2 running title: flooding stress signaling 3 corresponding ... · 4 64. 65. abstract . 66. 67....

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1 Running title: Flooding stress signaling 2 3 Corresponding author: Rashmi Sasidharan 4

Address: Padualaan 8, 3584 CH, Utrecht, The Netherlands 5

Telephone number: +31 30 2536871 6

Email: [email protected] 7

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Plant Physiology Preview. Published on November 2, 2017, as DOI:10.1104/pp.17.01232

Copyright 2017 by the American Society of Plant Biologists

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Signal dynamics and interactions during flooding stress. 33 34 Rashmi Sasidharan1, Sjon Hartman1, Zeguang Liu1, Shanice Martopawiro1, Nikita 35 Sajeev1,2, Hans van Veen1, Elaine Yeung1, Laurentius A.C.J. Voesenek1 36 37 1Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, The 38

Netherlands 39

2Molecular Plant Physiology, Institute of Environmental Biology, Utrecht University, The 40

Netherlands 41

42 Summary (200 characters): Flooding triggers several internal changes in plant cells, 43

and interactions between these signals can provide critical information for 44

downstream beneficial gene expression, stress acclimation and survival. 45

46 R.S., S.H., Z.L., S.M., N.S., H.v.V., E.Y. and L.A.C.J.V. all contributed to the writing of the 47 manuscript. 48 49 50 51 52 53



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Footnotes 54 55 Financial sources: This work was supported by grants from the Netherlands 56

Organization for Scientific Research (NWO-ALW No. 822.01.007, NWO-Veni No. 57

863.12.013 and NWO-Crop Sciences grant 867.15.031 to R.S.; NWO-EPS grant 58

831.15.001 to SH; NWO-ALW 824.14.007 to SM, LACJV; a China Scholarship Council 59

grant to ZL) 60

61 Corresponding author: Rashmi Sasidharan ([email protected]) 62

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mailto:[email protected]


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64 Abstract 65

66

Flooding is detrimental for nearly all higher plants including crops. The compound 67

stress elicited by slow gas exchange and low light levels under water is responsible 68

for both a carbon and an energy crisis ultimately leading to plant death. The 69

endogenous concentrations of four gaseous compounds: oxygen, carbon dioxide, 70

ethylene and nitric oxide, change during submergence of plant organs in water. 71

These gases play a pivotal role in signal transduction cascades leading to adaptive 72

processes such as metabolic adjustments and anatomical features. Of these gases, 73

ethylene is seen as the most consistent, pervasive and reliable signal of early 74

flooding stress most likely in tight interaction with the other gases. The production 75

of reactive oxygen species (ROS) in plant cells during flooding and directly after 76

subsidence, during which the plant is confronted with high light and oxygen levels, is 77

characteristic for this abiotic stress. Low, well-controlled levels of ROS are essential 78

for adaptive signaling pathways, in interaction with the other gaseous flooding 79

signals. On the other hand, excessive uncontrolled bursts of ROS can be highly 80

damaging for plants. A fine-tuned balance is therefore important with a major role 81

for ROS production and scavenging. Our understanding of the temporal dynamics of 82

the four gases and ROS is basal, whereas it is likely that they form a signature 83

readout of prevailing flooding conditions and subsequent adaptive responses. 84

85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100



5

INTRODUCTION 101

102

Global flood risk under climate change has increased dramatically in recent decades 103

(Hirabayashi et al., 2013). In the last 50 years, increasingly frequent and severe 104

flooding events have negatively impacted terrestrial plant life. When flooded, gas 105

exchange is severely restricted between the plant and its environment causing 106

several internal changes in plants. Flooded plant organs can experience a shortage of 107

oxygen (O2) and/or carbon dioxide (CO2), and accumulate high levels of the volatile 108

hormone ethylene. In addition, there are changes in the concentration of O2 derived 109

free radicals, nitric oxide (NO) and reactive oxygen species (ROS) (Bailey-Serres and 110

Voesenek, 2008). The generation, dynamics, concentration and exact balance of 111

these substances in flooded cells depend on the plant organ and type of flooding. 112

We propose that these substances and their interaction during flooding provide 113

plants with a signature readout of prevailing flooded conditions, which elicits an 114

appropriate adaptive response. Here we outline current knowledge regarding the 115

generation, dynamics and interactions of these signals in flooded plants and their 116

influence on downstream responses affecting plant survival. 117

118 SIGNAL GENERATION 119

Tissue level variation in O2 and CO2 120

Light energy drives fixation of CO2 into carbohydrates via photosynthesis. These 121

carbohydrates are vital structural building blocks for plants, and are also respired to 122

generate energy, a process that requires sufficient O2 supply. Flooding-induced 123

reduction in O2 and CO2 hinders respiration and photosynthesis and imposes a 124

severe energy and carbohydrate deficit in submerged plants. O2 and CO2 dynamics 125

are the direct result of consumption, production and diffusive resistance and these 126

factors can vary considerably depending on organ and flooding type (Voesenek and 127

Sasidharan, 2013). 128

Light availability is determined by floodwater clarity and depth. Murky water can 129

almost completely block light reaching the plant surface (Vervuren et al., 2003), thus 130

hampering underwater photosynthesis. Furthermore, limited CO2 access would 131

severely reduce the rate of carbon capture and limit O2 release from the plant 132



6

(Mommer and Visser 2005). Studies have shown that in clear water, submerged 133

shoots do not have an O2 deficit (Mommer et al., 2007; Lee et al. 2011; Vashisht et 134

al., 2011; van Veen et al., 2013) and in some cases can even be hyperoxic (Pedersen 135

et al., 2016). Such high O2 levels combined with CO2 limitation most likely lead to 136

increased photorespiration and prevents any net carbon gain for the plant (Mommer 137

et al. 2005a, b). When plants are submerged in dark conditions, internal O2 levels 138

rapidly decline as a result of respiratory consumption and limited diffusion from the 139

environment. However, shoot internal O2 levels rarely decline to zero (Vashisht et 140

al., 2011, Winkel et al., 2013). Though gas diffusion is impaired, the leaf tissue is 141

surrounded by water that usually has close to ambient O2 levels. The flat leaf, 142

sometimes in combination with gas films then does allow some gas exchange 143

(Pedersen et al., 2009; Verboven et al., 2014). 144

Roots experience a completely different environment when submerged. Flooded 145

soils are rapidly depleted of O2, as water fills existing airspaces and respiring 146

microorganisms and roots consume available O2 leading to an anoxic environment. 147

Heterotrophic roots invariably will rapidly consume internal O2 and by virtue of their 148

cylindrical anatomy have less favorable environmental gas exchange (Greenway et 149

al. 2006). Arabidopsis roots were hypoxic even under well-drained conditions, but 150

when submerged became anoxic within 15 minutes (Vashisht et al., 2011). This was 151

alleviated by submerging in light conditions, indicating that even in Arabidopsis, 152

internal shoot to root O2 diffusion is important. This highlights the importance of 153

tissue porosity, tissue tortuosity and diffusion distance for root O2 supply (Colmer, 154

2003). CO2 from respiring roots and rhizosphere microorganisms can lead to a high 155

CO2 environment. This could possibly influence roots via an effect on intracellular pH 156

and some key metabolic enzymes (Greenway et al., 2006). 157

Oxygen sensing was recently shown to occur via proteolysis of group VII Ethylene 158

Response Factors (ERFVIIs). ERFVIIs are important transcriptional regulators of 159

hypoxia responses via control of hypoxia adaptive gene expression (Hinz et al., 2010; 160

Licausi et al., 2011; Gibbs et al., 2011; Gasch et al., 2015). Studies in Arabidopsis have 161

revealed that the presence of a characteristic N-terminal motif makes ERFVIIs direct 162

targets of the N-end rule pathway of proteolysis where, in the presence of both 163

ambient NO and O2 these proteins are ubiquitinated and degraded (Licausi, et al. 164



7

2011; Gibbs et al., 2011; Gibbs et al., 2014). When either the NO or O2 concentration 165

declines, ERFVIIs are no longer flagged for ubiquitination, accumulate and activate 166

downstream target genes, including those required for fermentation. 167

168 Starvation strongly influences flooding responses 169

During complete submergence plants experience a strong decline in energy and 170

carbon availability. This is due to reduced photosynthesis, either through a lack of 171

light or reduced rate of CO2 diffusion, and due to impaired respiration through 172

reduced oxygen availability. Plants can sense and integrate a variety of signals 173

relaying cellular energy and carbon status. This includes sucrose sensing via 174

trehalose metabolism (Schluepmann et al., 2003), glucose via Hexokinase1 (Moore 175

et al., 2003) and fructose via NAC089 (Li et all, 2011). These responses are tightly 176

balanced by the opposing actions of the conserved kinases sucrose-non-fermenting-177

1-related protein kinase-1 (SnRK1) during starvation and by target of rapamycin 178

(TOR) Kinase during energy abundance (Lastdrager et al., 2014; Baena-Gonzalez and 179

Hansson, 2017). These central regulators maintain energy homeostasis and stress 180

acclimation through major transcriptomic, translatomic and metabolic 181

reprogramming (Lastdrager et al., 2014). Low energy signaling is intricately 182

connected with plant hormone signaling pathways, especially ABA and ethylene 183

(Finkelstein and Gibson, 2002; Cho et al., 2010; Ljung et al., 2015). 184

Starvation leads to a downregulation of energetically expensive secondary metabolic 185

processes and protein translation, a crucial adaptation to prioritize energy 186

expenditure during flooding (Branco-Price et al., 2008; Edwards et al., 2012; 187

Sorenson and Bailey Serres, 2014). Arabidopsis plants experiencing starvation in 188

darkness had a highly similar transcriptomic response as those under submerged 189

conditions (van Veen et al. 2016; Lee et al. 2011). This indicates that low energy 190

signaling occurs via a generic signaling mechanism regardless of the origin of the 191

starvation stress. 192

However, the regulatory action of the low energy sensing machinery might not 193

always be beneficial during flooding. For instance, some rice accessions can 194

germinate under anoxic conditions, but require a large amount of readily available 195

sugars to do so (Magneschi and Perata, 2008; Loreti et al. 2016). One way these 196



8

sugars are perceived is by trehalose-6-phosphate (T6P) levels, which directly reflects 197

sucrose availability (Yadav et al. 2014). However, in rice high T6P levels prevent 198

starch degradation via inhibition of SnRK1 activity, an undesirable process during 199

germination. This is avoided by T6P degradation via the induction of a T6P 200

phosphatase in varieties that harbor a specific T6P phosphatase gene (OsTPP7). 201

Active T6P removal reduces the sensitivity of rice blind to its available sugar levels 202

and facilitates starch mobilization to create a strong flux of sugars that fuels 203

anaerobic germination (Kretzschmar et al., 2015). Energy levels during anoxic 204

establishment of plants can thus be surprisingly high (Ishizawa et al., 1999). and The 205

regulation of energy signaling, e.g. trehalose metabolism, components occurs during 206

flooding in several species and tissues (Jung et al., 2010, van Veen et al., 2013; 207

Kretzschmar et al., 2015; Akman et al., 2017) suggesting that adjusting sensitivity to 208

sugar and energy signaling could be an essential part of regulating flooding 209

responses. 210

211 212 Ethylene invariably accumulates to high concentrations 213

All plant cells, except those of a few aquatic plant species with a permanently 214

submerged life style (Voesenek et al., 2015), are capable of synthesizing ethylene 215

and endogenous levels are determined by production rates and loss via diffusion to 216

the atmosphere. Ethylene biosynthesis starts with the conversion of the amino acid 217

methionine to S-Adenosyl-L-Methionine (SAM) by SAM synthetase. The enzyme 1-218

aminocyclopropane-1-carboxylic acid (ACC) synthase then catalyzes the production 219

of ACC from SAM followed by its oxidation to ethylene by ACC oxidase in a reaction 220

requiring O2. Both ACC synthase (ACS) and ACC oxidase (ACO) belong to large 221

multigene families and are regulated by various external and internal cues to control 222

ethylene production. In cells of flooded cells organs, endogenous ethylene levels 223

rapidly increase mainly due to hampered diffusion to the surrounding water. 224

Ethylene accumulates to high physiologically saturating levels in several plant species 225

in flooded shoots and roots (Voesenek and Sasidharan, 2013). Ethylene can reach 226

levels that are 20 fold (1 µlL-1) higher than non-submerged tissue within 1 hour 227

(Figure 1). Upon soil flooding, root ethylene levels were variable across species 228



9

determined by production rates and diffusion capacity. Wetland species possessing 229

aerenchymatous tissue could vent entrapped ethylene and had lower accumulated 230

ethylene in flooded roots (Visser and Pierik, 2007). An overview of ethylene 231

concentrations in various plant species and organs upon flooding can be found in 232

Voesenek and Sasidharan (2013). Ethylene accumulation is not known to be affected 233

directly by changes in light levels during flooding. Thus unlike O2 and CO2 levels that 234

can be highly variable and influenced by several factors, high ethylene 235

concentrations are the most consistent, pervasive and reliable signal conveying early 236

flooding (Voesenek and Sasidharan, 2013; Sasidharan et al., 2015). Since ACC 237

conversion to ethylene requires O2, ethylene production cannot occur under true 238

anoxic conditions and it is therefore not a signal in these extreme situations. 239

240

Nitric oxide metabolism 241

Nitric oxide (NO) is a short-lived, highly reactive molecule regulating several plant 242

developmental and stress responses (Astier et al., 2011; Manjunatha et al., 2012; 243

Farnese et al., 2016). Plants regulate endogenous NO levels via control of 244

biosynthesis and scavenging. The regulation of NO biosynthesis in plants is poorly 245

understood. Several studies suggest that the main source of NO production is via 246

enzymatic and non-enzymatic reduction of nitrite (NO2-) (Planchet et al., 2005; Mur 247

et al, 2013; reviewed in Chamizo-Ampudia et al., 2017). Nitrite production is highly 248

dependent on nitrate reductase (NR) activity. The dependency of NO production on 249

nitrite availability, makes NR the major player in NO production (Magalhaes et al., 250

2000; Gupta and Kaiser, 2010; Gupta et al., 2011; Chamizo-Ampudia et al. 2017) 251

Removal of synthesized NO can occur via multiple reactions. NO can react chemically 252

with O2 to produce NO2- and NO3

- or with ROS to form additional Reactive Nitrogen 253

Species (RNS) (Delledone et al., 2001; Chamizo-Ampudia et al., 2017). NO can be 254

scavenged by glutathione (GSH) to produce S-nitrosylated glutathione (GSNO) 255

(Wilson et al., 2008; Frungillo et al., 2014). Finally, phytoglobins (previously called 256

Class I non-symbiotic hemoglobins) (Voesenek et al., 2016) use O2 to dioxygenate NO 257

in the plant cell to form nitrate (Hebelstrup et al., 2006 & 2012; Hill, 2012). 258

There is limited and contrasting data regarding temporal and spatial NO dynamics in 259

flooded plants. In Arabidopsis and cotton, NO emissions declined in the aerial plant 260



10

tissues, while emissions increased in three waterlogged deciduous tree species 261

(Magalhaes et al., 2000; Copolovici and Uiinemets, 2010; Zhang et al., 2017). 262

However, NO dynamics under hypoxia have been studied more extensively. Both 263

cellular and exogenous NO levels increased in various plant species during hypoxia 264

(Planchet et al., 2005; Mugnai et al., 2012; Gupta and Igamberdiev, 2016). This NO 265

burst during hypoxia is thought to result from enhanced NR activity and nitrite 266

accumulation providing a substrate for NO production (Planchet et al., 2005; Mugnai 267

et al., 2012; Gupta and Igamberdiev, 2016). In roots, NO bursts could be specific to 268

the transition and division zone and dependent on hypoxia sensing in the root apex 269

(Mugnai et al., 2012) (Figure 1). Post-translational modification of NR via 270

phosphorylation effectively inactivated NO synthesis in tobacco (Lea et al., 2004), 271

and this phosphorylation may be impaired under hypoxic conditions leading to 272

higher NR activity. NR activity is also lowered under reduced light conditions (Nemie-273

Feyissa et al., 2013), with potential implications for NR activity during submergence 274

in turbid waters. In conclusion, the temporal and spatial dynamics of NO, and 275

therefore its effects, are likely dependent on the conditions of flooding. 276

277

ROS metabolism 278

ROS are highly reactive, chemical species formed by the stepwise reduction of 279

molecular O2. ROS include superoxide (O2.-), singlet oxygen (1O2), hydrogen peroxide 280

(H2O2) and the hydroxyl radical (OH.) (Demidchik, 2015; Mittler, 2017). ROS are by-281

products of various metabolic pathways and are produced enzymatically or non-282

enzymatically. Non-enzymatic ROS production can occur in chloroplasts and 283

mitochondria via electron transport chains (ETC). In both organelles, the occasional 284

leakage of electrons to O2 during electron transport can result in the partial 285

reduction of O2 generating O2.- which subsequently give rise to other more reactive 286

ROS (Møller, 2001; Asada, 2006). Enzymatic ROS production can occur at several 287

sites within the cell including peroxisomes, cell walls, plasma membrane and 288

apoplast (Mignolet-Spruyt et al., 2016). Peroxisomes are the site of several oxidative 289

metabolic processes that can generate ROS, such as β-oxidation of fatty acids and 290

photorespiration (del Río and López-Huertas, 2016). In the peroxisome, O2.- is 291

formed by xanthine oxidase (Bolwell and Wojtaszek, 1997), whilst glycolate oxidase 292



11

catalyzes H2O2 generation (del Río and López-Huertas, 2016). Another enzymatic ROS 293

source is plasma membrane bound NADPH oxidases, or respiratory burst oxidase 294

homologs (RBOHs). RBOHs reduce extracellular O2 to O2.- using cytosolic NADPH 295

(Møller, 2001). Plants counter excessive ROS production with an efficient scavenging 296

machinery. This consists of ROS scavenging enzymes like superoxide dismutase 297

(SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX) and 298

antioxidant molecules like glutathione, ascorbic acid and α-tocopherol (Mittler et al., 299

2004; Steffens et al., 2013). 300

Considering that ROS originate from O2, it is expected that under flooding-induced 301

hypoxic conditions, ROS production is also restricted. However, several studies 302

report increased ROS accumulation under hypoxia/anoxia (Figure 1) (Pucciariello et 303

al., 2012; Chang et al., 2012; Paradiso et al., 2016). Under O2 deprivation, ROS 304

production likely still occurs in the mitochondria, chloroplasts and peroxisomes. 305

Anoxia inhibits the mitochondrial ETC resulting in the formation of mitochondrial 306

ROS (Chang et al., 2012), and chloroplastic ROS generation might occur via a similar 307

process. ROS could also be formed by peroxisomes during flooding in light. When 308

terrestrial plants photosynthesize underwater, photorespiration rates can increase 309

(Mommer and Visser, 2005). Photorespiration is one route via which peroxisomal 310

H2O2 production can be boosted (del Río and López-Huertas, 2016). Furthermore, 311

the antioxidant system can be negatively affected by hypoxia (Lasanthi-Kudahettige 312

et al., 2007), disrupting the tightly regulated balance between scavenging and 313

production. During flooding and hypoxia, ROS is also produced in a regulated 314

manner via RBOHs. In Arabidopsis, RBOHD is specifically upregulated during flooding 315

and hypoxia and is one of the core hypoxia genes (Mustroph et al., 2009; Pucciariello 316

et al., 2012; Yao et al., 2017). ROS signaling via regulated ROS production is 317

considered an important component of hypoxia signaling and adaptive responses to 318

flooding (Steffens et al., 2012; Pucciariello et al. 2012; Yamauchi et al., 2013; Gonzali 319

et al, 2015; Yamauchi et al., 2017). 320

321 SIGNAL INTERACTIONS 322

Ethylene and hypoxia signaling interact with NO 323



12

The interplay between ethylene and NO has often been described but has rarely 324

been mechanistically investigated. However, chemical or genetic impairment of one 325

of these pathways often affects the other and impacts plant responses (Asgher et al., 326

2016; Magalhaes et al., 2000; Manjunatha et al., 2012). Like ethylene, NO could also 327

accumulate to higher concentrations in flooded tissues due to restricted gas 328

diffusion. However, since NO is highly reactive and short-lived, accumulation is likely 329

limited without the additional hypoxic NO burst described earlier. Accordingly, 330

waterlogged Arabidopsis and cotton plants showed elevated ethylene emission and 331

signaling, respectively, but declining NO emission from aerial tissues (Magalhaes et 332

al., 2000; Zhang et al., 2017). In addition, exogenous NO application increased 333

ethylene production in various plants species, possibly via enhanced ACO activity 334

(Magalhaes et al., 2000; Manac’h-Little et al., 2005). On the other hand, NO levels 335

declined in ethylene-deficient or constitutive mutants (Magalhaes et al., 2000; Liu et 336

al., 2017). Thus both gases may affect each other under the conditions that vary over 337

the course of a flooding event. 338

The NO scavenging phytoglobins could potentially facilitate crosstalk between NO 339

and ethylene. However, conclusive mechanistic evidence is lacking. Phytoglobin 340

mRNA levels increased under waterlogging and hypoxic conditions in multiple plant 341

species (Hebelstrup et al., 2012; van Veen et al., 2013; Mira et al., 2016). Phytoglobin 342

silencing in Arabidopsis and maize, increased ethylene and NO emissions, and 343

upregulated ethylene biosynthesis and signaling genes (Hebelstrup et al., 2012; Mira 344

et al., 2016). Interestingly, NO also enhanced phytoglobin mRNA abundance in rice, 345

cotton and spinach (Ohwaki et al., 2005; Qu et al., 2006; Bai et al., 2016) hinting at a 346

feedback mechanism. In the wetland species Rumex palustris, phytoglobin transcript 347

levels increased following a short ethylene treatment and could potentially reduce 348

NO in these tissues (van Veen et al., 2013). Taken together, phytoglobins modulate 349

NO and ethylene levels, while these gases in turn also affect phytoglobin abundance. 350

Crosstalk and feedback loops between NO and ethylene may also occur at 351

the level of ERFVIIs. ERFVII stability and action strongly depend on NO and O2 levels 352

(Licausi, et al. 2011; Gibbs et al., 2011; Gibbs et al., 2014). When either the NO or O2 353

concentration declines, ERFVIIs accumulate and facilitate downstream target gene 354

transcription. Interestingly, ERFVII regulated genes that contain the hypoxia-355



13

responsive promoter element include multiple ethylene signaling genes and the NO 356

scavenging phytoglobin, HEMOGLOBIN1 (HB1) (Gasch et al., 2015). In addition, 357

expression of several ERFVIIs is also regulated by ethylene (Chang et al., 2013). In 358

conclusion, ERFVII abundance is regulated by NO, O2 and possibly ethylene, while 359

ERFVII action in turn can induce positive feedback loops for ethylene biosynthesis 360

and NO scavenging (Gasch et al., 2015). 361

362

The functional role of NO 363

While exact NO dynamics in flooded plants remain vague, it is clear that an NO 364

upsurge during hypoxia has functional implications for survival (Mugnai et al., 2012; 365

Gupta and Igamberdiev, 2016; Mira et al., 2016). For instance, chemically blocking 366

the hypoxia-induced NO burst at the onset of hypoxia strongly impaired hypoxia 367

survival in maize root tips (Mugnai et al., 2012). In addition to its role in regulating 368

ERFVII abundance, NO may also exert a regulatory role during flooding or hypoxia, by 369

post-translational modification (PTM) of proteins via S- or metal-nitrosylation and 370

tyrosine (Tyr) nitration (Reviewed by Astier et al., 2011; León et al., 2016). 371

Exogenous NO application in Arabidopis effectively S-nitrosylated proteins involved 372

in respiration, metabolism, signaling and stress responses (Lindermair et al., 2005; 373

Astier et al., 2011; León et al., 2016). S-nitrosylated proteins potentially involved in 374

flooding signaling and adaptation include ERFVIIs, cytochrome c oxidase (COX), 375

aconitase, phytoglobins and the H2O2 scavenger APX1 (Millar et al., 1996; Perazzolli 376

et al., 2004; Gupta et al., 2012; Gibbs et al., 2014; Begara-Morales et al., 2016). 377

Indeed, some reports indicate that an NO burst may inhibit COX activity (Millar et al., 378

1996; Brown, 2001). On the other hand, S-nitrosylation and therefore inhibition of 379

aconitase leads to enhanced alternative oxidase (AOX) activity under hypoxia in 380

Arabidopsis (Gupta et al., 2012). This altered bioactivity of COX and AOX by NO 381

suggests a role in tight regulation of respiration and O2 consumption in plant 382

mitochondria during hypoxia. 383

Phytoglobins mediate NAD(P)+ regeneration under hypoxia via the so-called 384

phytoglobin/NO cycle (Perazzolli et al., 2004; Igamberdiev et al., 2005; Gupta and 385

Igamberdiev, 2016). In the absence of O2, plant mitochondria can keep the electron 386

transport functional using nitrite as the electron acceptor (Gupta et al., 2005; Gupta 387



14

and Igamberdiev, 2011). This nitrite reduction to NO in the ETC recycles NAD(P)H to 388

NAD(P)+ and leads to some ATP production. This process in addition to the ATP 389

generated by fermentation retains the energy status of cells as long as sugar 390

availability is sufficient. The produced NO can be scavenged by phytoglobins via S-391

nitrosylation and this is thought to contribute to regeneration of NAD(P)+ and 392

nitrate, in turn fueling glycolysis and ATP production. The observed induction of 393

phytoglobin transcripts by ethylene might enhance this process in some plant 394

species when submerged (van Veen et al., 2013). Finally, the importance of 395

phytoglobins for hypoxia acclimation is highlighted in various studies. Phytoglobin-396

impaired mutants showed reduced hypoxia tolerance, while over-expression 397

enhanced tolerance in multiple plant species (Dordas et al., 2003; Mira et al., 2016). 398

In conclusion, the phytoglobin/NO cycle shows a crucial strategy of adaptation 399

leading to a retained energy status under hypoxia. 400

401

ROS-mediated hypoxia acclimation 402

ROS production and signaling during hypoxia is considered essential for stress 403

acclimation. In hypoxic Arabidopsis seedlings, RBOHD mRNA levels are strongly 404

upregulated (Pucciariello et al., 2012; Yang and Hong, 2015). Elevated H2O2 levels in 405

Arabidopsis seedlings shortly after the imposition of anoxia (Baxter-Burrell et al., 406

2002; Pucciariello et al., 2012), is linked to RBOH-mediated electron flow from 407

NADPH to O2 resulting ultimately in H2O2 generation. Accordingly, this hypoxic H2O2 408

increase is absent and survival compromised in rbohD seedlings or upon chemical 409

inhibition of RBOH activity. RBOH activity and therefore H2O2 production during O2 410

deprivation is regulated by the activity of at least two other hypoxia-inducible 411

proteins: HYPOXIA RESPONSIVE UNIVERSAL STRESS PROTEIN 1 (HRU1) and RHO (Ras 412

homologous)-RELATED PROTEIN FROM PLANTS 2 (ROP2) (Baxter- Burrel et al., 2002; 413

Gonzali et al., 2015). 414

Hypoxic conditions convert ROP2 to its active form GTP-ROP2 and activate RBOH-415

mediated H2O2 production. The subsequent ROS burst triggers the expression of 416

downstream beneficial targets including fermentation genes (eg. ALCOHOL 417

DEHYDROGENASE (ADH)) required for hypoxia acclimation. However, ROP2-triggered 418

H2O2 signaling also upregulates ROP guanosine triphosphatase (GTPase) activating 419



15

protein 4 (ROPGAP4), a negative regulator of ROP2. ROPGAP4-mediated inactivation 420

of ROP2 consequently dampens RBOHD-mediated ROS production. In ropgap4 421

mutants or in lines expressing a constitutively active form of ROP2, ADH expression 422

and activity was increased but tolerance was reduced (Baxter-Burrel et al., 2002). 423

Thus negative feedback inhibition of ROP2 and tight regulation of ROS production 424

plays a role in preventing oxidative stress and improving hypoxia tolerance. 425

Another hypoxia-inducible gene and ERFVII target regulating RBOH-mediated ROS 426

production is HRU1. HRU1 interacts with ROP2-GTP and RBOHD both in vitro and in 427

vivo, and hru1 mutants lack the hypoxic H2O2 burst observed in wild-type 428

Arabidopsis seedlings. HRU1 can exist as cytosolic HRU1-HRU1 dimers or monomers 429

that can take another interacting protein partner. The balance between these 430

dimers and monomers is essential for the control of ROS production. A shift in 431

balance towards HRU1 monomers might be favored during hypoxia, because under 432

these conditions HRU1 translocation to the plasma membrane was observed. Here it 433

may form a HRU1–ROP2–RBOHD complex and influence ROS production (Gonzali et 434

al., 2015). Together these findings indicate that apoplastic ROS production is a tightly 435

regulated process involving multiple protein interactions and is essential for hypoxia 436

acclimation and survival. 437

438

Functional ROS-ethylene interactions 439

Plants growing in flooded environments use morphological adaptations to improve 440

internal aeration and avoid flooding-induced hypoxia. These traits include formation 441

of gas filled voids or aerenchyma in existing root/shoots or shoot-borne, 442

aerenchyma-rich adventitious roots. Aerenchyma either constitutive or induced, 443

improves gas diffusion between flooded and non-flooded plant parts and permit 444

aerobic respiration to continue in affected organs (Voesenek and Bailey-Serres, 445

2015). Several studies have revealed that interactions between ROS and ethylene 446

signaling regulate lysigenious (formed by regulated cortical cell death) aerenchyma 447

development and adventitious roots (Yamauchi et al., 2013; Yamauchi et al., 2017; 448

Steffens et al., 2012). 449

Ethylene-induced formation of lysigenous aerenchyma under O2-deprived 450

conditions, via control of ROS production has been demonstrated in species such as 451



16

rice, wheat and maize (Yamauchi et al., 2013; Takahashi et al., 2015; Yamauchi et al., 452

2017). Stem aerenchyma in deepwater rice internodes required ethylene-mediated 453

ROS accumulation to induce parenchymal cell death (Steffens et al., 2012). In rice 454

adventitious roots, stagnant flooding increased ethylene levels due to a combination 455

of restricted diffusion and enhanced biosynthesis. This increased transcript 456

abundance and subsequently activity of RBOHH. Interestingly, the strongest RBOHH 457

expression was in the root cortical cells and corresponded with ROS accumulation 458

and programmed cell death (PCD) only in these cells. Accordingly, in adventitious 459

roots of CRISPR/Cas9 RBOHH knockouts, H2O2 and aerenchyma were significantly 460

reduced under stagnant conditions (Yamauchi et al., 2017). Considering that 461

ethylene accumulates in all cells, the question arises as to how cellular specificity is 462

achieved for ROS generation and subsequent cell death. The answer might lie in the 463

distinct characteristics (thinner cell walls, higher ROS, low starch) and higher 464

ethylene sensitivity of pre-aerenchymatous cells (Justin and Armstrong, 1991; Visser 465

and Bögemann, 2006; Steffens et al., 2012). In situ staining of stagnant rice roots 466

showed O2.- accumulation and a radial expansion of collapsed cells starting from the 467

mid-cortical cells and spreading to the neighbouring cells within the cortex. RBOHH 468

mediated O2.- could be the signal propagating cellular collapse to adjacent cells 469

(Yamauchi et al., 2017). Such a systemic signaling role has been demonstrated in 470

Arabidopsis where RBOHD-generated H2O2 stimulated RBOHD activity in adjacent 471

cells resulting in an auto propagating wave of ROS production (Miller et al. 2009; 472

Mittler et al., 2011). Whether such a systemic signal transmission occurs during 473

aerenchyma formation is yet to be confirmed. 474

Interactions between ethylene and ROS signaling also regulates adventitious root 475

growth and emergence in rice. Preceding adventitious root emergence, the 476

epidermal cells overlying adventitious root primordia have to die (Steffens et al., 477

2012). Ethylene stimulates this epidermal cell death by promoting RBOH-mediated 478

H2O2 accumulation. In epidermal cells that undergo PCD, ethylene also reduced 479

expression of Metallothionein2b (MT2b), a ROS scavenger (Steffens et al., 2012). 480

Accordingly, enhanced constitutive epidermal cell death was observed in MT2b 481

knockdown mutants, which also had high H2O2 levels. Ethylene and ROS signaling 482

also mediate adventitious root growth regulation. Ethylene-induced adventitious 483



17

root growth clearly requires ROS, since chemical manipulation of ROS levels clearly 484

affected adventitious root formation. However, this was highly specific to the nature 485

of ROS perturbation. For example, chemical inhibition of CAT and RBOH activity 486

clearly restricted ethylene-induced adventitious root growth. In contrast, 487

adventitious root growth was unaffected in MT2b knockdown lines with enhanced 488

H2O2 (Steffens et al., 2012). Adventitious root growth and emergence needs to be 489

precisely coordinated with epidermal cell death to protect the emerging root 490

primordium. This requires accurate signaling of the location where cell death should 491

occur. Ethylene and ROS alone could elicit local epidermal cell death only when a 492

mechanical stimulus (the physical pressure of the emerging root) was also present. 493

According to the current hypothesis, adventitious root formation requires ethylene-494

mediated ROS production in both the adventitious root primordium and the 495

overlying epidermal cells. ROS accumulation in the adventitious root primordium 496

promotes growth. The growing root exerts a mechanical force on specific epidermal 497

cells above it, whereby mechanical signaling and ethylene-induced ROS signaling 498

together trigger PCD (Steffens et al., 2012). 499

500

SIGNAL GENERATION AND INTERACTION UPON RE-AERATION 501

When floodwaters subside, submergence-mediated damage is further compounded. 502

Plants are re-exposed to higher O2 concentrations and increased light intensity, 503

resulting in further oxidative stress through a burst of ROS production (Fukao et al., 504

2011; Luo et al., 2012; Alpuerto et al., 2016) (Figure 1). Post-submergence ROS 505

damage is parallel to oxidative damage during hypoxic conditions, in which ROS 506

disrupts the photosynthetic apparatus (Luo et al., 2011; Panda and Sarkar, 2012; 507

Alpuerto et al., 2016) and consequently hinders photosynthetic recovery and 508

replenishment of carbohydrate reserves (Bhowmick et al., 2014; Gautam et al., 509

2017). During re-oxygenation and re-illumination, ROS and photo-inhibition can 510

further trigger desiccation stress (Setter et al., 2010), leaf senescence (Gautam et al., 511

2016; Liu and Jiang, 2016) and cell death (Tamang et al., 2014). Upon re-512

oxygenation, ROS accumulation likely occurs due to a combination of reduced 513

scavenging capacity and increased ROS production (Rhoads et al., 2006; Blokhina and 514

Fagerstedt, 2010; Shapiguzov et al., 2012). Excessive ROS accumulation is associated 515



18

with high-energy demands of reactivated mitochondrial and photosynthetic 516

metabolism due to re-oxygenation and re-illumination, causing electron leakage in 517

ETCs and proton leakage in mitochondrial matrixes (Elstner and Osswald, 1994; 518

Smirnoff, 1995; Roach et al., 2015). Excess O2 reacting with ROS-related byproducts 519

produced during hypoxic conditions can also trigger additional ROS formation. 520

While ethylene is well established as a signal triggering adaptive responses during 521

flooding, less is known on its role during flooding recovery. Several studies have 522

reported increased ethylene biosynthesis and enhanced ACS and ACO expression in 523

plants upon re-oxygenation (Khan et al., 1987; Voesenek et al., 2003; García et al., 524

2014; Tsai et al., 2014; Ravanbakhsh et al., 2017). Anoxia limits ethylene 525

biosynthesis, since ACO requires O2 for ACC conversion to ethylene (Yang and 526

Hoffman 1984). However, re-oxygenation may trigger increased ethylene 527

biosynthesis, promoted by elevated levels of the rate-limiting ACC enzymes. The role 528

of ethylene during re-oxygenation could be distinct from its regulatory roles during 529

flooding and hypoxia (Fukao et al., 2011; Tsai et al., 2014; Tsai et al., 2016). In 530

Rumex, ethylene accumulation upon de-submergence correlated with increased ACC 531

levels and its conversion to ethylene by increased ACO activity (Voesenek et al., 532

2003). This rapid induction of ethylene synthesis upon de-submergence promoted 533

shoot elongation as a strategy to avoid complete submergence later (Voesenek et al., 534

2003). In addition, shoot elongation rates in R. palustris upon de-submergence was 535

dependent on submergence duration, suggesting that time taken for ACC 536

accumulation could be the rate-limiting determinant (Voesenek et al., 2003). Thus 537

the basal level of ACC biosynthesis could be critical for post-submergence ethylene 538

responses. 539

In Arabidopsis seedlings, ethylene signaling was important for limiting post-anoxic 540

injury (Tsai et al., 2014). Ethylene response transcription factor 1 (ERF1), a marker of 541

the ethylene transduction pathway, together with ERF2 were induced during re-542

oxygenation. Moreover, two ethylene-insensitive mutants, ein2-5 and ein3eil1, 543

displayed increased chlorosis and cell damage upon re-oxygenation compared to the 544

wild type. Genes encoding heat shock factors (HSF), heat shock proteins (HSP) and 545

antioxidants were significantly enriched, implying the potential challenges caused by 546



19

re-oxygenation. The activation of ROS amelioration genes suggests that ethylene 547

could be important in eliminating ROS produced upon re-aeration. However, 548

ethylene accumulation under submergence negatively affected antioxidant levels 549

upon de-submergence in intolerant rice cultivars (Kawano et al., 2002). This again 550

suggests that regulatory roles of ethylene during hypoxia and re-oxygenation could 551

be different. In addition, comparison of the transcriptome wild type and ethylene-552

insensitive Arabidopsis mutants also suggested that ethylene might be involved in 553

regulating distinct pathways upon re-oxygenation such as jasmonate signaling, 554

feedback inhibiting its own production, and suppressing dehydration via inhibition of 555

ABA signaling (Tsai et al., 2014). 556

557

CONCLUSIONS 558

The energy and carbon crisis in flooded plants poses the largest threat to survival. 559

Sometimes starvation is ameliorated through increasing gas exchange via 560

aerenchyma and adventitious root development. However, a large majority of 561

flooding responses, such as reduced protein synthesis and down regulation of 562

secondary metabolism, most likely are coordinated via elaborate sugar sensing 563

mechanisms. Though energy signaling is essential to plant survival, by itself it is not 564

specific enough to reliably perceive flooding. However, a plant can utilize a variety of 565

other cues to precisely gauge a flooding event. 566

Changes in the gases ethylene, O2 and CO2 do not necessarily mean plants use them 567

for initiating adaptive responses. Ethylene is well established as an important signal 568

triggering several flood-adaptive traits (e.g. adventitious root and escape 569

growth)(Sasidharan & Voesenek, 2015). Rapid ethylene accumulation regardless of 570

the flooded conditions makes it a reliable signal in contrast with O2 levels that are 571

highly variable. For long it was unclear if O2 sensing occurred through direct 572

mechanisms or through an indirect effect of O2 on metabolism. It is now evident that 573

plants sense O2 through the O2-dependent degradation of ERF-VIIs (Licausi et al., 574

2011; Gibbs et al., 2011). Changes in CO2 could potentially also act as a flooding 575

signal. However, though several possible roles have been suggested (Greenway et 576



20

al., 2006), currently, there is no evidence for a significant function in plant flooding 577

responses (Voesenek et al., 1997; Colmer et al., 2006). 578

Plants have relatively little control over these signals, which for a large part result 579

directly from the restriction of gas diffusion underwater. However, adaptive 580

downregulation of O2 consumption rate has been suggested (Zabalza et al. 2009) In 581

this sense ROS production during flooding is similar since it also occurs in an 582

unregulated process, mainly at the ETCs and peroxisomes. However, regulated ROS 583

production via the RBOHs also occurs and is essential for hypoxia acclimation and 584

survival (Loreti et al., 2016). In aerenchyma and adventitious root formation, a 585

certain background level of unregulated ROS, together with ethylene regulated 586

scavenging is required to induce cell death in specific cells (Steffens and Rasmussen, 587

2016). Taken together, rather than a cue to gauge flooding, ROS is a signaling 588

intermediate in hypoxia sensing and ethylene regulated root development. 589

NO dynamics during flooding remain unclear. However, an NO burst does occur 590

upon hypoxia, linked to hypoxia-induced NR activity. This could make NO, unlike 591

ROS, a possible signal to assess the flood event. However, NO is strongly regulated 592

by phytoglobin, which is under both ERF-VII and ethylene control (Figure 2). NO thus 593

also assumes the role of a signaling intermediate. 594

Although ethylene invariably accumulates upon flooding, a plant needs hypoxia 595

sensing to activate fermentation pathways. That this metabolic adaptation is linked 596

to O2-sensing ERF-VIIs makes sense, as it prevents fermentation in shoots submerged 597

under light conditions where not aerobic respiration, but photosynthesis is impaired. 598

Interestingly, O2 availability seems of little importance in aerenchyma formation or 599

adventitious root development (Figure 2). Given that even under drained soil 600

conditions roots experience hypoxia, could mean that O2 is not such a robust 601

flooding signal for roots. Instead, ethylene is the key player mediating this plasticity 602

in root development. These separate roles of ethylene and O2 permit a response 603

tailored to specific flooding conditions. 604

Little is known regarding O2 and ethylene interactions. However, ethylene mutants 605

have reduced hypoxic ADH upregulation (Peng et al., 2001; Yang et al. 2011), 606

ethylene-induced escape growth was enhanced under hypoxic conditions (Voesenek 607

et al., 1997) and ethylene pre-treatment can enhance anoxia tolerance (van Veen et 608



21

al., 2013). Here there is a potential role for ROS and NO. Both are affected by and 609

have an impact on hypoxia and ethylene signaling. While NO destabilizes ERF-VIIs, it 610

is also scavenged by ethylene-inducible and ERF-VII target phytoglobin, and provides 611

a mechanistic link between ethylene and NO (Figure 2). Similarly, ROS is part of both 612

ethylene and ERF-VII signaling pathways. However, it remains unclear whether ROS 613

derived from either signal are interchangeable. 614

It is clear that plants use a multitude of signals to assess a flooding event and trigger 615

appropriate responses that prolong survival (Figure 2). Interestingly, the role of 616

these signals changes through time, as is apparent from the distinct signal 617

interactions during and after submergence (Figure 1). Relatively little is known about 618

signaling dynamics during recovery and how this links to responses initiated during 619

flooding. Additionally, electrophysiological changes occur within minutes of 620

hypoxia/anoxia, but their physiological role remains unestablished (Wang et al., 621

2017). Likewise, NO and ROS bursts occur within the first hours upon hypoxia. It is 622

unclear whether these bursts only push the plant into an altered physiological state 623

that it can homeostatically maintain, or whether they are recurring events during 624

flooding. Too little is known of the temporal dynamics of flooding signals, and the 625

future challenge lies in determining this to assess the relevant positive and negative 626

regulatory feedback loops under actual flooded conditions and how they influence 627

plant response and survival. 628

629

630

631

FIGURE LEGENDS 632 Figure 1. Signal dynamics during a typical light-limited flooding event. During early 633 submergence (light gray shading), ethylene accumulates rapidly while oxygen levels 634 decline gradually. Upon hypoxia, nitric oxide (NO) and reactive oxygen species (ROS) 635 bursts occur. Upon recovery from prolonged submergence (dark gray shading), there 636 is transient ethylene production while oxygen levels return to normal. NO dynamics 637 upon de-submergence are unknown, but a strong ROS burst likely occurs. The 638 schematic conveys general trends based on current knowledge and is intended to 639 show that flooding signals can display strong variability during different phases of 640 the flooding event. Furthermore, these signal dynamics are strongly dependent on 641 flood conditions, plant species and the organ and tissues affected. 642 643



22

Figure 2. An overview of the major flooding signals (yellow boxes) and their 644 interactions, leading to the regulation of major adaptive responses (grey boxes). 645 Restricted gas exchange between the plant and its environment during flooding 646 results in alterations in endogenous levels of CO2, O2 and ethylene. These primary 647 signals can further give rise to the secondary signals ROS, NO and starvation. 648 Changes in the availability of O2 and CO2 is the net result of production, consumption 649 and diffusion and are therefore highly dependent on light conditions during flooding. 650 Changes in CO2 likely influence flooding responses due to its role as a substrate for 651 photosynthesis. CO2 limitation in the light leads to starvation and subsequent 652 metabolic reprogramming via energy signaling mechanisms. A decline in O2 levels 653 limits aerobic respiration, but also triggers downstream acclimation responses via 654 the group VII ethylene response factor (ERFVIIs) transcription factors. Oxygen 655 dependent stabilization of ERF-VIIs via the N-end rule enhances hypoxia-responsive 656 gene expression including the fermentation enzymes (eg: ALCOHOL 657 DEHYDROGENASE). However, an efficient transcriptional induction requires an ERF-658 VII dependent ROS burst through RBOHD. ROS is also formed non-enzymatically 659 during hypoxia via the electron transport chain (ETC). ERF-VII degradation is also 660 dependent on NO. Hypoxia induces NO accumulation, probably due to increased NR 661 activity and subsequent nitrite reduction at the mitochondrial ETC. However NO is 662 also scavenged during hypoxia by hemoglobin (HB1) which in turn is induced by ERF-663 VIIs. O2 levels also play an essential role in energy homeostasis not just via their role 664 as a substrate for respiration. The activation of fermentation through hypoxia-665 stabilized ERF-VIIs boosts ATP production diminishing starvation. At the same time, 666 fermentation is highly dependent on sufficient sugar availability and is thus inhibited 667 by starvation. Additionally, NO increase upon hypoxia is suggested to inhibit 668 cytochrome c oxidase and the TCA cycle enzyme aconitase, altering efficient ATP 669 generation via respiration. 670 Ethylene biosynthesis rates can change upon flooding, but reduced gas exchange is 671 the primary reason for ethylene accumulation to saturating levels. Ethylene 672 accumulation plays a pivotal role in aerenchyma and adventitious root (AR) 673 development mediated by interactions with ROS. Programmed cell death of 674 epidermal cells covering AR primordia is required for penetration, and is essential in 675 the cortex for aerenchyma formation. Ethylene-mediated ROS accumulation occurs 676 via RBOH activity or due to reduced ROS scavenging. 677 678 679

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1127

1128

1129



ADVANCES

• Plants use spatial and temporal dynamics in

ethylene, O2, NO, and ROS to convey information

about flooding conditions.

• A complex web of interactions between these

various signals fine-tunes plant flooding

responses.

• Ethylene accumulates during submergence

regardless of water turbidity and light

penetration, making it a reliable flooding signal.

• The hypoxia-induced NO burst is critical for

hypoxia acclimation, possibly via S-nitrosylation

of key proteins involved in flooding adaptation.

• ROS homeostasis is important for hypoxia

survival.

• Ethylene, NO, and ROS dynamics could also be

important signals during recovery, with roles that

are distinct from those during flooding.



OUTSTANDING QUESTIONS

• How do the spatial and temporal responses to

ethylene, O2, ROS, and NO vary during

flooding and subsequent recovery?

• To what extent are dynamics of ROS and NO

observed in hypoxic systems relevant to actual

flooded conditions?

• Do regulated and uncontrolled ROS or NO

production have similar roles during flooding

and recovery?

• What is the mechanism of ethylene and

oxygen crosstalk?

• Is there variation across species in the ability

to perceive and process flooding signals, and

does this correspond with flooding tolerance?



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http://scholar.google.com/scholar?as_q=Longâ�?�distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Colmer&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

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Gibbs DJ, Lee SC, Isa NM, Gramuglia S, Fukao T, Bassel GW, Correia CS, Corbineau F, Theodoulou FL, Bailey-Serres J, Holdsworth www.plantphysiol.orgon April 4, 2019 - Published by Downloaded from Copyright © 2017 American Society of Plant Biologists. All rights reserved.

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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%3A 15151&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Greenway H%2C Armstrong W%2C Colmer TD %282006%29 Conditions leading to high CO2 %28%3E 5 kPa%29 in waterlogged%2Dflooded soils and possible effects on root growth and metabolism%2E Ann Bot 98%3A 9�??32&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Gupta KJ%2C Igamberdiev AU %282011%29 The anoxic plant mitochondrion as a nitrite%3A NO reductase%2E Mitochondrion 11%3A 537�??543&dopt=abstract

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Setter TL, Bhekasut P, Greenway H (2010) Desiccation of leaves after de- submergence is one cause for intolerance to completesubmergence of the rice cultivar IR 42. Funct Plant Biol 37: 1096–1104


Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjärvi J (2012) ROS-talk – how the apoplast, the chloroplast, and the nucleus get themessage through. Front Plant Sci 3: 292


Smirnoff N (1995) Antioxidant systems and plant response to the environment. In Smirnoff N (Ed.) Environment and plant metabolism:flexibility and acclimation. BIOS Scientific Publishers, Oxford, UK: 217-243


Sorenson R, Bailey-Serres, J (2014) Selective mRNA sequestration by OLIGOURIDYLATE-BINDING PROTEIN 1 contributes totranslational control during hypoxia in Arabidopsis. Proc Natl Acad Sci USA 111: 2373–2378


Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170: 603–617Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Steffens B, Kovalev A, Gorb S N, Sauter M (2012) Emerging roots alter epidermal cell fate through mechanical and reactive oxygenspecies signaling. Plant Biol Cell 24: 3296–3306


Steffens B, Steffen-Heins A, Sauter M (2013) Reactive oxygen species mediate growth and death in submerged plants. Front Plant Sci4: 479


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http://www.ncbi.nlm.nih.gov/pubmed?term=Rhoads DM%2C Umbach AL%2C Subbaiah CC%2C Siedow JN %282006%29 Mitochondrial reactive oxygen species%2E Contribution to oxidative stress and interorganellar signaling%2E Plant Physiol 141%3A 357�??366&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Rhoads DM, Umbach AL, Subbaiah CC, Siedow JN (2006) Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol 141: 357?366

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http://search.crossref.org/?page=1&rows=2&q=Roach T, Na CS, Krieger?Liszkay A (2015) High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability. Plant J 81: 759?766

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2 running title: flooding stress signaling 3 corresponding ... · 4 64. 65. abstract . 66. 67....

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