Molecular and physiological responses of trees to waterlogging stress

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Molecular and physiological responses of trees to waterlogging stress1 1

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Jürgen Kreuzwieser1*

, Heinz Rennenberg1 3

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1Institute of Forest Science, Chair of Tree Physiology, Albert-Ludwigs-Universität 5

Freiburg; Georges-Köhler-Allee 53; 79110 Freiburg, Germany 6

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*corresponding author and present address: 11

Institute of Forest Science, Chair of Tree Physiology, Albert-Ludwigs-Universität 12

Freiburg; Georges-Köhler-Allee 53; 79110 Freiburg, Germany 13

Email : [email protected] 14

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This article has been accepted for publication and undergone full peer review but has not

been through the copyediting, typesetting, pagination and proofreading process, which

may lead to differences between this version and the Version of Record. Please cite this

article as doi: 10.1111/pce.12310

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Abstract 23

One major effect of global climate change will be altered precipitation patterns in many 24

regions of the world. This will cause a higher probability of long-term waterlogging in 25

winter/spring and flash floods in summer due to extreme rainfall events. Particularly trees 26

not adapted at their natural site to such waterlogging stress can be impaired. Despite the 27

enormous economic, ecological and social importance of forest ecosystems, the effect of 28

waterlogging on trees is far less understood than the effect on many crops or the model 29

plant Arabidopsis. There is only a handful of studies available investigating the 30

transcriptome and metabolome of waterlogged trees. Main physiological responses of trees 31

to waterlogging include the stimulation of fermentative pathways and an accelerated 32

glycolytic flux. Many energy consuming, anabolic processes are slowed down to 33

overcome the energy crisis mediated by waterlogging. A crucial feature of waterlogging 34

tolerance is the steady supply of glycolysis with carbohydrates, particularly in the roots; 35

stress sensitive trees fail to maintain sufficient carbohydrate availability resulting in the 36

dieback of the stressed tissues. The present review summarizes physiological and 37

molecular features of waterlogging tolerance of trees; the focus is on carbon metabolism in 38

both, leaves and roots of trees. 39

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Keywords: waterlogging, hypoxia, trees, carbon metabolism, nitrogen metabolism, 41

transcriptome, metabolome. 42

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45

Introduction 46

47

The concentrations of the trace gases carbon dioxide, methane and nitrous oxide in the 48

atmosphere are continuously rising due to anthropogenic activity. Between the pre-49

industrial era and 2005 they increased by 36% (CO2; from 280 to 379 ppm), 148% (CH4; 50

from 715 to 1774 ppb) and 18% (N2O; from 270 to 319 ppb) (Forster et al., 2007). 51

Consequently, the global air temperatures considerably increased between 1850 and 2007 52

and will further increase in the future (Christensen et al., 2007). In Central Europe, for 53

example, a temperature rise in the range of 1.9-7.0°C is expected in the next 50 years 54

(Frei, 2004). Such temperature elevation will strongly affect the global hydrological cycle. 55

Like in North and Central Europe, annual precipitation in East Africa, Northern, East, 56

South and Southeast Asia, Canada and Northeast USA is likely to increase whereas it will 57

decrease in Central America, Southwest USA, Mediterranean Europe, and Central Asia 58

(Christensen et al., 2007). However, precipitation will not change equally over the year; in 59

Central Europe, winter precipitation is predicted to increase in the future, but summer 60

precipitation will be considerably lower causing a higher possibility of drought periods 61

during the summer months (Frei et al., 2006). On the other hand, most model projections 62

forecast increased extreme precipitation events despite decreased mean summer 63

precipitation (Palmer and Räisänen, 2002; Christensen and Christensen, 2003). Because of 64

such intense rainfall events, terrestrial ecosystems in the concerned regions will 65

experience more and probably longer waterlogging periods during winter and spring and 66

more extreme short-term flooding events during summer (Christensen and Christensen, 67

2003; Kundzewicz et al., 2005; Kundzewicz, 2006) particularly on compacted and / or 68

heavy, clay-rich soils where drainage is inhibited (Dennis and Grindley, 1983; Kozlowski, 69

1984). 70 Acc

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71

Soil processes 72

Flooding (i.e. water standing above soil level) and waterlogging (i.e. only the soil is 73

flooded) lead to a deprivation of oxygen in the soil because the floodwater entering the 74

soil removes oxygen rich air from soil pores. In addition, the ca. 10.000 times higher 75

diffusion resistance of oxygen in water than in air leads to an inhibited supply of the soil 76

with oxygen in water saturated soils (Armstrong, 1979). Microbial and plant activities 77

quickly consume the remaining oxygen leading either to hypoxic (low oxygen 78

concentrations: mitochondrial respiration reduced; fermentation takes place) or anoxic 79

(oxygen absent: energy gain by fermentation only) conditions (Pradet and Bomsel, 1978). 80

Due to the lack of oxygen, soil physico-chemical properties such as pH and redox 81

potential strongly change during waterlogging (Pezeshki and Chambers, 1985a; 1985b). 82

The diminished gas diffusion velocity between the soil and the atmosphere causes an 83

accumulation of gaseous compounds in the waterlogged soil such as the plant hormone 84

ethylene or other metabolic products like carbon dioxide (Jackson, 1982). Oxygen 85

shortage further affects microbial communities in the soil (Unger et al., 2009) and 86

numerous microbial processes, which eventually cause changes in soil chemical 87

composition. This can lead to a reduced abundance of oxidised nutrients (e.g. NO3-, SO4

2-, 88

Fe3+

) and elevated levels of reduced compounds such as Mn2+

, Fe2+

, H2S, NH4+, and 89

organic compounds (alkanes, acids, carbonyls, etc) which can be toxic for plants 90

(Ponnamperuma, 1972; 1984; McKee and McKevlin, 1993; Snowden and Wheeler, 1993; 91

Lucassen et al., 2000; 2002; Jackson and Colmer, 2005). The velocity and extent of the 92

changes of soil physico-chemical properties depends on soil type, the duration of the 93

waterlogging event, prevailing environmental conditions (such as temperature) and the 94

type of flooding or waterlogging (Drew, 1997; Kozlowski, 1997). Stagnant conditions 95

reduce the oxygen availability in the soil much faster leading to stronger stress conditions 96

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than moving floodwater where turbulences facilitate oxygen solubilisation in the 97

floodwater. 98

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Effects on trees 100

About 31% of the terrestrial earth surface, i.e. around 4 billion hectares, is covered by 101

forest ecosystems with Latin America (sharing 24% of the world’s forest), former Soviet 102

Union (21%), Africa (20%), and North-America (16%) as the regions with the largest 103

forested areas (FAO, 2012; The Columbia Electronic Encyclopedia, 2012). It is obvious 104

that forests fulfil a plethora of essential ecological (e.g. maintenance of biodiversity, 105

involvement in biogeochemical cycles of water, carbon and nitrogen), economic (e.g. 106

timber and other natural resources, energy source) and social (e.g. recreation) functions. In 107

addition, trees are of particular importance in urban environments as street and park 108

vegetation (Dwyer et al., 1991) or in orchards and as bioenergy source from fast growing 109

plantations, the latter covering 187 million hectares in 2000, with a strongly increasing 110

trend (Carnus et al., 2006). 111

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Because major parts of the landscapes covered by trees/forests are assumed to be more 113

strongly exposed to waterlogging and flooding in the future, plant mechanisms to cope 114

with such stress conditions are of particular interest. However, today the knowledge on 115

physiological and molecular aspects of flooding/waterlogging tolerance in trees is far 116

behind that of herbaceous species (Kreuzwieser et al., 2009). This is due to the fact that 117

studying trees provides particular challenges. Trees are characterised by longevity, making 118

it difficult to work with adult trees under environmentally controlled conditions. The 119

combination of long lifetime and seasonality complicates many plant internal processes: 120

alternating phases of dormancy and growth over the growing season need well-adjusted 121

storage and remobilization processes in order to support meristematic tissues with 122

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nutrients (Tuskan et al., 2003). Supply of growing tissues with nutrients depends on highly 123

orchestrated and regulated long-distance transport processes in phloem and xylem. 124

Storage, mobilization, and long-distance transport can all be affected in different ways by 125

environmental factors such as soil oxygen deficiency. The lack of knowledge on 126

mechanisms of environmental control of these processes in trees compared to crops and 127

model plants such as Arabidopsis or rice becomes particularly evident at the molecular 128

level (Kreuzwieser et al., 2009; Mustroph et al., 2010; Christianson et al., 2010; Narsai et 129

al., 2011). This is partially due to the limited availability of relevant tools and techniques. 130

For example, the first commercially distributed microarray for a tree species became 131

available for poplar only in 2006, after the genome of Populus trichocarpa has been 132

sequenced (Tuskan et al., 2006). As nicely reviewed by Neale and Kremer (2011), forest 133

tree genomics made great progress in recent years as modern sequencing technologies 134

(next generation sequencing, NGS) considerably facilitate tree genome studies and 135

transcriptome profiling (RNA-seq). This certainly will allow faster progress of research on 136

trees in near future. 137

138

As aerobic organisms, trees depend on a steady supply with oxygen to all living cells, and 139

interruption from oxygen availability therefore causes disturbance of plant metabolism 140

(Drew, 1997; Bailey-Serres and Voesenek, 2008). Depending on the tolerance of soil 141

oxygen depletion, this can cause dysfunction of processes at the cellular level, eventually 142

leading to visible damages. Flooding and waterlogging tolerance and the occurrence of 143

injuries is strongly species-dependent (Table 1; Gill, 1970; Kozlowski, 1982; 1997; 144

McClean, 2000; Glenz et al., 2006; Niinemets and Valladares, 2006; Kramer et al., 2008; 145

Parolin et al., 2004; 2010; Ferner et al., 2012). Highly adapted species survive 146

waterlogging periods up to some months without any injuries (Table 1), but less tolerant 147

or sensitive species can develop damages already after a few hours of oxygen deprivation 148

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(see Kozlowski, 1997; Glenz et al., 2006). Besides a reduction of root (see refs in 149

Kozlowski, 1997) and shoot growth (e.g. Colin-Belgrand et al., 1990; Pezeshki et al., 150

1996; Parolin, 2001; Ye et al., 2003; Alaoui-Sossé et al., 2005; Mielke et al., 2005; Parelle 151

et al., 2006; Neatrour et al., 2007; Ferreira et al., 2007; de Oliveira and Joly, 2010; Ferry et 152

al., 2010; Guo et al., 2011), typical symptoms of soil oxygen shortage in sensitive trees are 153

leaf necrosis and shedding, bark damages, elevated susceptibility to fungal and insect 154

pathogens, or dieback of the whole tree (Kozlowski, 1997; Parolin, 2001; Kreuzwieser et 155

al., 2004; Parolin and Wittmann, 2010). The extent of damages depends on the type 156

(stagnant or moving water), duration and height of flooding, the environmental conditions 157

during the stress event (e.g. air, water and soil temperature, solar radiation), the season, 158

but also on a wide range of plant specific features (Kozlowski, 1997; Vreugdenhil et al., 159

2006). The development of damages depends to a high degree on the species considered 160

but also on the ecotype of a given species (Jaeger et al., 2009; Guo et al. 2011), the tree’s 161

age, size and developmental stage (Kozlowski, 1997; Siebel and Blom, 1998; Glenz et al., 162

2006). It is generally observed that adult trees tolerate waterlogging and flooding better 163

than seedlings of the same species (Table 2) (Gill, 1970; Siebel and Blom, 1998). Recent 164

studies even indicated that the sex of a tree plays a role in flooding tolerance of dioecious 165

species such as willow and poplar. There is clear evidence that female willow and poplar 166

trees are more tolerant against the stress than male trees explaining the spatial segregation 167

of the sexes with higher abundance of females in low-elevation zones of riparian forests 168

(Hultine et al. 2007; Nielsen et al. 2010). Nielsen et al. (2010) therefore proposed the 169

concept of “strategic positioning” where the seed-producing female trees are better 170

adapted to sites which are more often flooded and where seedling recruitment usually 171

occurs. 172

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Tree adaptation to flooding 174

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Tree species inhabiting ecosystems, which are regularly exposed to flooding, evolved a 175

broad range of adaptive strategies to cope with the stress mediated by this exposure. Most 176

wetland species apply avoidance strategies based on morphological-anatomical features. 177

Such adaptations have been reviewed for woody species by Kozlowski (1997) and Glenz 178

et al. (2006), and are therefore only briefly mentioned here. Many flood tolerant species 179

develop hypertrophied lenticels at the stem base in response to flooding (compilations of 180

tree species are given by Kozlowski (1997) and Glenz et al. (2006)). These organs 181

penetrate the relatively strongly gas resistant phellogen layer of the trees, enabling gas 182

exchange between stem and environment. Thus, hypertrophied lenticels allow oxygen 183

uptake into the plant, but they are also assumed to contribute to the release of gaseous 184

compounds (carbon dioxide, acetaldehyde, ethanol) out of the stem into the atmosphere 185

(Li et al., 2006; Shimamura et al., 2010). Another feature often associated with the 186

appearance of hypertrophied lenticels is the formation of adventitious roots (Glenz et al., 187

2006) (Fig. 1). Such roots are produced when the primary root system of the tree is 188

impaired because of soil oxygen deficiency. Adventitious roots possess a high portion of 189

intercellular spaces facilitating longitudinal oxygen transport. In a studies with Central 190

Amazonian trees such as Salix martiana and Tabernaemontana juruana, it was 191

demonstrated that the main entry point of atmospheric oxygen were gas-permeable pores 192

in the stem near the origin of the adventitious roots (Haase et al., 2003; Haase & Rätsch, 193

2010). Uptake of oxygen seems also to be possible along the root if it is growing at the 194

water surface being in contact with the atmosphere (Haase et al., 2003). Such oxygen 195

uptake is required for the maintenance of mitochondrial respiration; it further allows radial 196

oxygen loss (ROL) from the roots which contributes to the oxidation of the rhizosphere 197

(Kludze et al., 1994; Li et al., 2006). Further important functions of adventitious roots are 198

absorption of water and nutrients as a replacement of the damaged primary root system 199

(Barlow, 1986; Calvo-Polanco et al., 2012). Impressive examples for adventitious roots 200

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are the prop roots of Rhizophora and the pneumatophores of Avicennia, both inhabitants of 201

mangrove ecosystems (Baylis, 1950; Allaway et al., 2001; Aziz and Khan, 2001) (Fig. 1). 202

The formation of aerenchyma is a third adaptation of plants to cope with oxygen 203

deficiency in the soil (Kozlowski, 1997; Kludze et al., 2004). The formation of lacunae air 204

spaces enhances the porosity of the root tissue facilitating oxygen diffusion within roots 205

and they are likely to contribute to the export of phytotoxic volatile metabolites 206

(acetaldehyde, ethanol) from the plant (Visser et al., 1997). The formation of 207

hypertrophied lenticels, adventitious roots and aerenchyma depends on the accumulation 208

of ethylene in plant tissue (Steffens et al., 2006; Bailey-Serres et al., 2012). Plant internal 209

concentrations of ethylene increase, if floodwater surrounding the plant inhibits the 210

diffusive loss of this volatile plant hormone into the atmosphere, and if – at the same time 211

– ethylene biosynthesis proceeds (Bailey-Serres and Voesenek, 2008). In addition to 212

ethylene, reactive oxygen species (ROS) are involved as signalling intermediates in this 213

ethylene-controlled adaptation (Steffens et al., 2013). Other components also known to 214

play a role in adventitious root formation are the auxin indole acetic acid (IAA) and NO 215

(see Bailey-Serres et al., 2012). IAA abundance induces a transient accumulation of NO 216

(Pagnussat et al., 2002) which in turn activates a MAPK signalling cascade eventually 217

leading to adventitious root formation (Pagnussat et al. 2004). Such knowledge has been 218

gained mainly by studies with herbaceous plants; the mechanisms of hypoxia induced 219

adventitious root formation in trees and particularly the interplay of the different 220

components are still widely unknown. 221

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Physiological effects of waterlogging on trees 224

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Net CO2 assimilation and stomatal conductance of waterlogged trees 226

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One of the most often studied physiological processes during waterlogging of trees is leaf 227

gas exchange, particularly net CO2 assimilation. It is a general phenomenon that 228

assimilation rates tend to decrease during periods of waterlogging stress as observed in 229

trees of tropical (Nunez-Elisea et al., 1999; Fernandez et al., 1999; Ojeda et al., 2004; 230

Fernandez, 2006; Herrera, 2013) and temperate (Pezeshki and Chambers 1985a; 1985b; 231

1986; Pezeshki, 1994; Pezeshki et al., 1996, Dreyer et al., 1991; Reece and Riha, 1991; 232

Beckman et al., 1992; Ewing, 1996; Gravatt and Kirkby, 1998; Jaeger et al., 2009; Ferner 233

et al., 2012) ecosystems. The extent of this decrease depends on the species’ tolerance to 234

soil oxygen deficiency. Highly tolerant trees maintain rates of photosynthesis at a 235

relatively high level or are even unaffected by the stress, whereas net CO2 assimilation of 236

less tolerant or sensitive species is strongly reduced (Dreyer, 1994; Wagner and Dreyer, 237

1997; Graves et al., 2002; Vu and Yelenosky, 2006; Jaeger et al., 2009; Parent et al., 2011; 238

Ferner et al., 2012). In addition, as seen in flood tolerant tree species of the Amazonian 239

floodplain, rates of photosynthesis can completely recover or even increase during long-240

term periods of soil oxygen deficiency; such recovery often coincides with morpho-241

anatomical changes like the appearance of hypertrophied lenticels and/or adventitious 242

roots (Herrera, 2013). 243

244

The reasons for inhibited photosynthesis of waterlogged trees are still not completely 245

understood. There are strong hints that both, non-stomatal and stomatal limitations are 246

involved. Non-stomatal limitation is associated with lowered pigment concentrations in 247

leaves of waterlogged trees (Kreuzwieser et al., 2002; Ojeda et al., 2004), decreased 248

activity (Vu and Yelenosky, 2006) and abundance (Herrera, 2013) of ribulose-1,5-249

bisphosphate carboxylase/oxygenase (Rubisco) and accumulation of soluble carbohydrates 250

which might cause feedback inhibition of photosynthesis (Iglesias et al., 2002; Islam and 251

MacDonald, 2004; Rengifo et al., 2005; Vu and Yelenosky, 2006; Jaeger et al., 2009; 252

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Ferner et al., 2012). On the other hand, waterlogging causes stomatal closure, which has 253

been discussed as the main reason for reduced photosynthesis in numerous trees (Reece 254

and Riha, 1991; Gravatt and Kirkby, 1998, Pezeshki et al., 1996; Schmull and Thomas, 255

2000; Rodríguez-Gamir et al., 2011; Ferner et al., 2012). Although intensively studied, the 256

mechanisms leading to reduced stomatal conductance during periods of waterlogging is far 257

from being understood. It is assumed to be connected to reduced root hydraulic 258

conductivity and subsequently lowered water absorption by the roots and/or caused by 259

chemical signals, which are transported from waterlogged roots to the shoot via the 260

transpiration stream. The nature of potential signalling compounds responsible for 261

stomatal closure is still not known (Else et al., 1996; 2006; Aroca et al., 2011). The 262

involvement of abscisic acid (ABA) transport in the xylem has been proposed (Jackson et 263

al., 2003; Herrera, 2013) but is still a matter of debate, particularly since some reports 264

clearly excluded root-to-shoot ABA transport (Else et al., 2006; Rodríguez-Gamir et al., 265

2011). Waterlogging induced changes in the pH of the xylem sap have also been proposed 266

as a long-distance signal. However, there does not seem to be a consistent plant response 267

as both alkalisation (Else et al., 2006) and acidification (Rodríguez-Gamir et al., 2011) of 268

the xylem sap was observed in waterlogged plants. Recently, mobilization of root stored 269

sulphate and its root-to-shoot transport have been proposed to mediate stomatal closure in 270

response to drought (Ernst et al., 2010); whether these processes are also involved in 271

stomatal closure in response to waterlogging remains to be elucidated. 272

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Reduced root hydraulic conductance 274

Waterlogging induced reduction of stomatal conductance is often associated with 275

diminished root hydraulic conductance as demonstrated in many flood tolerant and 276

sensitive tree species (Syvertsen et al., 1983; Dreyer, 1994; Schmull and Thomas, 2000; 277

Islam et al., 2003; Nicolás et al., 2005; Rodríguez-Gamir et al., 2011). The phenomenon 278

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seems to be more pronounced in the latter group of trees and can be due to a higher degree 279

of damage of their root system and/or lower root biomass due to impaired growth 280

(Schmull and Thomas, 2000). Water absorption by roots is at least partially (ca. 50%) 281

mediated by root water channels (aquaporins) of the plasma membrane intrinsic protein 282

(PIP) family (Tournaire-Roux et al., 2003; McElrone et al., 2007). It can therefore be 283

assumed that modifications of the channel protein or down-regulation of aquaporin 284

expression and subsequent reduced protein abundance might contribute to reduced water 285

permeability of waterlogged roots. The water transport across the plasmalemma can be 286

slowed-down efficiently if a histidine residue of PIPs is protonated, a process depending 287

on acidification of the cytosol (Tournaire-Roux et al., 2003). This cytosolic decrease of pH 288

is a common phenomenon in roots of waterlogged plants that occurs within minutes (Gout 289

et al., 2001). It is assumed to be caused by (i) a passive influx of protons from the external 290

solution or from the vacuole, (ii) the hydrolysis of nucleoside triphosphates and sugar 291

phosphates, and (iii) the accumulation of organic acids including the biosynthesis of lactic 292

acid (Davies et al., 1974; Felle, 2001; Gout et al., 2001). Besides modulation of the 293

aquaporin protein, down-regulation of aquaporin gene expression has also been reported in 294

some tree species (Fig. 2) (Kreuzwieser et al., 2009; LeProvost et al., 2011; Rodríguez-295

Gamir et al., 2011). The question arises, how changes in root hydraulic conductance can 296

be translated into altered stomatal conductance in the leaves. As mentioned above, root-to-297

shoot transport of signalling compounds might be one option. Another widely ignored 298

possibility of root-to-shoot communication is hydraulic signalling. This mechanism of 299

signalling is supposed to maintain water homeostasis in drought stressed plants as recently 300

reviewed by Christmann et al. (2013). It depends on the transfer of a hydraulic signal, i.e. 301

a change in plant water potential, in the xylem and conversion of this signal into a 302

biochemical signal in target cells. A hydraulic – so far unidentified - sensor in leaf cells 303

could initiate a signaling cascade eventually causing ABA biosynthesis leading to the 304

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closure of stomata (Christmann et al., 2013). The idea of hydraulic signaling is supported 305

by reduced water potential in a variety of waterlogged trees that usually is much stronger 306

in flood sensitive than in flood tolerant species (Ruiz-Sánchez et al., 1996; Nicolás et al., 307

2005; Ortuno et al., 2007; Parent et al., 2011; Striker, 2012; Herrera, 2013). 308

Figure 3 summarizes some aspects of plant water relations in waterlogged trees; the switch 309

from normoxia to hypoxia/anoxia by soil waterlogging, results in major changes of root 310

metabolism (see chapters below). This metabolic adjustment is associated with a drop of 311

cytoplasmic pH in root cells (Davies et al., 1974; Roberts et al., 1984; Felle, 2001; Gout et 312

al., 2001), which causes protonation of the PIPs responsible for water absorption by roots. 313

Consequently, root hydraulic resistance increases thereby inhibiting water uptake and 314

affecting plant water status. A hydraulic signal or a chemical signal of yet unknown nature, 315

which is transferred / transported in the xylem, communicates apparent water limitation to 316

the shoot, thereby initiating stomatal closure. 317

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Molecular and physiological changes in roots of waterlogged trees 320

321

Waterlogging causes an enhanced glycolytic flux and fermentative processes 322

If stress avoidance strategies such as hypertrophied lenticels, adventitious roots or 323

aerenchyma are not yet formed or are overburden during a stress period, waterlogged roots 324

may become oxygen deficient and molecular and physiological tolerance mechanisms are 325

essential for plant survival. Several studies indicated that under such conditions major 326

changes occur in the metabolism of roots of trees. In flood tolerant poplar trees, for 327

example, over 2,000 differentially expressed genes were detected after 5 hours of hypoxic 328

treatment compared to roots under normoxic conditions. Less dramatic changes (ca. 1,000 329

differentially expressed genes) were observed in cotton roots, a flood sensitive woody 330

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species, hypoxically treated for 4 hours (see Christianson et al., 2010). Such effects on the 331

trees’ transcriptome were accompanied by strong changes in the root metabolite profile 332

(Kreuzwieser et al., 2009). Because oxygen is the final electron acceptor of mitochondrial 333

respiration, this crucial process of plant energy metabolism is slowed down under hypoxia 334

or even completely inhibited under anoxia. Thus, ATP cannot be produced any longer by 335

aerobic respiration and the cells affected suffer from an energy crisis (Bailey-Serres and 336

Voesenek, 2008). Numerous molecular and physiological studies with flood tolerant and 337

sensitive tree species have demonstrated that fermentative pathways are stimulated under 338

such conditions. Consistent with observations in herbaceous plants (Davies et al., 1974; 339

Roberts et al., 1984), also trees seem to switch in response to hypoxia initially from 340

mitochondrial respiration to lactic acid fermentation. This switch has been documented at 341

both, the metabolite level and the level of lactate dehydrogenase (LDH) gene expression 342

(Joly and Crawford, 1982; Gout et al., 2001; Kolb et al., 2002; Kreuzwieser et al., 2009). 343

Because the accumulation of lactic acid leads to an acidification of the cytosolic pH 344

(Davies et al., 1974), LDH activity is lowered and alcoholic fermentation is stimulated. 345

This change in fermentation processes is suggested from increased pyruvate decarboxylase 346

(PDC) and alcohol dehydrogenase (ADH) activities in waterlogged roots, accompanied by 347

the formation of the intermediate acetaldehyde (Atkinson et al., 2008) and the end-product 348

ethanol (Joly and Crawford, 1982; Kreuzwieser et al., 1999; 2002; Kolb et al., 2002; 349

Jaeger et al., 2009; Ferner et al., 2012). Consistently, elevated transcript levels of PDC and 350

ADH are observed in a great variety of tree species (e.g. Christianson et al., 2010; 351

LeProvost et al., 2012); in poplar, elevated ADH and PDC transcript abundance appeared 352

in less than one hour after the change from normoxia to hypoxia (Kreuzwieser et al., 353

2009). There are hints that flood tolerant species exhibit higher rates of alcoholic 354

fermentation than flood sensitive trees (Porth et al. 2005; Parelle et al. 2006; LeProvost et 355 Acc

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al., 2012), but such patterns are not consistent (Yamanoshita et al., 2005; Ferner et al., 356

2012). 357

358

The few studies on changes in the transcriptome of waterlogged woody species (poplar: 359

Kreuzwieser et al., 2009; cotton: Christianson et al., 2010; pedunculate and sessile oak: 360

LeProvost et al., 2012) suggest that together with an up-regulation of the genes of 361

fermentative pathways (mainly LDH, ADH and PDC), also the glycolytic flux is 362

enhanced, most likely in order to maintain ATP production under conditions of inhibited 363

mitochondrial respiration. In poplar and cotton, enhanced glycolytic flux is suggested from 364

an up-regulation of key enzymes of this pathway, i.e. phosphofructokinase and pyruvate 365

kinase (Kreuzwieser et al., 2009; Christianson et al., 2010). Accelerated glycolysis has 366

also been suggested from a transcriptome approach in which two oak species of different 367

flood tolerance were compared (LeProvost et al., 2012). Maintaining enhanced glycolysis 368

by a steady and sufficient supply with carbohydrates seems to be crucial for tree survival 369

under hypoxia. There are clear experimental evidences that flood tolerant and sensitive 370

species differ in their ability to maintain adequate carbohydrate supply over prolonged 371

periods of waterlogging (Vu and Yelenoski, 1991; Ferner et al., 2012; LeProvost et al., 372

2012). Whereas more sensitive trees deplete of soluble sugars already after some days of 373

waterlogging, more tolerant species maintain carbohydrate concentrations at a high level 374

(Fig. 4) (Herschbach et al., 2005; Jaeger et al., 2009; Martínez-Alcántara et al., 2012; 375

Ferner et al., 2012). The increased demand for soluble carbohydrates in roots of 376

waterlogged trees can at least partially be satisfied by degradation of starch reserves in 377

flood tolerant species (Kreuzwieser et al., 2009; LeProvost et al., 2012). Studies with 378

hypoxically treated poplar indicated another possibility likely to contribute to alleviate the 379

enhanced sugar demand in roots. Elevated levels of succinate together with an up-380

regulation of genes encoding for lipases and enzymes involved in fatty acid degradation, 381

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as well as up-regulation of the isocitrate lyase and the malate synthase genes suggest that 382

the glyoxylate cycle is induced under hypoxia. This pathway is assumed to link lipid 383

degradation with carbohydrate biosynthesis (Eastmond et al., 2000); in waterlogged 384

poplar, it could channel acetyl-CoA formed from β-oxidation of fatty acids into sugar 385

biosynthesis (Kreuzwieser et al., 2009). Degradation of fatty acids has also been observed 386

in some neo-tropical tree species due to prolonged waterlogging (Kolb et al., 2002). 387

Elevated sugar consumption in hypoxia stressed roots could also be compensated by 388

enhanced shoot-to-root transport of photo-assimilates in the phloem (Kreuzwieser et al., 389

2009; Merchant et al., 2010). Moreover, some studies underlined the importance of altered 390

sucrose degradation during hypoxia stress. Changes in root transcript levels indicate that 391

sucrose cleavage via invertases is replaced by phosphorolytic degradation via sucrose 392

synthase (Kreuzwieser et al., 2009; Christianson et al., 2010a; 2010b; LeProvost et al., 393

2012). From an energetic point of view, this switch makes sense, because sucrose synthase 394

uses only one molecule of pyrophosphate as a substrate during sucrose cleavage, whereas 395

invertases use two ATP molecules. The question arises why normoxic roots do not use this 396

pathway as well. Several studies indicated that under non-stress conditions sucrose 397

synthase delivers UDP-glucose mainly for the well-regulated process of cellulose 398

biosynthesis (Albrecht and Mustroph, 2003). Up-regulated UDP-glucose delivery could 399

impair this process. However, under hypoxic conditions cellulose biosynthetic is strongly 400

down-regulated (Kogawara et al., 2006; Kreuzwieser et al., 2009) and it seem 401

energetically advantageous if UDP-glucose is channelled into glycolysis. 402

It seems to be paradox that - particularly in flood sensitive but to a minor extent also in 403

flood tolerant species - root flooding leads to an accumulation of carbohydrate 404

concentrations in the leaves (Vu and Yelenosky, 1991; Gravatt and Kirby, 1998; Merchant 405

et al., 2010; Martínez-Alcántara et al., 2012; Ferner et al., 2012; Herrera, 2013). The even 406

more massive accumulation of soluble carbohydrates in the phloem of some waterlogged, 407

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stress sensitive trees together with considerably reduced carbohydrate concentrations in 408

the roots, suggests that in flooding sensitive species the transport of sugars from the 409

phloem into root cells is dramatically impaired during flooding (Fig. 4) (Jaeger et al., 410

2009; Merchant et al., 2010; Ferner et al., 2012). Alternatively, the conversion of sucrose 411

into monosaccharides may severely be affected. Impaired shoot-to-root transport of photo-412

assimilates has been demonstrated directly from slowed down transport of the 13

C tracer 413

after 13

CO2 fumigation of leaves of flooded citrus trees (Martínez-Alcántara et al., 2012). 414

However, the exact mechanisms causing impaired supply of hypoxia treated roots with 415

photo-assimilates is still not fully understood and needs further investigations. 416

417

Trees become energy safers during periods of waterlogging 418

From the massive changes in transcript abundance observed in roots of poplar, cotton and 419

oak trees, it can be concluded that – in accordance with observations in herbaceous species 420

– numerous energy intensive processes are slowed down under hypoxic conditions 421

(Kreuzwieser et al., 2009; Christianson et al., 2010; LeProvost et al., 2012). For example, 422

the transcript levels of many genes encoding transporters are decreased suggesting 423

diminished nutrient uptake in waterlogged trees (Kreuzwieser and Gessler, 2010). This 424

assumption is supported by reduced rates of N uptake and strongly affected nitrate and 425

amino acid concentrations in roots of hypoxically treated trees (Kreuzwieser et al., 2002; 426

Alaoui-Sossé et al., 2005). Other energy consuming processes strongly affected in 427

waterlogged trees are the biosynthesis of cell wall components such as cellulose, 428

hemicellulose, and cell wall proteins, as well as lignin (Kreuzwieser et al., 2009; 429

Christianson et al., 2010a; b; LeProvost et al., 2012). Consistent with slowed down 430

anabolic processes, reduced growth is often observed in waterlogged trees; growth of 431

flooding sensitive trees is usually stronger impaired than that of more tolerant species (see 432

Kreuzwieser et al., 2004; Herrera 2013). 433

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434

Changes in N metabolism of waterlogged roots 435

As mentioned above, root nitrate and ammonium uptake is often strongly impaired by 436

waterlogging. Such effects were much more pronounced in flood sensitive compared to 437

more tolerant species (Kreuzwieser et al., 2002). Transcript abundance profiles indicate 438

that many genes involved in amino acid biosynthesis and degradation differed in hypoxia 439

treated trees (Kreuzwieser et al., 2009; Christianson et al., 2010; LeProvost et al., 2012). 440

Consistent with gene expression patterns, many amino acids with increased abundance in 441

hypoxia treated trees were derived from pyruvate (e.g. alanine, valine, leucine) or other 442

intermediates of glycolysis (glycine, serine, tyrosine). In contrast, amino acids formed 443

from TCA cycle components (glutamine, glutamate, aspartate, asparagine) generally 444

showed lower levels in hypoxic than in normoxic roots (Kreuzwieser et al., 2002; 2009; 445

Jaeger et al., 2009). The latter finding suggests that the metabolic flux of organic acids 446

into the TCA cycle is inhibited under hypoxic conditions; thus, lower concentrations of 447

these amino acids seem to be caused by limited availability of carbon compounds from the 448

TCA cycle. 449

450

Kreuzwieser et al. (2002) observed a significant accumulation of γ-aminobutyrate 451

(GABA) and alanine but decreased glutamate levels in roots of waterlogged European 452

beech, Pedunculate oak and Grey poplar. Accumulation of GABA and alanine was 453

strongest in the roots of flooding sensitive beech. This metabolite pattern indicates that the 454

GABA shunt was induced by waterlogging; this assumption is further supported by a 455

strongly elevated transcript abundance of the glutamate decarboxylase gene in 456

waterlogged poplar roots (Kreuzwieser et al., 2009). The GABA shunt is a proton 457

consuming pathway and is thought to contribute to pH stabilisation during periods of 458

oxygen deprivation (Crawford et al., 1994). The metabolite GABA has also been 459

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discussed as a signalling compound, likely to contribute to ethylene biosynthesis and, 460

therefore, being involved in morphological adaptations of waterlogged plant (Kreuzwieser 461

et al., 2009). 462

463

It has been hypothesized that nitrate contributes to the maintenance of redox and energy 464

homeostasis of hypoxia treated cells (Igamberdiev and Hill, 2004). The responsible 465

mechanism proposed depends on the contribution of class 1 non-symbiotic haemoglobin, 466

NO and the enzyme nitrate reductase (NR). In several trees oxygen deprivation causes an 467

up-regulation of the gene encoding for non-symbiotic haemoglobin (Parent et al., 2008; 468

Kreuzwieser et al., 2009; Parent et al., 2011; LeProvost et al., 2012). This protein is 469

directly involved in the oxidation of NO thereby forming nitrate. Nitrate can again be 470

reduced by the action of NR to yield NO. The reduced haemoglobin molecule is oxidized 471

by interaction with molecular oxygen; this step also involves oxidation of NADH. The 472

haemoglobin/NO cycle therefore contributes to the maintenance of glycolysis and 473

consequently to ATP production during hypoxia (Igamberdiev et al., 2005). As a 474

signalling compound, NO generated by NR activity has a regulatory function for 475

morphological adaptations to flooding such as the formation of aerenchyma, adventitious 476

roots and hypertrophied lenticels (Parent et al., 2011). Importantly, the higher flooding 477

tolerance of Pedunculate oak (moderately tolerant) compared Sessile oak (flooding 478

sensitive) has been linked to the abundance of the non-symbiotic haemoglobin that was 479

found to be considerably higher in the more flooding tolerant genotype (Parent et al., 480

2011). 481

482

The root-to-shoot transport of metabolites is affected by flooding 483

Metabolite profiling indicates massive changes in the content of soluble carbohydrates, 484

amino acids and organic acids in roots and leaves of waterlogged trees (Kreuzwieser et al., 485

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2002; Kreuzwieser et al., 2009; Jaeger et al., 2009). Despite its importance for 486

communication between distant organs, long-distance transport of metabolites from shoot 487

to roots and vice versa has not been studied intensively in waterlogged plants. Hypoxia 488

induced altered metabolite and nutrient levels have been observed in the phloem of 489

Eucalyptus globulus suggesting that the transport between shoot and roots is impaired by 490

waterlogging (Merchant et al., 2010). Figure 5 indicates that hypoxia also considerably 491

affects the transport of metabolites from roots to the shoot. In consistence with elevated 492

levels of GABA, alanine, glycine in the roots of waterlogged poplar (Kreuzwieser et al., 493

2009), these amino acids were present in higher concentrations in the xylem sap of 494

hypoxia stressed trees (Fig. 5; Fig. 6). Similarly, the concentrations of the product of 495

alcoholic fermentation accumulated in roots and the xylem sap (Kreuzwieser et al., 1999). 496

On the other hand, metabolites with lower abundance in waterlogged roots (glutamate, 497

glutamine) tended to show decreased xylem sap concentrations under the same conditions. 498

Similar effects were found in flooding sensitive Fagus sylvatica and Quercus robur 499

seedlings (Kreuzwieser, unpublished data). Future studies should aim to get a more 500

detailed picture on hypoxia caused effects on long-distance transport of metabolites 501

between roots and the shoot. Such changes could contribute to signalling between below- 502

and above-ground plant parts. 503

504

Several studies have demonstrated that waterlogging strongly affects the exchange of trace 505

gases between leaves and the atmosphere. A common phenomenon observed in 506

hypoxically treated trees are the strongly induced emissions of acetaldehyde and ethanol 507

by the leaves (Fig. 6) (Kreuzwieser et al., 1999; Holzinger et al., 2000; Parolin et al., 2004; 508

Rottenberger et al., 2008; Copolovici and Niinemets, 2010; Bracho-Nunez et al., 2012). In 509

Grey poplar, for example, ca. 75% of the ethanol formed in the roots via alcoholic 510

fermentation is transported to the leaves with the transpiration stream (Kreuzwieser et al., 511

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1999). Considering the high membrane permeability of ethanol, it is assumed that the 512

xylem loading of ethanol occurs passively by diffusion. In the leaves ethanol is oxidised 513

by ADH thereby forming acetaldehyde which is further converted into acetate 514

(Kreuzwieser et al., 2001). Acetate can enter primary carbon metabolism after activation 515

to acetyl-CoA (Ferner et al., 2012). Small portions of the ethanol delivered to the leaves is 516

released as volatile compounds ethanol, acetaldehyde and acetate into the atmosphere via 517

the stomata (Kreuzwieser et al., 1999; Ferner et al., 2012). The transport of ethanol from 518

roots to the shoot and its conversion to metabolites used in primary carbon metabolism can 519

be seen as a physiological adaptation to waterlogging, since the energy rich carbon 520

skeletons of these compounds can be re-used in the leaves. In addition, an accumulation of 521

phytotoxic acetaldehyde is avoided in the roots. However, a clear correlation of this 522

mechanism to a species’ flooding tolerance has not been observed, as both, highly tolerant 523

and less tolerant species show this ethanol cycling (Kreuzwieser and Rennenberg, 2013). 524

525

Interestingly, not only metabolites linked to fermentative pathways show altered emission 526

due to waterlogging but also several other trace gases (Fig. 6) (Copolovici and Niinemets, 527

2010; Holzinger et al., 2010). These volatiles are typically stress induced like ethylene, 528

NO or wound induced VOC. The latter compounds are products of the lipoxygenase 529

reaction such as hexenal or hexenol (Copolovici and Niinemets, 2010). The emission of 530

most of these compounds correlates with the flooding tolerance of the tree investigated: 531

flooding tolerant trees show lower emission rates than more sensitive species. In addition, 532

the emission of NO correlates with the trees’ flooding tolerance, probably its role during 533

oxidative stress scavenging (Copolovici and Niinemets, 2010). Another compound, which 534

is emitted at higher rates in waterlogged trees, is methanol. This alcohol is formed during 535

cell wall modifications by pectin methylesterases; these enzymes catalyse the 536

demethylation of pectins during leaf expansion and cell wall degradation (Hüve et al., 537

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2007; Copolovici and Niinemets, 2010). The increased emission rates of methanol from 538

leaves of waterlogged trees might therefore be a result of stress-induced cell wall 539

degradation in the leaves or a product of aerenchyma and adventitious root formation in 540

the roots. These mechanisms would depend on the transport of methanol from roots to the 541

shoot in the xylem sap of the trees. Future studies should therefore include an analysis of 542

methanol in the xylem sap of waterlogged trees. 543

544

Conclusions and perspectives 545

Despite their great economic, ecological and social significance, the response of trees to 546

waterlogging is far from being understood. This is due to a lack of studies at both, the 547

physiological and the molecular level. So far, there are only three publications on four 548

woody species providing data on changes of the transcriptome of trees in response to 549

waterlogging. In these studies, two flooding tolerant (poplar, Pedunculate oak) and two 550

sensitive species (cotton, Sessile oak) were investigated (Kreuzwieser et al., 2009; 551

Christianson et al., 2010; LeProvost et al., 2012). Even less data are available for 552

waterlogging effects on the metabolome of trees. However, such information is urgently 553

needed for a better understanding of physiological adaptations of woody species to 554

hypoxia. Surprisingly, although the xylem sap of trees can be collected relatively easily, 555

studies on hypoxia effects on the composition of the xylem sap are scarce and metabolite 556

profiling has not been reported. Future studies, investigating the effect of waterlogging 557

stress on trees, should include such approaches in order to elucidate which processes are 558

decisive for flooding tolerance of trees. The few –omics studies performed indicate 559

similarities between herbaceous plants and trees. It seems to be common that hypoxia 560

causes an energy crisis in plants leading to down-regulation of energy consuming 561

processes including shoot and root growth. Apparently, the initiation of fermentative 562

pathways together with enhanced glycolytic flux is of greatest importance for survival of 563

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waterlogging periods (Fig. 6). In trees, steady carbohydrate supply for maintenance of 564

glycolysis seems to be crucial and flooding sensitive and tolerant species display large 565

differences in this capability. The reasons for such differences are, however, not 566

understood and should be in the focus of future research. 567

568

569 570

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992

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994 Figure legends 995

Fig. 1: dventitious roots of different tree species as adaptive responses to flooding. A, 996

the mangrove species Rhizophora; B, close-up of Rhizophora prop roots; C, 997

pneumatophores of Avicennia; D, adventitious roots of Grey poplar (P. x canescens). 998

999

Fig. 2: Aquaporin gene expression in poplar roots as affected by waterlogging. Leafs of P. 1000

x canescens trees were harvested after 168 hours, roots after 5, 24 and 168 hours of 1001

waterlogging and transcript abundances were determined by microarray analysis. Shown 1002

are the log2 values of fold changes of flooded compared to control trees by using the 1003

colour code indicated. Relative abundance indicates the raw signal value of normoxic 1004

controls on the microarray. Data are from Kreuzwieser et al. (2009). 1005

1006

Fig. 3: Processes assumed to be involved in the reduction of hydraulic conductance of 1007

flooded roots. A change from normoxia to flooding induced hypoxia or anoxia causes 1008

several adjustments in root metabolism (Kreuzwieser et al., 2009). Cytosolic pH decrease 1009

may result from lactic acid fermentation, hydrolysis of nucleoside triphosphates (NTP), 1010

proton influx from vacuoles or external medium, and the biosynthesis of organic acids 1011

other than lactic acid (Gout et al., 2001). Subsequent protonation of PIPs reduces the water 1012

absorption by roots, thereby decreasing the root water potential (Tournaire et al., 2003). 1013

Root-to-shoot signals of unknown nature (hydraulic signal or chemical signal) lead to the 1014

closure of the stomata. 1015

1016

Fig. 4. Effects of waterlogging on whole plant carbon cycling of flood tolerant and flood 1017

sensitive tree species. Net photosynthesis and soluble carbohydrate contents in leaves, 1018

roots, phloem and xylem sap were determined in plants waterlogged for 7 days and in non-1019 Acc

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waterlogged control plants (data from Ferner et al., 2012). Starch content of leaves and 1020

roots were not affected by waterlogging (Ferner et al., 2012) (data not shown;). Blue / red 1021

/green colours indicate values significantly higher / lower / unaffected compared to 1022

controls; the numbers give percent differences relative to controls. Grey arrows and areas 1023

indicate the 100 % levels of control plants. 1024

1025

Fig. 5. Waterlogging induced changes in the xylem sap composition of poplar trees. 1026

Xylem sap of 3 months old Populus x canescens trees normally watered or waterlogged 1027

for 2 days was collected and analysed for metabolites via GC/MS (Kreuzwieser et al., 1028

2009). Log2 of fold changes (FC) is displayed by the colour code shown. P-values of a 1029

Student’s t’test are indicated (n=4). 1030

1031

Fig. 6. Simplified scheme of the temporal response of trees to waterlogging. Processes and 1032

metabolites indicated in blue are usually up-regulated and increased in abundance, 1033

respectively, due to the stress. Red colour indicated processes usually down-regulated or 1034

metabolites with reduced abundance. 1035

1036

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Tables 1037 1038

Table 1. Estimated maximum number of days of flooding tolerated by some adult 1039

European tree species grown in riparian floodplains of the Upper Rhine River in South-1040

West Germany. Trees were assessed for visible damages of the aboveground plant parts, 1041

i.e. leaf shedding and necrosis and bark damages. Assessments took place after natural 1042

flood events which occurred during summer. Data compiled from Späth (1988, 2002) and 1043

Armbruster et al. (2006). 1044

Species maximum duration

without damages (days)

dieback expected

duration (days)

Salix alba 170 none

Populus nigra 140 none

Ulmus minor 136 none

Quercus robur 113 none

Alnus glutinosa 108 none

Betula 101 none

Populus balsamifera 87 none

Platanus 60 none

Pinus sylvestris 49 none

Acer campestre 48 none

Juglans regia 41 none

Robinia pseudoacacia 40 55

Malus sylvestris 35 51

Carpinus betulus 35 51

Fraxinus excelsior 30 46

Tilia 30 48 Acc

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Acer pseudoplatanus <30 43

Acer platanoides <12 43

Fagus sylvatica 9 37

Prunus avium 10 12

1045

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1047

Table 2: Some examples of waterlogging tolerances of field grown European tree species 1048

of different age. Trees were grown under natural conditions in riparian forests; they were 1049

assessed for stress symptoms of the aboveground parts (leaf necrosis, leaf shedding, bark 1050

damages) after flood events during the vegetation period. Data compiled from Dister 1051

(1983), Späth (1988, 2002), Schaffrath (2000), Armbruster et al. (2006). 1052

Species Maximal waterlogging period without stress symptoms

[number of days]

Seedling Young stand Adult tree

Quercus robur

Fraxinus excelsior

30-46

14-35

25

48

113-150

30-72

Acer pseudoplatanus 16-20 17-46 17-30

Fagus sylvatica 9 16 9-35

1053

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Figure 2

Putative aquaporins Closest AGI

ProteinID

Log2 of fold changes

Relative Abundance

[mean±s.d.]

L168 R5 R24 R168 Leaf Root

PIP1.4, putative At4g00430 656216 428±300 1675±320

water channel // aquaporin PIP At2g37180 735494 44±13 663±579

water channel // aquaporin PIP At4g00430 701598 1257±472 372±168

PIP3 At4g35100 721668 579±208 124±17

PIP2;4/PIP2F; aquaporin PIP At5g60660 723536 74±19 2773±684

PIP24 567607 2650±338 3376±665

MIP family protein 573880 158±53 118±23

MIP family protein 691926 1942±1020 1215±590

GAMMA-TIP; // aquaporin TIP At2g36830 702770 643±530 970±439

GAMMA-TIP; // aquaporin TIP At2g36830 576791 480±145 266±83

Delta-TIP, or NH3 transporter At3g16240 7±2 99±23

TIP, putative At2g25810 561759 445±93 4072±738

< -8 -6 -4 -2 0 2 4 6 > 8

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Figure 5 12

Compound Log2_FC p-value GABA 0.018Glycine 0.032Alanine 0.019Lactic acid 0.000Proline 0.362 Quinic acid 0.168 Serine 0.041Uracil, dihydro- 0.117 Inositol, myo- 0.059 Carbohydrate 0.569 Dehydroascorbic acid 0.176 Threonine 0.474 Leucine 0.007Salicin 0.335 Pyroglutamic acid 0.105 Butandioic acid 0.008Sucrose 0.787 Glucose 0.971 Oxalic acid, allyl nonylester 0.201 Malic acid 0.066 Asparagine 0.657 Sorbose 0.035Fructose 0.102 Mannose 0.007Glutamic acid 0.241 Glutamine 0.209 Glucopyranose, D- 0.146

3‐3 ‐2 ‐1 0 1 2 3

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