteine oxidases control the oxygen%2Ddependent branch of the N%2Dend%2Drule pathway%2E Nat Commun 5%3A 3425&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Weits DA, Giuntoli B, Kosmacz M, Parlanti S, Hubberten H-M, Riegler H, Hoefgen R, Perata P, van Dongen JT, Licausi F (2014) Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun 5: 3425

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http://www.ncbi.nlm.nih.gov/pubmed?term=White MD%2C Klecker M%2C Hopkinson RJ%2C Weits DA%2C Mueller C%2C Naumann C%2C O%27Neill R%2C Wickens J%2C Yang J%2C Brooks%2DBartlett JC%2C Garman EF%2C Grossmann TN%2C Dissmeyer N%2C Flashman E %282017%29 Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase%2Dcatalysed arginylation of N%2Dend rule targets%2E Nat Commun%2E 8%3A14690&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=White MD, Klecker M, Hopkinson RJ, Weits DA, Mueller C, Naumann C, O'Neill R, Wickens J, Yang J, Brooks-Bartlett JC, Garman EF, Grossmann TN, Dissmeyer N, Flashman E (2017) Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nat Commun. 8:14690

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http://www.ncbi.nlm.nih.gov/pubmed?term=Wiel C%2C Lallet%2DDaher H%2C Gitenay D%2C Gras B%2C Le Calv� B%2C Augert A%2C Ferrand M%2C Prevarskaya N%2C Simonnet H%2C Vindrieux D%2C Bernard D %282014%29 Endoplasmic reticulum calcium release through ITPR2 channels leads to mitochondrial calcium accumulation and senescence%2E Nat Commun 5%3A3792&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Wouters BG%2C Koritzinsky M %282008%29 Hypoxia signalling through mTOR and the unfolded protein response in cancer%2E Nat Rev Cancer 8%3A851%2D64&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Yemelyanov VV%2C Shishova MF%2C Chirkova TV%2C Lindberg SM %282011%29 Anoxia%2Dinduced elevation of cytosolic Ca2%2B concentration depends on different Ca2%2B sources in rice and wheat protoplasts%2E Planta 234%3A271%2D80&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Yemelyanov VV, Shishova MF, Chirkova TV, Lindberg SM (2011) Anoxia-induced elevation of cytosolic Ca2+ concentration depends on different Ca2+ sources in rice and wheat protoplasts. Planta 234:271-80

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhang S%2C Hosaka M%2C Yoshihara T%2C Negishi K%2C Iida Y%2C Tobita S%2C Takeuchi T %282010%29 Phosphorescent light%2Demitting iridium complexes serve as a hypoxia%2Dsensing probe for tumor imaging in living animals%2E Cancer Res 70%3A 4490�??4498&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu JK %282016%29 Abiotic Stress Signaling and Responses in Plants%2E Cell 167%3A313�??324&dopt=abstract

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Documents

Oxygen sensing and integrative stress signaling in plants132 retrograde signals in hypoxia has been partly investigated, for example mitochondrial ROS 133 signals were shown to impact