Molecular and physiological responses of trees to waterlogging stress1

Accepted Article

1 2 3

Jürgen Kreuzwieser1*, Heinz Rennenberg1

4 5

1

6

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

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

7 8 9

10 11

*corresponding author and present address:

12

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

13

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

14

Email : [email protected]

15 16 17 18 19 20 21

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 1 This article is protected by copyright. All rights reserved.

Abstract

24

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

25

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

26

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

27

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

28

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

29

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

30

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

31

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

32

to waterlogging include the stimulation of fermentative pathways and an accelerated

33

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

34

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

35

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

36

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

37

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

38

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

39

both, leaves and roots of trees.

Accepted Article

22 23

40 41

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

42

transcriptome, metabolome.

43 44

2 This article is protected by copyright. All rights reserved.

Accepted Article

45 46

Introduction

47 48

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

49

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

50

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

51

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

52

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

53

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

54

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

55

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

56

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

57

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

58

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

59

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

60

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

61

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

62

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

63

forecast increased extreme precipitation events despite decreased mean summer

64

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

65

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

66

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

67

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

68

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

69

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

70

1984).

3 This article is protected by copyright. All rights reserved.

Accepted Article

71 72

Soil processes

73

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

74

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

75

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

76

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

77

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

78

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

79

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

80

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

81

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

82

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

83

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

84

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

85

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

86

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

87

numerous microbial processes, which eventually cause changes in soil chemical

88

composition. This can lead to a reduced abundance of oxidised nutrients (e.g. NO3-, SO42-,

89

Fe3+) and elevated levels of reduced compounds such as Mn2+, Fe2+, H2S, NH4+, and

90

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

91

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

92

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

93

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

94

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

95

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

96

reduce the oxygen availability in the soil much faster leading to stronger stress conditions 4 This article is protected by copyright. All rights reserved.

than moving floodwater where turbulences facilitate oxygen solubilisation in the

98

floodwater.

Accepted Article

97

99

100

Effects on trees

101

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

102

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

103

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

104

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

105

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

106

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

107

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

108

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

109

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

110

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

111

trend (Carnus et al., 2006).

112 113

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

114

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

115

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

116

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

117

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

118

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

119

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

120

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

121

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

122

storage and remobilization processes in order to support meristematic tissues with 5 This article is protected by copyright. All rights reserved.

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

124

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

125

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

126

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

127

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

128

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

129

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

130

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

131

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

132

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

133

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

134

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

135

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

136

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

137

trees in near future.

Accepted Article

123

138 139

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

140

interruption from oxygen availability therefore causes disturbance of plant metabolism

141

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

142

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

143

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

144

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

145

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

146

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

147

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

148

or sensitive species can develop damages already after a few hours of oxygen deprivation 6 This article is protected by copyright. All rights reserved.

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

150

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

151

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

152

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

153

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

154

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

155

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

156

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

157

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

158

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

159

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

160

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

161

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

162

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

163

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

164

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

165

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

166

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

167

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

168

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

169

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

170

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

171

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

172

occurs.

Accepted Article

149

173 174

Tree adaptation to flooding 7 This article is protected by copyright. All rights reserved.

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

176

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

177

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

178

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

179

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

180

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

181

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

182

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

183

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

184

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

185

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

186

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

187

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

188

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

189

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

190

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

191

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

192

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

193

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

194

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

195

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

196

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

197

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

198

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

199

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

200

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

Accepted Article

175

8 This article is protected by copyright. All rights reserved.

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

202

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

203

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

204

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

205

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

206

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

207

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

208

hypertrophied lenticels, adventitious roots and aerenchyma depends on the accumulation

209

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

210

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

211

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

212

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

213

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

214

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

215

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

216

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

217

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

218

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

219

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

220

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

221

components are still widely unknown.

Accepted Article

201

222 223 224

Physiological effects of waterlogging on trees

225 226

Net CO2 assimilation and stomatal conductance of waterlogged trees 9 This article is protected by copyright. All rights reserved.

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

228

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

229

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

230

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

231

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

232

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

233

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

234

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

235

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

236

relatively high level or are even unaffected by the stress, whereas net CO 2 assimilation of

237

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

238

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

239

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

240

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

241

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

242

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

243

roots (Herrera, 2013).

Accepted Article

227

244 245

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

246

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

247

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

248

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

249

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

250

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

251

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

252

MacDonald, 2004; Rengifo et al., 2005; Vu and Yelenosky, 2006; Jaeger et al., 2009; 10 This article is protected by copyright. All rights reserved.

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

254

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

255

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

256

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

257

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

258

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

259

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

260

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

261

transpiration stream. The nature of potential signalling compounds responsible for

262

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

263

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

264

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

265

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

266

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

267

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

268

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

269

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

270

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

271

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

272

stomatal closure in response to waterlogging remains to be elucidated.

Accepted Article

253

273 274

Reduced root hydraulic conductance

275

Waterlogging induced reduction of stomatal conductance is often associated with

276

diminished root hydraulic conductance as demonstrated in many flood tolerant and

277

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

278

Islam et al., 2003; Nicolás et al., 2005; Rodríguez-Gamir et al., 2011). The phenomenon 11 This article is protected by copyright. All rights reserved.

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

280

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

281

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

282

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

283

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

284

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

285

expression and subsequent reduced protein abundance might contribute to reduced water

286

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

287

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

288

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

289

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

290

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

291

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

292

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

293

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

294

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

295

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

296

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

297

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

298

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

299

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

300

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

301

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

302

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

303

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

304

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

Accepted Article

279

12 This article is protected by copyright. All rights reserved.

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

306

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

307

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

308

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

309

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

310

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

311

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

312

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

313

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

314

Consequently, root hydraulic resistance increases thereby inhibiting water uptake and

315

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

316

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

317

the shoot, thereby initiating stomatal closure.

Accepted Article

305

318 319 320

Molecular and physiological changes in roots of waterlogged trees

321 322

Waterlogging causes an enhanced glycolytic flux and fermentative processes

323

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

324

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

325

may become oxygen deficient and molecular and physiological tolerance mechanisms are

326

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

327

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

328

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

329

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

330

differentially expressed genes) were observed in cotton roots, a flood sensitive woody 13 This article is protected by copyright. All rights reserved.

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

332

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

333

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

334

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

335

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

336

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

337

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

338

sensitive tree species have demonstrated that fermentative pathways are stimulated under

339

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

340

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

341

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

342

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

343

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

344

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

345

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

346

This change in fermentation processes is suggested from increased pyruvate decarboxylase

347

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

348

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

349

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

350

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

351

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

352

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

353

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

354

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

355

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

Accepted Article

331

14 This article is protected by copyright. All rights reserved.

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

357

2012).

Accepted Article

356

358 359

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

360

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

361

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

362

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

363

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

364

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

365

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

366

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

367

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

368

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

369

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

370

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

371

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

372

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

373

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

374

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

375

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

376

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

377

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

378

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

379

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

380

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

381

regulation of genes encoding for lipases and enzymes involved in fatty acid degradation, 15 This article is protected by copyright. All rights reserved.

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

383

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

384

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

385

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

386

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

387

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

388

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

389

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

390

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

391

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

392

sucrose cleavage via invertases is replaced by phosphorolytic degradation via sucrose

393

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

394

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

395

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

396

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

397

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

398

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

399

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

400

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

401

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

402

energetically advantageous if UDP-glucose is channelled into glycolysis.

403

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

404

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

405

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

406

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

407

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

Accepted Article

382

16 This article is protected by copyright. All rights reserved.

stress sensitive trees together with considerably reduced carbohydrate concentrations in

409

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

410

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

411

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

412

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

413

assimilates has been demonstrated directly from slowed down transport of the

414

after 13CO2 fumigation of leaves of flooded citrus trees (Martínez-Alcántara et al., 2012).

415

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

416

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

Accepted Article

408

13

C tracer

417 418

Trees become energy safers during periods of waterlogging

419

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

420

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

421

– numerous energy intensive processes are slowed down under hypoxic conditions

422

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

423

the transcript levels of many genes encoding transporters are decreased suggesting

424

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

425

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

426

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

427

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

428

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

429

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

430

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

431

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

432

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

433

Kreuzwieser et al., 2004; Herrera 2013). 17 This article is protected by copyright. All rights reserved.

Accepted Article

434 435

Changes in N metabolism of waterlogged roots

436

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

437

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

438

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

439

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

440

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

441

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

442

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

443

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

444

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

445

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

446

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

447

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

448

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

449

TCA cycle.

450 451

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

452

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

453

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

454

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

455

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

456

strongly elevated transcript abundance of the glutamate decarboxylase gene in

457

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

458

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

459

oxygen deprivation (Crawford et al., 1994). The metabolite GABA has also been 18 This article is protected by copyright. All rights reserved.

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

461

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

462

et al., 2009).

Accepted Article

460

463 464

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

465

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

466

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

467

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

468

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

469

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

470

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

471

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

472

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

473

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

474

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

475

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

476

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

477

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

478

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

479

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

480

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

481

2011).

482 483

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

484

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

485

amino acids and organic acids in roots and leaves of waterlogged trees (Kreuzwieser et al., 19 This article is protected by copyright. All rights reserved.

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

487

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

488

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

489

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

490

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

491

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

492

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

493

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

494

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

495

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

496

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

497

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

498

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

499

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

500

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

501

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

502

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

503

and above-ground plant parts.

Accepted Article

486

504 505

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

506

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

507

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

508

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

509

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

510

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

511

fermentation is transported to the leaves with the transpiration stream (Kreuzwieser et al., 20 This article is protected by copyright. All rights reserved.

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

513

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

514

by ADH thereby forming acetaldehyde which is further converted into acetate

515

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

516

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

517

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

518

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

519

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

520

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

521

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

522

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

523

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

524

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

Accepted Article

512

525 526

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

527

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

528

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

529

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

530

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

531

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

532

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

533

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

534

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

535

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

536

cell wall modifications by pectin methylesterases; these enzymes catalyse the

537

demethylation of pectins during leaf expansion and cell wall degradation (Hüve et al., 21 This article is protected by copyright. All rights reserved.

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

539

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

540

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

541

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

542

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

543

methanol in the xylem sap of waterlogged trees.

Accepted Article

538

544 545

Conclusions and perspectives

546

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

547

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

548

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

549

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

550

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

551

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

552

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

553

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

554

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

555

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

556

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

557

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

558

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

559

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

560

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

561

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

562

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

563

pathways together with enhanced glycolytic flux is of greatest importance for survival of 22 This article is protected by copyright. All rights reserved.

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

565

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

566

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

567

understood and should be in the focus of future research.

Accepted Article

564

568 569 570 571

References

572 573

Alaoui-Sossé B., Gérard B., Binet P., Toussaint M.-L. & Badot P.-M. (2005) Influence of

574

flooding on growth, nitrogen availability in soil, and nitrate reduction of young oak

575

seedlings (Quercus robur L.). Annals of Forest Science 62, 593-600.

576

Albrecht G. & Mustroph A. (2003) Localization of sucrose synthase in wheat roots:

577

increased in situ activity of sucrose synthase correlates with cell wall thickening by

578

cellulose deposition under hypoxia. Planta 217, 252–260.

579

Allaway W.G., Curran M., Hollington L.M., Ricketts M.C. & Skelton N.J. (2001) Gas

580

space and oxygen exchange in roots of Avicennia marina (Forssk.) Vierh. var.

581

australasica (Walp.) Moldenke ex N. C. Duke, the Grey Mangrove. Wetlands

582

Ecology and Management 9, 211–218.

583

Armbruster J., Muley-Fritze A., Pfarr U., Rhodius R., Siepmann-Schinker D., Sittler B.,

584

Späth V., Trémolières M., Rennenberg H. & Kreuzwieser J. (2006) FOWARA -

585

Forested water retention areas – guideline for decision makers, forest managers and

586

land owners. Albert-Ludwigs-Universität Freiburg. pp. 84.

587 588 589 590

Armstrong W. (1979) Aeration in higher plants. Advances in Botanical Research 7:225332.

Aroca R., Porcel R. & Ruis-Lozano J.M. (2011) Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany 63: 43–57.

591

Atkinson C.J., Harrison-Murray R.S. & Taylor J.M. (2008) Rapid flood-induced stomatal

592

closure accompanies xylem sap transportation of root-derived acetaldehyde and

593

ethanol in Forsythia. Environmental and Experimental Botany 64, 196–205. 23

This article is protected by copyright. All rights reserved.

Aziz I. & Khan M.A. (2001) Effect of Seawater on the Growth, Ion Content and Water

595

Potential of Rhizophora mucronata Lam. Journal of Plant Research 114, 369-373.

596

Bailey-Serres J. & Voesenek L.A.C.J. (2008) Flooding stress: acclimations and genetic

Accepted Article

594

597 598 599

diversity. Annual Reviews of Plant Biology 59, 313–339.

Bailey-Serres J., Cho Lee S. & Brinton E. (2012) Waterproofing crops: effective flooding survival strategies. Plant Physiology 160, 1698-1709.

600

Barlow P.W. (1986) Adventitious roots of whole plants: Their forms, functions, and

601

evolution. In New Root Formation in Plants and Cuttings, Jackson M.B. (Ed.).

602

Martinus Nijhoff Publishers, Dordrecht, The Netherlands.

603 604 605 606

Baylis G.T.S. (1950) Root system of the New Zealand mangrove. Transactions of the Royal Society of New Zealand 78: 509–514.

Beckman T.G., Perry R.L. & Flore J.A. (1992) Short-term flooding affects gas exchange characteristics of containerized sour cherry trees. Hortscience 27, 1297-1301.

607

Bracho-Nunez A., Knothe N.M., Costa W.R., Liberato M.A.R., Kleiss B., Rottenberger S.,

608

Piedade M.T.F. & Kesselmeier J. (2012) Root anoxia effects on physiology and

609

emissions of volatile organic compounds (VOC) under short- and long-term

610

inundation of trees from Amazonian floodplains. SpringerPlus 1:9 doi:10.1186/2193-

611

1801-1-9.

612

Calvo-Polanco M., Jorge Señorans J. & Zwiazek J.J. (2012) Role of adventitious roots in

613

water relations of tamarack (Larix laricina) seedlings exposed to flooding. BMC

614

Plant Biology 12:99. http://www.biomedcentral.com/1471-2229/12/99.

615

Carnus J.-M., Parrotta J., Brockerhoff E., Arbez M., Jactel H., Kremer A., Lamb D.,

616

O’Hara K.& Walters B. (2006) Planted forests and biodiversity. Journal of Forestry

617

104, 65–77.

618 619

Christensen J.H., Christensen O.B. (2003) Severe summertime flooding in Europe. Nature, 421, 805

620

Christensen J.H., Hewitson B., Busuioc A., Chen A., Gao X., Held I., Jones R., Kolli

621

R.K., Kwon W.-T., Laprise R., Magaña Rueda V., Mearns L.,. Menéndez C.G,

622

Räisänen J.,. Rinke A., Sarr A. & Whetton P. (2007) Regional Climate Projections.

623

In: Climate Change 2007: The Physical Science Basis. Contribution of Working

624

Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate 24

This article is protected by copyright. All rights reserved.

Change [Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M.

626

Tignor and H.L. Miller (eds.)]. Cambridge University Press, Cambridge, United

627

Kingdom and New York, NY, USA.

Accepted Article

625

628

Christianson J.A., Llewellyn D.J., Dennis E.S. & Wilson I.W. (2010) Comparisons of

629

early transcriptome responses to low-oxygen environments in three dicotyledonous

630

plant species. Plant Signalling and Behaviour 30, 1006–1009.

631 632

Christmann A., Grill E. & Huang J. (2013) Hydraulic signals in long-distance signalling. Current Opinion in Plant Biology 16, 293–300.

633

Colin-Belgrand M., Dreyer E. & Biron P. (1990) Sensitivity of seedlings from different

634

oak species to waterlogging: effects on root growth and mineral nutrition. Annals of

635

Forest Science 48, 193–204.

636

Copolovici L. & Niinemets U. (2010) Flooding induced emissions of volatile signalling

637

compounds in three tree species with differing waterlogging tolerance. Plant, Cell

638

and Environment 33, 1582–1594.

639

Crawford L.A., Bown A.W., Breitkreuz K.E. & Guinel F.C. (1994) The synthesis of

640

gamma-aminobutyric acid in response to treatments reducing cytosolic pH. Plant

641

Physiology 104, 865–871.

642 643

Davies D.D., Grego S. & Kenworthy P. (1974) The control of the production of lactate and ethanol by higher plants. Planta 118, 297–310.

644

de Oliveira V.C. & Joly C.A. (2010) Flooding tolerance of Calophyllum brasiliense

645

Camb. (Clusiaceae): morphological, physiological and growth responses. Trees 24,

646

185–193.

647 648 649 650 651 652

Dennis C.W. & Grindley J. (1984) Probability of waterlogging estimated from historical rainfall records. Agricultural Water Management 6, 397–401.

Dister E. (1983) Zur Hochwassertoleranz von Auenwaldbäumen an lehmigen Standorten. Verhandlungen der Gesellschaft für Ökologie, Mainz Band 10, 325-336.

Drew M.C. (1997) Oxygen deficiency and root metabolism: Injury and acclimation under hypoxia and anoxia. Annual Reviews of Plant Molecular Biology 48, 223-250.

653

Dreyer E. (1994) Compared sensitivity of seedlings from 3 woody species (Quercus robur

654

L., Quercus rubra L. and Fagus sylvatica L.) to waterlogging and associated root

25 This article is protected by copyright. All rights reserved.

hypoxia: effects on water relations and photosynthesis. Annals of Forest Science 51,

656

417-429.

Accepted Article

655

657

Dreyer E., Colin-Belgrand M. & Biron P. (1991) Photosynthesis and shoot water status of

658

seedlings from different oak species submitted to waterlogging. Annals of Forest

659

Science 48, 205-214.

660

Dwyer J.F., Schroeder H.W. & Gobster P.H. (1991) The significance of urban trees and

661

forests: towards a deeper understanding of values. Journal of Arboriculture 17, 276-

662

284.

663

Eastmond P.J., Germain V., Lange P.R., Bryce J.H., Smith S.M. & Graham I.A. (2000)

664

Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle.

665

Proceedings of the National Academy of Science USA 97, 5669–5674.

666

Else M.A., Taylor J.M. & Atkinson C.J. (2006) Anti-transpirant activity in xylem sap from

667

flooded tomato (Lycopersicon esculetum Mill.) plants is not due to pH-mediated

668

redistributions of root- or shoot-sourced ABA. Journal of Experimental Botany 57,

669

3349–3357.

670

Else M.A., Tiekstra A.E., Croker S.J., Davies W.J. & Jackson M.B. (1996) Stomatal

671

closure in flooded tomato plants involves abscisic acid and a chemical unidentified

672

anti-transpirant in xylem sap. Plant Physiology 112, 239-247.

673

Ernst L., Goodger J.Q.D., Alvarez S., Marsh E.L., Berla B., Lockhart E., Jung J., Li P.H.,

674

Bohnert H.J. & Schachtman D.P. (2010) Sulphate as a xylem-borne chemical signal

675

precedes the expression of ABA biosynthetic genes in maize roots. Journal of

676

Experimental Botany 61, 3395-3405.

677

Felle H.H. (2001) pH: signal and messenger in plant cells. Plant Biology 3, 577–591.

678

Fernandez M. D., Pieters A., Donoso C., Herrera C., Tezara W., Rengifo E. & Herrera A.

679

(1999) Seasonal changes in photosynthesis of trees in the flooded forest of the Mapire

680

River. Tree Physiology 19, 79-85.

681

Fernandez M.D. (2006) Changes in photosynthesis and fluorescence in response to

682

flooding in emerged and submerged leaves of Pouteria orinocoensis. Photosynthetica

683

44, 32-38.

26 This article is protected by copyright. All rights reserved.

Ferner E., Rennenberg H. & Kreuzwieser J. (2012) Effect of flooding on C metabolism of

685

flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree

686

Physiology. 32, 135-145.

Accepted Article

684

687

Ferreira C.S., Piedade M.T.F., Junk W.J. & Parolin P. (2007) Floodplain and upland

688

populations of Amazonian Himatanthus sucuuba: effects of flooding on germination,

689

seedling growth and mortality. Environmental and Experimental Botany 60, 477–483.

690

Ferry B., Morneau F., Bontemps J.D., Blanc L. & Freycon V. (2010) Higher treefall rates

691

on slopes and waterlogged soils result in lower stand biomass and productivity in a

692

tropical rain forest. Journal of Ecology 98, 106–116.

693 694

Food and Agriculture Organization (FAO) (2012) State of the World’s Forests 2012. Rome. FAO of the United Nations. 60 p.

695

Forster P., Ramaswamy V., Artaxo P., Berntsen T., Betts R., Fahey D.W., Haywood J.,

696

Lean J., Lowe D.C., Myhre G., Nganga J., Prinn R., Raga G., Schulz M. & Van

697

Dorland R. (2007) Changes in Atmospheric Constituents and in Radiative Forcing.

698

In: Climate Change 2007: The Physical Science Basis. Contribution of Working

699

Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate

700

Change [Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt,

701

M.Tignor and H.L. Miller (eds.)]. Cambridge University Press, Cambridge, United

702

Kingdom and New York, NY, USA.

703

Frei C. (2004) Eidgenössische Technische Hochschule (Zürich) Institut für Atmosphäre

704

und

Klima,

and

MeteoSchweiz,

2004.

Klimazukunft

705

probabilistische Projektion. MeteoSchweiz, Zürich:8.

der

Schweiz-Eine

706

Frei, C., Regina Schöll R., Fukutome S., Schmidli J. & Vidale P.L. (2006) Future change

707

of precipitation extremes in Europe: Intercomparison of scenarios from regional

708

climate

709

doi:10.1029/2005JD005965.

710 711 712 713

models.

Journal

of

Geophysical

Research

111,

D06105,

Gill C. (1970) The flooding tolerance of woody species – a review. Forestry Abstracts 31, 671-688.

Glenz C., Schlaepfer R., Iorgulescu I. & Kienast F. (2006) Flooding tolerance of Central European tree and shrub species. Forest Ecology and Management 235, 1-13.

27 This article is protected by copyright. All rights reserved.

Gout E., Boisson A.-M., Aubert S., Douce R. & Bligny, R. (2001) Origin of the

715

cytoplasmic pH changes during anaerobic stress in higher plant cells. Carbon-13 and

716

phosphorous-31 nuclear magnetic resonance studies. Plant Physiology 125, 912–925.

Accepted Article

714

717

Gravatt D.A. & Kirby C.J. (1998) Patterns of photosynthesis and starch allocation in

718

seedlings of four bottomland hardwood tree species subjected to flooding. Tree

719

Physiology 18, 411-417.

720

Guo X-Y, Huang Z-Y, Xu A-C & Zhang X-S. (2011) A comparison of physiological,

721

morphological and growth responses of 13 hybrid poplar clones to flooding. Forestry

722

84, doi:10.1093/forestry/cpq037.

723 724

Haase K., De Simone O., Junk W.J. & Schmidt W. (2003) Internal oxygen transport in cutting from flood-adapted várzea tree species. Tree Physiology 23, 1069-1076.

725

Haase K. & Rätsch G. (2010) The morphology and anatomy of tree roots and their

726

aeration strategies. In: Junk W.J., Piedade M.T.F., Wittmann F., Schöngart J. &

727

Parolin P. (eds.) Central Amazonian floodplain forests: ecophysiology, biodiversity

728

and sustainable management. Springer, Berlin/Heidelberg/New York. pp. 141-162.

729

Herrera A. (2013). Responses to flooding of plant water relations and leaf gas exchange in

730

tropical tolerant trees of a black-water wetland. Frontiers in Plant Science 4. doi:

731

10.3389/fpls.2013.00106

732

Herschbach C., Mult S., Kreuzwieser J. & Kopriva S. (2005) Influence of anoxia on whole

733

plant sulphur nutrition of flooding tolerant poplar (Populus tremula x P. alba). Plant,

734

Cell and Environment 28, 167-175.

735

Holzinger R., Sandoval-Soto L., Rottenberger S., Crutzen P.J. & Kesselmeier J. (2000)

736

Emissions of volatile organic compounds from Quercus ilex L. measured by Proton

737

Transfer Reaction Mass Spectrometry under different environmental conditions.

738

Journal of Geophysical Research 105, 20573–20579.

739

Hultine K.R., Bush S.E., West A.G. & Ehleringer J.R.. (2007) Population structure,

740

physiology and ecohydrological impacts of dioecious riparian tree species of western

741

North America. Oecologia 154:85–93.

742

Hüve K., Christ M.M., Kleist E., Uerlings R., Niinemets Ü., Walter A. & Wildt J. (2007)

743

Simultaneous growth and emission measurements demonstrate an interactive control

28 This article is protected by copyright. All rights reserved.

of methanol release by leaf expansion and stomata. Journal of Experimental Botany

745

58, 1783–1793.

Accepted Article

744

746

Igamberdiev A.U. & Hill R.D. (2004) Nitrate, NO and haemoglobin in plant adaptation to

747

hypoxia: an alternative to classic fermentation pathways. Journal of Experimental

748

Botany 55, 2473-2482.

749

Igamberdiev A.U., Baron K., Manac’h-Little N., Stoimenova M. & Hill R.D. (2005) The

750

haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on

751

hormone signaling. Annals of Botany 96, 557-564.

752

Iglesias D.J., Lliso I., Tadeo F.R. & Talón M. (2002) Regulation of photosynthesis

753

through source: sink imbalance in citrus is mediated by carbohydrate content in

754

leaves. Physiologia Plantarum 116, 563–572.

755 756

Islam M.A. & MacDonald S.E. (2004) Ecophysiological adaptations of black spruce (Picea marinana) and tamarack (Larix laricina) seedlings to flood. Trees 18, 35-42.

757

Islam M.A., MacDonald S.E. & Zwiazek J.J. (2003) Responses of black spruce (Picea

758

mariana) and tamarack (Larix laricina) to flooding and ethylene. Tree Physiology 23,

759

545–552.

760 761

Jackson M.B. & Colmer T.D. (2005) Response and Adaptation by Plants to Flooding Stress. Annals of Botany 96, 501–505.

762

Jackson M.B. (1982) Ethylene as a growth promoting hormone under flooded conditions.

763

In: Wareing PF, ed. Plant growth regulators. London: Academic Press, 291–301.

764

Jaeger C., Gessler A., Biller S., Rennenberg H. & Kreuzwieser J. (2009) Differences in C

765

metabolism of ash species and provenances as a consequence of root oxygen

766

deprivation by waterlogging. Journal of Experimental Botany 60: 4335-4345.

767 768

Joly C.A. & Crawford R.M.M. (1982) Variation in tolerance and metabolic responses to flooding in some tropical trees. Journal of Experimental Botany 33, 799-809.

769

Kludze H.K., Pezeshki S.R. & DeLaune R.D. (1994) Evaluation of root oxygenation and

770

growth in baldcypress in response to short-term soil hypoxia. Canadian Journal of

771

Forest Research 24, 804–809.

772

Kolb R.M., Rawyler A. & Braendle R. (2002) Parameters affecting the early seedling

773

development of four neotropical trees under oxygen deprivation stress. Annals of

774

Botany 89, 551-558. 29 This article is protected by copyright. All rights reserved.

Kozlowski T.T. (1984a) Extent, causes and impacts of flooding. In Flooding and plant

Accepted Article

775 776

growth. Kozlowski T.T., ed., Academic Press, Orlando, FL, pp 1-7.

777

Kozlowski T.T. (1984b) Plant responses to flooding of soil. Bio Science 34, 162–167.

778

Kozlowski T.T. (1997) Responses of woody plants to flooding and salinity. Tree

779

Physiology Monograph No.1. 29 pages.

780

Kramer K., Vreugdenhil S.J. & van der Werf D.C. (2008) Effects of flooding on the

781

recruitment, damage and mortality of riparian tree species: A field and simulation

782

study on the Rhine floodplain. Forest Ecology and Management 255, 3893–3903.

783

Kreuzwieser J. & Gessler A. (2010) Global climate change and tree nutrition: influence of

784

water availability. Tree Physiology 30, 1221-1234.

785

Kreuzwieser J. & Rennenberg H. (2013) Flooding-driven emissions from trees. In:

786

Biology, controls and models of tree volatile organic compound emissions

787

(Niinemets Ü. & Monson R.K., eds.) Springer series Tree Physiology volume 5, pp.

788

237-252.

789

Kreuzwieser J., Fürniss S. & Rennenberg H. (2002) The effects of flooding on the N

790

metabolism of flood tolerant and sensitive tree species. Plant, Cell and Environment

791

25, 1039-1050.

792

Kreuzwieser J., Harren F.J.M., Laarhoven L.J.J.,

Boamfa I., te Lintel-Hekkert S.,

793

Scheerer U., Hüglin C. & Rennenberg H. (2001) Acetaldehyde emission by the

794

leaves of trees - correlation with physiological and environmental parameters.

795

Physiologia Plantarum 113, 41–49.

796

Kreuzwieser J., Hauberg J., Howell K.A., Carroll A., Rennenberg H., Millar A.H. &

797

Whelan J. (2009) Differential response of Grey poplar leaves and roots underpins

798

stress adaptation during hypoxia. Plant Physiology, 149, 461-473.

799

Kreuzwieser J., Scheerer U. & Rennenberg H. (1999) Metabolic origin of acetaldehyde

800

emitted by poplar (Populus tremula x P. alba) trees. Journal of Experimental Botany

801

50, 757-765.

802

Kundzewicz Z.W. (2005) Climate change and floods. WMO Bulletin 55, 170-173.

803

Kundzewicz Z.W., Ulbrich U., Brücher T., Gracyk D., Krüger A., Leckebusch G., Menzel

804

L., Pinskwar I., Radziejewski M. & Szwed M. (2005) Summer floods in central

805

Europe – climate change track? Natural Hazards 36, 165-189. 30 This article is protected by copyright. All rights reserved.

Laur J. & Hacke U.G. (2013) Transpirational demand affects aquaporin expression in

Accepted Article

806 807

poplar roots. Journal of Experimental Botany 64, 2283-2293.

808

LeProvost G., Sulmon C., Frigerio J.M., Bodénès C., Kremer A. & Plomion C. (2012)

809

Role of waterlogging-responsive genes in shaping interspecific differentiation

810

between two sympatric oak species. Tree Physiology 32, 119-134.

811

Li S., Pezeshki S.R. & Shields F.D. (2006) Partial flooding enhances aeration in

812

adventitious roots of black willow (Salix nigra) cuttings. Journal of Plant Physiology

813

163, 619-628.

814

Lucassen E.C.H.E.T., Bobbink R., Smolders A.J.P., van der Ven P.J.M., Lamers L.P.M. &

815

Roelofs J.G.M. (2002) Interactive effects of low pH and high ammonium levels

816

responsible for the decline of Cirsium dissectum (L.) Hill. Plant Ecology 165, 45 – 52.

817

Lucassen E.C.H.E.T., Smolders A.J.P. & Roelofs J.G.M. (2000) Increased ground-water

818

levels cause iron toxicity in Glyceria fluitans (L.). Aquatic Botany 66, 321 – 327.

819

Martínez-Alcántara1 B., Jover S., Quinones A., Forner-Giner M.A., Rodríguez-Gamir J.,

820

Legaz F., Primo-Millo E. & Iglesias D.J. (2012) Flooding affects uptake and

821

distribution of carbon and nitrogen in citrus seedlings. Journal of Plant Physiology

822

169, 1150-1157.

823 824 825 826

McClean J. (2000) Wetter is not always better - Flood Tolerance of Woody Species. Technical Note #52 from Watershed Protection Techniques. 1, 208-210.

McKee W.H. & McKevlin M.R. (1993) Geochemical processes and nutrient uptake by plants in hydric soils. Environmental Toxicology and Chemistry 12, 2197–2207.

827

Merchant A., Peuke A.D., Keitel C., Macfarlane C., Warren C.R. & Adams M.A. (2010)

828

Phloem sap and leaf δ13C, carbohydrates, and amino acid concentrations in

829

Eucalyptus globulus change systematically according to flooding and water deficit

830

treatment. Journal of Experimental Botany 61, 1785-1793.

831

Mielke M.S., De Almeida A.A.F., Gomes F.P., Mangabeira P.A.O. & Silva D.D.C. (2005)

832

Effects of soil flooding on leaf gas exchange and growth of two neotropical pioneer

833

tree species. New Forests 29, 161–168.

834

Mustroph A., Lee S.C., Oosumi T., Zanetti M.E., Yang H., Ma K., Yaghoubi-Masihi A.,

835

Fukao T. & Bailey-Serres J. (2010) Cross-kingdom comparison of transcriptomic

31 This article is protected by copyright. All rights reserved.

adjustments to low-oxygen stress highlights conserved and plant-specific responses.

837

Plant Physiology 152: 1484–1500.

Accepted Article

836

838

Narsai R., Rocha M., Peter Geigenberger P., James Whelan J. & van Dongen J.T. (2011)

839

Comparative analysis between plant species of transcriptional and metabolic

840

responses to hypoxia. New Phytologist 190, 472-487.

841 842

Nealle D.B. & Kremer A. (2011) Forest tree genomics: growing resources and applications. Nature Reviews Genetics 12, 111-122.

843

Neatrour M.A., Jones R.H. & Golladay S.W. (2007) Response of three floodplain tree

844

species to spatial heterogeneity in soil oxygen and nutrients. Journal of Ecology 95,

845

1274–1283.

846

Nicolás E., Torrecillas A., Dell’Amico J., Alarcón J. (2005) The effect of short-term

847

flooding on the sap flow, gas exchange and hydraulic conductivity of young apricot

848

trees. Trees-Structure and Function 19, 51–57.

849

Nielsen J.L., Rood S.B., Pearce D.W., Letts M.G. & Jiskoot H. (2010) Streamside trees:

850

responses of male, female and hybrid cottonwoods to flooding. Tree Physiology 30,

851

1479-1488.

852

Niinemets Ü. & Valladares F. (2006) Tolerance to shade, drought, and waterlogging of

853

temperate northern hemisphere trees and shrubs. Ecological Monographs 76, 521-

854

547.

855

Nunez-Elisea R., Schaffer B., Fisher J.B., Colls A.M. & Crane J.H. (1999) Influence of

856

flooding on net CO2 assimilation, growth and stem anatomy of Annona species.

857

Annals of Botany 84, 771-80.

858 859 860 861 862 863

Ojeda M., Schaffer B. & Davies F.S. (2004) Flooding, root temperature, physiology and growth of two Annona species. Tree Physiology 24, 1019 –1025.

Ortuño M.F., Alarcón J.J., Nicolás E. & Torrecillas A. (2007) Water status indicators of lemon trees in response to flooding and recovery. Biologia Plantarum 51, 292-296.

Pagnussat G.C., Simontacchi M., Puntarulo S. & Lamattina L. (2002) Nitric oxide is required for root organogenesis. Plant Physiology 129, 954–956.

864

Pagnussat G.C., Lanteri M.L., Lombardo M.C. & Lamattina L. (2004) Nitric oxide

865

mediates the indole acetic acid induction activation of a mitogen-activated protein

32 This article is protected by copyright. All rights reserved.

kinase cascade involved in adventitious root development. Plant Physiology 135, 279-

867

286.

Accepted Article

866

868 869

Palmer T.N. & Räisänen J. (2002) Quantifying the risk of extreme seasonal precipitation events in a changing climate. Nature 415, 512-514.

870

Parelle J., Brendel O., Bodenes C., Berveiller D., Dizengremel P., Jolivet Y. & Dreyer E.

871

(2006) Differences in morphological and physiological responses to water-logging

872

between two sympatric oak species (Quercus petraea [Matt.] Liebl., Quercus robur

873

L.). Annals of Forest Science 63, 849–859.

874

Parent C., Berger A., Folzer H., Dat J.F., Crèvecoeur M., Badot P.-M. & Capelli N. (2008)

875

A novel nonsymbiotic hemoglobin from oak: cellular and tissue specificity of gene

876

expression. New Phytologist 177, 142-154.

877

Parent C., Crèvecoeur M., Capelli N. & Dat J.F. (2011) Contrasting growth and adaptive

878

responses of two oak species to flooding stress: role of non-symbiotic haemoglobin.

879

Plant, Cell and Environment 34, 1113-1126.

880

Parent C., Crèvecoeur M., Capelli N. & Dat J.F. (2011) Contrasting growth and adaptive

881

responses of two oak species to flooding stress: role of non-symbiotic haemoglobin.

882

Plant, Cell and Environment 34, 1113–1126.

883

Parolin P. & Wittmann F. (2010) Struggle in the flood: tree responses to flooding stress in

884

four tropical floodplain systems. AoB Plants 2010: doi: 10.1093/aobpla/plq003.

885

Parolin P. (2001) Morphological and physiological adjustments to waterlogging and

886

drought in seedlings of Amazonian floodplain trees. Oecologia 128, 326–335.

887

Parolin P., De Simone O., Haase K., Waldhoff D., Rottenberger S., Kuhn U., Kesselmeier

888

J., Kleiss B., Schmidt W., Piedade M.T.F. & Junk W.J. (2004) Central Amazonian

889

Floodplain Forest: Tree Adaptations in a Pulsing System. The Botanical Review 70,

890

357–380.

891

Parolin P., Lucas C., Piedade M. T. F. & Wittmann F. (2010) Drought responses of

892

extremely flood-tolerant trees of Amazonian floodplains. Annals of Botany 105, 129–

893

139.

894

Pezeshki S.R. & Chambers J.L. (1985a) Stomatal and photosynthetic response of sweet

895

gum (Liquidambar styraciflua) to flooding. Canadian Journal of Forest Research 15,

896

371--375. 33

This article is protected by copyright. All rights reserved.

Pezeshki S.R. & Chambers J.L. (1985b) Responses of cherry bark oak (Quercus falcata

898

var. pagodaefolia) seedlings to short-term flooding. Forest Sciences 31, 760--771.

899

Pezeshki S.R. (1994) Responses of baldcypress (Taxodium distichum) seedlings to

900

hypoxia: Leaf protein content, ribulose-1,5-bisphosphate carboxylase/oxygenase

901

activity and photosynthesis. Photosynthetica 30, 59-68.

Accepted Article

897

902

Pezeshki S.R., & Chambers J.C. (1986) Variation in flood-induced stomatal and

903

photosynthetic responses of three bottomland tree species. Forest Sciences 32, 914-

904

923.

905

Pezeshki S.R., Pardue J.H. & DeLaune R.D. (1996) Leaf gas exchange and growth of

906

flood-tolerant and flood-sensitive tree species under low soil redox conditions. Tree

907

Physiology 16, 452-458.

908

Pezeshki, S.R., Pardue, J.H. & DeLaune, R.D. (1996) Leaf gas exchange and growth of

909

flood-tolerant and flood-sensitive tree species under low soil redox conditions. Tree

910

Physiology 16, 453-458.

911 912 913 914

Ponnamperuma F.N. (1972) The chemistry of submerged soils. Advances in Agronomy 24, 29-95.

Ponnamperuma F.N. (1984) Effects of flooding on soils. Chapter 2. In Flooding and plant growth. (Kozlowski, T.T., ed.), Orlando: Academic Press, pp. 9-193.

915

Porth I., Koch M., Berenyi M., Burg A. & Burg K. (2005) Identification of adaptation-

916

specific differences in mRNA expression of sessile and pedunculate oak based on

917

osmotic-stress-induced genes. Tree Physiology 25, 1317–1329.

918

Pradet A. & Bomsel J.L. (1978) Energy metabolism in plants under hypoxia and anoxia.

919

In Plant life in anaerobic environments. Hook D.D. & Crawford R.M.M., eds. Ann

920

Arbor Science Publishers Inc., Ann Arbor, pp. 89-118.

921 922

Reece C.F. & Riha S.J. (1991) Role of root systems of Eastern larch and White spruce in response to flooding. Plant, Cell and Environment 14, 229-234.

923

Rengifo E., Tezara W. & Herrera A. (2005) Water relations, chlorophyll a fluorescence

924

and carbohydrate contents in trees of a tropical forest in response to flood.

925

Photosynthetica 43, 203-210.

34 This article is protected by copyright. All rights reserved.

Roberts J.K.M., Callis J., Wemmer D., Walbot V. & Jardetzky O. (1984) Mechanism of

927

cytoplasmic pH regulation in hypoxic maize root tips and its role in survival under

928

hypoxia. Proceeding of the National Academy of Science USA 81, 3379–3383.

929

Rodríguez-Gamir J., Ancillo G., González-Mas M.C., Primo-Millo E., Iglesias D.J. &

930

Forner-Giner M.A. (2011) Root signalling and modulation of stomatal closure in

931

flooded citrus seedlings. Plant Physiology and Biochemistry 49, 636–645.

Accepted Article

926

932

Ruiz-Sánchez M.C., Domingo R., Morales D. & Torrecillas A. (1996).Water relations of

933

Fino lemon plants on two rootstocks under flooded conditions. Plant Sciences 120,

934

119–125.

935

Schaffrath J. (2000) Auswirkungen des extremen Sommerhochwassers des Jahres 1997

936

auf die Gehölzvegetation in der Oderaue bei Frankfurt (O). Naturschutz und

937

Landschaftspflege in Brandenburg 9, 4-13.

938

Schmull M. & Thomas F.M. (2000) Morphological and physiological reactions of young

939

deciduous trees (Quercus robur L., Q. petraea [Matt.] Liebl., Fagus sylvatica L.) to

940

waterlogging. Plant and Soil 225, 227-242.

941

Shimamura S., Yamamoto R., Nakamura T., Shimada S. & Komatsu S. (2010) Stem

942

hypertrophic lenticels and secondary aerenchyma enable oxygen transport to roots of

943

soybean in flooded soil. Annals of Botany 106, 277-284.

944 945 946 947 948 949 950 951

Siebel H.N. & Blom C.W.P.M. (1998) Effects of irregular flooding on the establishment of tree species. Acta Botanica Neerlandica 47, 231–240.

Snowden R.E. &Wheeler B.D. (1993) Iron toxicity to fen plant species. Journal of Ecology 81, 35 – 46.

Späth V. (1988) Zur Hochwassertoleranz von Auenwaldbäumen. Natur und Landschaft H.7/8, S.312-315.

Späth V. (2002) Hochwassertoleranz von Waldbäumen in der Rheinaue. Allgemeine Forstzeitschrift/ Der Wald 15, 807-810.

952

Steffens B., Wang J. & Sauter M. (2006) Interactions between ethylene, gibberelin and

953

abscisic acid regulate emergence and growth rate of adventitious roots in deepwater

954

rice. Planta 223, 604-612.

35 This article is protected by copyright. All rights reserved.

Steffens B., Steffen-Heins A. & Sauter M. (2013) Reactive oxygen species mediate

956

growth and death in submerged plants. Frontiers in Plant Science 4, doi:

957

10.3389/fpls.2013.00179.

Accepted Article

955

958 959

Striker G.G. (2012) Flooding stress on plants: anatomical, morphological and physiological responses. Mworia J. (ed.), ISBN 978-953-51-0355-4.

960

Syvertsen J.P., Zablotowicz R.M. & Smith Jr M.L. (1983) Soil temperature and flooding

961

effects on two species of citrus. I. Plant growth and hydraulic conductivity. Plant

962

and Soil 72:3–12.

963

The Columbia Electronic Encyclopedia, 6th ed. Copyright © 2012, Columbia University

964

Press.

965

forests.html#ixzz2hryOK2Ua

http://www.infoplease.com/encyclopedia/science/forest-the-importance-

966

Tournaire-Roux C., Sutka M., Javot H., Gout E., Gerbeau P., Luu D.T., Bligny R. &

967

Maurel C. (2003) Cytosolic pH regulates root water transport during anoxic stress

968

through gating of aquaporins. Nature 425, 393–397.

969 970

Tuskan G.A., DiFazio S. & Teichmann T. (2003) Poplar genomics is getting popular: The impact of the poplar genome project on tree research. Plant Biology 5, 1-3.

971

Tuskan G.A., DiFazio S. Jansson S., Bohlmann J., Grigoriev I., Hellsten U., ... Rokhsar D.

972

(2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).

973

Science 313, 1596–1604.

974 975

Unger I.M., Kennedy A.C. & Muzika R.-M. (2009) Flooding effects on soil microbial communities. Applied Soil Ecology 42, 1–8.

976

Visser E., Nabben R., Blom C. & Voesenek L. (1997) Elongation by primary lateral roots

977

and adventitious roots during conditions of hypoxia and high ethylene

978

concentrations. Plant, Cell and Environment 20, 647-653.

979

Vreugdenhil S.J., Kramer K. & Pelsma T. (2006) Effects of flooding duration, -frequency

980

and -depth on the presence of saplings of six woody species in north-west Europe.

981

Forest Ecology and Management 236, 47-55.

982 983 984 985

Vu J. & Yelenosky G. (1991) Photosynthetic responses of citrus trees to soil flooding. Physiologia Plantarum 81, 7–14.

Vu J.C.V. & Yelenoski G. (2006) Photosynthetic response of citrus trees to soil flooding. Physiologia Plantarum 81, 7-14. 36 This article is protected by copyright. All rights reserved.

Yamanoshita T., Masumori M., Yagi H. & Kojima K. (2005) Effects of flooding on

987

downstream processes of glycolysis and fermentation in roots of Melaleuca cajuputi

988

seedlings. Journal of Forest Research 10, 199-204.

Accepted Article

986

989

Ye Y., Tam N.F.Y., Wong Y.S. & Lu C.Y. (2003) Growth and physiological responses of

990

two mangrove species (Bruguiera gmynorrhiza and Kandelia candel) to

991

waterlogging. Environmental and Experimental Botany 49, 209-221.

992 993

37 This article is protected by copyright. All rights reserved.

Figure legends

996

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

997

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

998

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

Accepted Article

994 995

999

1000

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

1001

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

1002

waterlogging and transcript abundances were determined by microarray analysis. Shown

1003

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

1004

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

1005

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

1006 1007

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

1008

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

1009

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

1010

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

1011

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

1012

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

1013

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

1014

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

1015

closure of the stomata.

1016 1017

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

1018

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

1019

roots, phloem and xylem sap were determined in plants waterlogged for 7 days and in non38 This article is protected by copyright. All rights reserved.

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

1021

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

1022

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

1023

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

1024

indicate the 100 % levels of control plants.

Accepted Article

1020

1025 1026

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

1027

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

1028

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

1029

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

1030

Student’s t’test are indicated (n=4).

1031 1032

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

1033

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

1034

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

1035

metabolites with reduced abundance.

1036

39 This article is protected by copyright. All rights reserved.

Tables

1040

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

1041

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

1042

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

1043

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

1044

Armbruster et al. (2006).

Accepted Article

1037 1038 1039

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

Species

maximum duration

dieback expected

without damages (days)

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

40 This article is protected by copyright. All rights reserved.

Molecular and physiological responses of trees to waterlogging stress.

One major effect of global climate change will be altered precipitation patterns in many regions of the world. This will cause a higher probability of...
1MB Sizes 3 Downloads 3 Views