Molecular and physiological responses of trees to waterlogging stress1
Accepted Article
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Jürgen Kreuzwieser1*, Heinz Rennenberg1
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Freiburg; Georges-Köhler-Allee 53; 79110 Freiburg, Germany
Institute of Forest Science, Chair of Tree Physiology, Albert-Ludwigs-Universität
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*corresponding author and present address:
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Institute of Forest Science, Chair of Tree Physiology, Albert-Ludwigs-Universität
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Freiburg; Georges-Köhler-Allee 53; 79110 Freiburg, Germany
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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
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One major effect of global climate change will be altered precipitation patterns in many
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regions of the world. This will cause a higher probability of long-term waterlogging in
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winter/spring and flash floods in summer due to extreme rainfall events. Particularly trees
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not adapted at their natural site to such waterlogging stress can be impaired. Despite the
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enormous economic, ecological and social importance of forest ecosystems, the effect of
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waterlogging on trees is far less understood than the effect on many crops or the model
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plant Arabidopsis. There is only a handful of studies available investigating the
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transcriptome and metabolome of waterlogged trees. Main physiological responses of trees
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to waterlogging include the stimulation of fermentative pathways and an accelerated
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glycolytic flux. Many energy consuming, anabolic processes are slowed down to
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overcome the energy crisis mediated by waterlogging. A crucial feature of waterlogging
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tolerance is the steady supply of glycolysis with carbohydrates, particularly in the roots;
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stress sensitive trees fail to maintain sufficient carbohydrate availability resulting in the
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dieback of the stressed tissues. The present review summarizes physiological and
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molecular features of waterlogging tolerance of trees; the focus is on carbon metabolism in
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both, leaves and roots of trees.
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Keywords: waterlogging, hypoxia, trees, carbon metabolism, nitrogen metabolism,
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transcriptome, metabolome.
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2 This article is protected by copyright. All rights reserved.
Accepted Article
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Introduction
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The concentrations of the trace gases carbon dioxide, methane and nitrous oxide in the
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atmosphere are continuously rising due to anthropogenic activity. Between the pre-
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industrial era and 2005 they increased by 36% (CO2; from 280 to 379 ppm), 148% (CH4;
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from 715 to 1774 ppb) and 18% (N2O; from 270 to 319 ppb) (Forster et al., 2007).
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Consequently, the global air temperatures considerably increased between 1850 and 2007
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and will further increase in the future (Christensen et al., 2007). In Central Europe, for
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example, a temperature rise in the range of 1.9-7.0°C is expected in the next 50 years
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(Frei, 2004). Such temperature elevation will strongly affect the global hydrological cycle.
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Like in North and Central Europe, annual precipitation in East Africa, Northern, East,
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South and Southeast Asia, Canada and Northeast USA is likely to increase whereas it will
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decrease in Central America, Southwest USA, Mediterranean Europe, and Central Asia
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(Christensen et al., 2007). However, precipitation will not change equally over the year; in
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Central Europe, winter precipitation is predicted to increase in the future, but summer
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precipitation will be considerably lower causing a higher possibility of drought periods
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during the summer months (Frei et al., 2006). On the other hand, most model projections
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forecast increased extreme precipitation events despite decreased mean summer
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precipitation (Palmer and Räisänen, 2002; Christensen and Christensen, 2003). Because of
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such intense rainfall events, terrestrial ecosystems in the concerned regions will
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experience more and probably longer waterlogging periods during winter and spring and
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more extreme short-term flooding events during summer (Christensen and Christensen,
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2003; Kundzewicz et al., 2005; Kundzewicz, 2006) particularly on compacted and / or
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heavy, clay-rich soils where drainage is inhibited (Dennis and Grindley, 1983; Kozlowski,
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1984).
3 This article is protected by copyright. All rights reserved.
Accepted Article
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Soil processes
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Flooding (i.e. water standing above soil level) and waterlogging (i.e. only the soil is
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flooded) lead to a deprivation of oxygen in the soil because the floodwater entering the
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soil removes oxygen rich air from soil pores. In addition, the ca. 10.000 times higher
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diffusion resistance of oxygen in water than in air leads to an inhibited supply of the soil
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with oxygen in water saturated soils (Armstrong, 1979). Microbial and plant activities
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quickly consume the remaining oxygen leading either to hypoxic (low oxygen
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concentrations: mitochondrial respiration reduced; fermentation takes place) or anoxic
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(oxygen absent: energy gain by fermentation only) conditions (Pradet and Bomsel, 1978).
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Due to the lack of oxygen, soil physico-chemical properties such as pH and redox
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potential strongly change during waterlogging (Pezeshki and Chambers, 1985a; 1985b).
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The diminished gas diffusion velocity between the soil and the atmosphere causes an
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accumulation of gaseous compounds in the waterlogged soil such as the plant hormone
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ethylene or other metabolic products like carbon dioxide (Jackson, 1982). Oxygen
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shortage further affects microbial communities in the soil (Unger et al., 2009) and
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numerous microbial processes, which eventually cause changes in soil chemical
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composition. This can lead to a reduced abundance of oxidised nutrients (e.g. NO3-, SO42-,
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Fe3+) and elevated levels of reduced compounds such as Mn2+, Fe2+, H2S, NH4+, and
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organic compounds (alkanes, acids, carbonyls, etc) which can be toxic for plants
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(Ponnamperuma, 1972; 1984; McKee and McKevlin, 1993; Snowden and Wheeler, 1993;
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Lucassen et al., 2000; 2002; Jackson and Colmer, 2005). The velocity and extent of the
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changes of soil physico-chemical properties depends on soil type, the duration of the
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waterlogging event, prevailing environmental conditions (such as temperature) and the
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type of flooding or waterlogging (Drew, 1997; Kozlowski, 1997). Stagnant conditions
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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
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floodwater.
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Effects on trees
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About 31% of the terrestrial earth surface, i.e. around 4 billion hectares, is covered by
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forest ecosystems with Latin America (sharing 24% of the world’s forest), former Soviet
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Union (21%), Africa (20%), and North-America (16%) as the regions with the largest
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forested areas (FAO, 2012; The Columbia Electronic Encyclopedia, 2012). It is obvious
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that forests fulfil a plethora of essential ecological (e.g. maintenance of biodiversity,
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involvement in biogeochemical cycles of water, carbon and nitrogen), economic (e.g.
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timber and other natural resources, energy source) and social (e.g. recreation) functions. In
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addition, trees are of particular importance in urban environments as street and park
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vegetation (Dwyer et al., 1991) or in orchards and as bioenergy source from fast growing
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plantations, the latter covering 187 million hectares in 2000, with a strongly increasing
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trend (Carnus et al., 2006).
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Because major parts of the landscapes covered by trees/forests are assumed to be more
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strongly exposed to waterlogging and flooding in the future, plant mechanisms to cope
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with such stress conditions are of particular interest. However, today the knowledge on
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physiological and molecular aspects of flooding/waterlogging tolerance in trees is far
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behind that of herbaceous species (Kreuzwieser et al., 2009). This is due to the fact that
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studying trees provides particular challenges. Trees are characterised by longevity, making
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it difficult to work with adult trees under environmentally controlled conditions. The
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combination of long lifetime and seasonality complicates many plant internal processes:
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alternating phases of dormancy and growth over the growing season need well-adjusted
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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
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orchestrated and regulated long-distance transport processes in phloem and xylem.
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Storage, mobilization, and long-distance transport can all be affected in different ways by
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environmental factors such as soil oxygen deficiency. The lack of knowledge on
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mechanisms of environmental control of these processes in trees compared to crops and
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model plants such as Arabidopsis or rice becomes particularly evident at the molecular
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level (Kreuzwieser et al., 2009; Mustroph et al., 2010; Christianson et al., 2010; Narsai et
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al., 2011). This is partially due to the limited availability of relevant tools and techniques.
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For example, the first commercially distributed microarray for a tree species became
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available for poplar only in 2006, after the genome of Populus trichocarpa has been
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sequenced (Tuskan et al., 2006). As nicely reviewed by Neale and Kremer (2011), forest
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tree genomics made great progress in recent years as modern sequencing technologies
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(next generation sequencing, NGS) considerably facilitate tree genome studies and
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transcriptome profiling (RNA-seq). This certainly will allow faster progress of research on
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trees in near future.
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As aerobic organisms, trees depend on a steady supply with oxygen to all living cells, and
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interruption from oxygen availability therefore causes disturbance of plant metabolism
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(Drew, 1997; Bailey-Serres and Voesenek, 2008). Depending on the tolerance of soil
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oxygen depletion, this can cause dysfunction of processes at the cellular level, eventually
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leading to visible damages. Flooding and waterlogging tolerance and the occurrence of
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injuries is strongly species-dependent (Table 1; Gill, 1970; Kozlowski, 1982; 1997;
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McClean, 2000; Glenz et al., 2006; Niinemets and Valladares, 2006; Kramer et al., 2008;
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Parolin et al., 2004; 2010; Ferner et al., 2012). Highly adapted species survive
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waterlogging periods up to some months without any injuries (Table 1), but less tolerant
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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
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Kozlowski, 1997) and shoot growth (e.g. Colin-Belgrand et al., 1990; Pezeshki et al.,
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1996; Parolin, 2001; Ye et al., 2003; Alaoui-Sossé et al., 2005; Mielke et al., 2005; Parelle
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et al., 2006; Neatrour et al., 2007; Ferreira et al., 2007; de Oliveira and Joly, 2010; Ferry et
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al., 2010; Guo et al., 2011), typical symptoms of soil oxygen shortage in sensitive trees are
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leaf necrosis and shedding, bark damages, elevated susceptibility to fungal and insect
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pathogens, or dieback of the whole tree (Kozlowski, 1997; Parolin, 2001; Kreuzwieser et
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al., 2004; Parolin and Wittmann, 2010). The extent of damages depends on the type
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(stagnant or moving water), duration and height of flooding, the environmental conditions
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during the stress event (e.g. air, water and soil temperature, solar radiation), the season,
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but also on a wide range of plant specific features (Kozlowski, 1997; Vreugdenhil et al.,
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2006). The development of damages depends to a high degree on the species considered
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but also on the ecotype of a given species (Jaeger et al., 2009; Guo et al. 2011), the tree’s
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age, size and developmental stage (Kozlowski, 1997; Siebel and Blom, 1998; Glenz et al.,
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2006). It is generally observed that adult trees tolerate waterlogging and flooding better
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than seedlings of the same species (Table 2) (Gill, 1970; Siebel and Blom, 1998). Recent
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studies even indicated that the sex of a tree plays a role in flooding tolerance of dioecious
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species such as willow and poplar. There is clear evidence that female willow and poplar
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trees are more tolerant against the stress than male trees explaining the spatial segregation
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of the sexes with higher abundance of females in low-elevation zones of riparian forests
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(Hultine et al. 2007; Nielsen et al. 2010). Nielsen et al. (2010) therefore proposed the
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concept of “strategic positioning” where the seed-producing female trees are better
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adapted to sites which are more often flooded and where seedling recruitment usually
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occurs.
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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
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broad range of adaptive strategies to cope with the stress mediated by this exposure. Most
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wetland species apply avoidance strategies based on morphological-anatomical features.
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Such adaptations have been reviewed for woody species by Kozlowski (1997) and Glenz
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et al. (2006), and are therefore only briefly mentioned here. Many flood tolerant species
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develop hypertrophied lenticels at the stem base in response to flooding (compilations of
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tree species are given by Kozlowski (1997) and Glenz et al. (2006)). These organs
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penetrate the relatively strongly gas resistant phellogen layer of the trees, enabling gas
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exchange between stem and environment. Thus, hypertrophied lenticels allow oxygen
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uptake into the plant, but they are also assumed to contribute to the release of gaseous
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compounds (carbon dioxide, acetaldehyde, ethanol) out of the stem into the atmosphere
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(Li et al., 2006; Shimamura et al., 2010). Another feature often associated with the
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appearance of hypertrophied lenticels is the formation of adventitious roots (Glenz et al.,
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2006) (Fig. 1). Such roots are produced when the primary root system of the tree is
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impaired because of soil oxygen deficiency. Adventitious roots possess a high portion of
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intercellular spaces facilitating longitudinal oxygen transport. In a studies with Central
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Amazonian trees such as Salix martiana and Tabernaemontana juruana, it was
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demonstrated that the main entry point of atmospheric oxygen were gas-permeable pores
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in the stem near the origin of the adventitious roots (Haase et al., 2003; Haase & Rätsch,
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2010). Uptake of oxygen seems also to be possible along the root if it is growing at the
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water surface being in contact with the atmosphere (Haase et al., 2003). Such oxygen
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uptake is required for the maintenance of mitochondrial respiration; it further allows radial
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oxygen loss (ROL) from the roots which contributes to the oxidation of the rhizosphere
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(Kludze et al., 1994; Li et al., 2006). Further important functions of adventitious roots are
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absorption of water and nutrients as a replacement of the damaged primary root system
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(Barlow, 1986; Calvo-Polanco et al., 2012). Impressive examples for adventitious roots
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are the prop roots of Rhizophora and the pneumatophores of Avicennia, both inhabitants of
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mangrove ecosystems (Baylis, 1950; Allaway et al., 2001; Aziz and Khan, 2001) (Fig. 1).
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The formation of aerenchyma is a third adaptation of plants to cope with oxygen
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deficiency in the soil (Kozlowski, 1997; Kludze et al., 2004). The formation of lacunae air
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spaces enhances the porosity of the root tissue facilitating oxygen diffusion within roots
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and they are likely to contribute to the export of phytotoxic volatile metabolites
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(acetaldehyde, ethanol) from the plant (Visser et al., 1997). The formation of
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hypertrophied lenticels, adventitious roots and aerenchyma depends on the accumulation
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of ethylene in plant tissue (Steffens et al., 2006; Bailey-Serres et al., 2012). Plant internal
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concentrations of ethylene increase, if floodwater surrounding the plant inhibits the
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diffusive loss of this volatile plant hormone into the atmosphere, and if – at the same time
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– ethylene biosynthesis proceeds (Bailey-Serres and Voesenek, 2008). In addition to
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ethylene, reactive oxygen species (ROS) are involved as signalling intermediates in this
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ethylene-controlled adaptation (Steffens et al., 2013). Other components also known to
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play a role in adventitious root formation are the auxin indole acetic acid (IAA) and NO
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(see Bailey-Serres et al., 2012). IAA abundance induces a transient accumulation of NO
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(Pagnussat et al., 2002) which in turn activates a MAPK signalling cascade eventually
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leading to adventitious root formation (Pagnussat et al. 2004). Such knowledge has been
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gained mainly by studies with herbaceous plants; the mechanisms of hypoxia induced
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adventitious root formation in trees and particularly the interplay of the different
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components are still widely unknown.
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Physiological effects of waterlogging on trees
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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
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gas exchange, particularly net CO2 assimilation. It is a general phenomenon that
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assimilation rates tend to decrease during periods of waterlogging stress as observed in
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trees of tropical (Nunez-Elisea et al., 1999; Fernandez et al., 1999; Ojeda et al., 2004;
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Fernandez, 2006; Herrera, 2013) and temperate (Pezeshki and Chambers 1985a; 1985b;
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1986; Pezeshki, 1994; Pezeshki et al., 1996, Dreyer et al., 1991; Reece and Riha, 1991;
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Beckman et al., 1992; Ewing, 1996; Gravatt and Kirkby, 1998; Jaeger et al., 2009; Ferner
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et al., 2012) ecosystems. The extent of this decrease depends on the species’ tolerance to
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soil oxygen deficiency. Highly tolerant trees maintain rates of photosynthesis at a
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relatively high level or are even unaffected by the stress, whereas net CO 2 assimilation of
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less tolerant or sensitive species is strongly reduced (Dreyer, 1994; Wagner and Dreyer,
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1997; Graves et al., 2002; Vu and Yelenosky, 2006; Jaeger et al., 2009; Parent et al., 2011;
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Ferner et al., 2012). In addition, as seen in flood tolerant tree species of the Amazonian
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floodplain, rates of photosynthesis can completely recover or even increase during long-
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term periods of soil oxygen deficiency; such recovery often coincides with morpho-
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anatomical changes like the appearance of hypertrophied lenticels and/or adventitious
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roots (Herrera, 2013).
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The reasons for inhibited photosynthesis of waterlogged trees are still not completely
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understood. There are strong hints that both, non-stomatal and stomatal limitations are
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involved. Non-stomatal limitation is associated with lowered pigment concentrations in
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leaves of waterlogged trees (Kreuzwieser et al., 2002; Ojeda et al., 2004), decreased
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activity (Vu and Yelenosky, 2006) and abundance (Herrera, 2013) of ribulose-1,5-
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bisphosphate carboxylase/oxygenase (Rubisco) and accumulation of soluble carbohydrates
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which might cause feedback inhibition of photosynthesis (Iglesias et al., 2002; Islam and
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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
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been discussed as the main reason for reduced photosynthesis in numerous trees (Reece
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and Riha, 1991; Gravatt and Kirkby, 1998, Pezeshki et al., 1996; Schmull and Thomas,
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2000; Rodríguez-Gamir et al., 2011; Ferner et al., 2012). Although intensively studied, the
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mechanisms leading to reduced stomatal conductance during periods of waterlogging is far
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from being understood. It is assumed to be connected to reduced root hydraulic
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conductivity and subsequently lowered water absorption by the roots and/or caused by
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chemical signals, which are transported from waterlogged roots to the shoot via the
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transpiration stream. The nature of potential signalling compounds responsible for
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stomatal closure is still not known (Else et al., 1996; 2006; Aroca et al., 2011). The
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involvement of abscisic acid (ABA) transport in the xylem has been proposed (Jackson et
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al., 2003; Herrera, 2013) but is still a matter of debate, particularly since some reports
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clearly excluded root-to-shoot ABA transport (Else et al., 2006; Rodríguez-Gamir et al.,
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2011). Waterlogging induced changes in the pH of the xylem sap have also been proposed
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as a long-distance signal. However, there does not seem to be a consistent plant response
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as both alkalisation (Else et al., 2006) and acidification (Rodríguez-Gamir et al., 2011) of
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the xylem sap was observed in waterlogged plants. Recently, mobilization of root stored
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sulphate and its root-to-shoot transport have been proposed to mediate stomatal closure in
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response to drought (Ernst et al., 2010); whether these processes are also involved in
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stomatal closure in response to waterlogging remains to be elucidated.
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Reduced root hydraulic conductance
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Waterlogging induced reduction of stomatal conductance is often associated with
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diminished root hydraulic conductance as demonstrated in many flood tolerant and
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sensitive tree species (Syvertsen et al., 1983; Dreyer, 1994; Schmull and Thomas, 2000;
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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
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of damage of their root system and/or lower root biomass due to impaired growth
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(Schmull and Thomas, 2000). Water absorption by roots is at least partially (ca. 50%)
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mediated by root water channels (aquaporins) of the plasma membrane intrinsic protein
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(PIP) family (Tournaire-Roux et al., 2003; McElrone et al., 2007). It can therefore be
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assumed that modifications of the channel protein or down-regulation of aquaporin
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expression and subsequent reduced protein abundance might contribute to reduced water
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permeability of waterlogged roots. The water transport across the plasmalemma can be
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slowed-down efficiently if a histidine residue of PIPs is protonated, a process depending
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on acidification of the cytosol (Tournaire-Roux et al., 2003). This cytosolic decrease of pH
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is a common phenomenon in roots of waterlogged plants that occurs within minutes (Gout
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et al., 2001). It is assumed to be caused by (i) a passive influx of protons from the external
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solution or from the vacuole, (ii) the hydrolysis of nucleoside triphosphates and sugar
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phosphates, and (iii) the accumulation of organic acids including the biosynthesis of lactic
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acid (Davies et al., 1974; Felle, 2001; Gout et al., 2001). Besides modulation of the
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aquaporin protein, down-regulation of aquaporin gene expression has also been reported in
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some tree species (Fig. 2) (Kreuzwieser et al., 2009; LeProvost et al., 2011; Rodríguez-
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Gamir et al., 2011). The question arises, how changes in root hydraulic conductance can
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be translated into altered stomatal conductance in the leaves. As mentioned above, root-to-
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shoot transport of signalling compounds might be one option. Another widely ignored
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possibility of root-to-shoot communication is hydraulic signalling. This mechanism of
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signalling is supposed to maintain water homeostasis in drought stressed plants as recently
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reviewed by Christmann et al. (2013). It depends on the transfer of a hydraulic signal, i.e.
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a change in plant water potential, in the xylem and conversion of this signal into a
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biochemical signal in target cells. A hydraulic – so far unidentified - sensor in leaf cells
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could initiate a signaling cascade eventually causing ABA biosynthesis leading to the
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12 This article is protected by copyright. All rights reserved.
closure of stomata (Christmann et al., 2013). The idea of hydraulic signaling is supported
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by reduced water potential in a variety of waterlogged trees that usually is much stronger
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in flood sensitive than in flood tolerant species (Ruiz-Sánchez et al., 1996; Nicolás et al.,
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2005; Ortuno et al., 2007; Parent et al., 2011; Striker, 2012; Herrera, 2013).
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Figure 3 summarizes some aspects of plant water relations in waterlogged trees; the switch
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from normoxia to hypoxia/anoxia by soil waterlogging, results in major changes of root
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metabolism (see chapters below). This metabolic adjustment is associated with a drop of
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cytoplasmic pH in root cells (Davies et al., 1974; Roberts et al., 1984; Felle, 2001; Gout et
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al., 2001), which causes protonation of the PIPs responsible for water absorption by roots.
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Consequently, root hydraulic resistance increases thereby inhibiting water uptake and
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affecting plant water status. A hydraulic signal or a chemical signal of yet unknown nature,
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which is transferred / transported in the xylem, communicates apparent water limitation to
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the shoot, thereby initiating stomatal closure.
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Molecular and physiological changes in roots of waterlogged trees
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Waterlogging causes an enhanced glycolytic flux and fermentative processes
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If stress avoidance strategies such as hypertrophied lenticels, adventitious roots or
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aerenchyma are not yet formed or are overburden during a stress period, waterlogged roots
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may become oxygen deficient and molecular and physiological tolerance mechanisms are
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essential for plant survival. Several studies indicated that under such conditions major
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changes occur in the metabolism of roots of trees. In flood tolerant poplar trees, for
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example, over 2,000 differentially expressed genes were detected after 5 hours of hypoxic
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treatment compared to roots under normoxic conditions. Less dramatic changes (ca. 1,000
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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
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trees’ transcriptome were accompanied by strong changes in the root metabolite profile
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(Kreuzwieser et al., 2009). Because oxygen is the final electron acceptor of mitochondrial
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respiration, this crucial process of plant energy metabolism is slowed down under hypoxia
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or even completely inhibited under anoxia. Thus, ATP cannot be produced any longer by
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aerobic respiration and the cells affected suffer from an energy crisis (Bailey-Serres and
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Voesenek, 2008). Numerous molecular and physiological studies with flood tolerant and
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sensitive tree species have demonstrated that fermentative pathways are stimulated under
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such conditions. Consistent with observations in herbaceous plants (Davies et al., 1974;
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Roberts et al., 1984), also trees seem to switch in response to hypoxia initially from
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mitochondrial respiration to lactic acid fermentation. This switch has been documented at
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both, the metabolite level and the level of lactate dehydrogenase (LDH) gene expression
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(Joly and Crawford, 1982; Gout et al., 2001; Kolb et al., 2002; Kreuzwieser et al., 2009).
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Because the accumulation of lactic acid leads to an acidification of the cytosolic pH
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(Davies et al., 1974), LDH activity is lowered and alcoholic fermentation is stimulated.
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This change in fermentation processes is suggested from increased pyruvate decarboxylase
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(PDC) and alcohol dehydrogenase (ADH) activities in waterlogged roots, accompanied by
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the formation of the intermediate acetaldehyde (Atkinson et al., 2008) and the end-product
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ethanol (Joly and Crawford, 1982; Kreuzwieser et al., 1999; 2002; Kolb et al., 2002;
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Jaeger et al., 2009; Ferner et al., 2012). Consistently, elevated transcript levels of PDC and
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ADH are observed in a great variety of tree species (e.g. Christianson et al., 2010;
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LeProvost et al., 2012); in poplar, elevated ADH and PDC transcript abundance appeared
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in less than one hour after the change from normoxia to hypoxia (Kreuzwieser et al.,
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2009). There are hints that flood tolerant species exhibit higher rates of alcoholic
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fermentation than flood sensitive trees (Porth et al. 2005; Parelle et al. 2006; LeProvost et
Accepted Article
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al., 2012), but such patterns are not consistent (Yamanoshita et al., 2005; Ferner et al.,
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2012).
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The few studies on changes in the transcriptome of waterlogged woody species (poplar:
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Kreuzwieser et al., 2009; cotton: Christianson et al., 2010; pedunculate and sessile oak:
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LeProvost et al., 2012) suggest that together with an up-regulation of the genes of
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fermentative pathways (mainly LDH, ADH and PDC), also the glycolytic flux is
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enhanced, most likely in order to maintain ATP production under conditions of inhibited
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mitochondrial respiration. In poplar and cotton, enhanced glycolytic flux is suggested from
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an up-regulation of key enzymes of this pathway, i.e. phosphofructokinase and pyruvate
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kinase (Kreuzwieser et al., 2009; Christianson et al., 2010). Accelerated glycolysis has
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also been suggested from a transcriptome approach in which two oak species of different
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flood tolerance were compared (LeProvost et al., 2012). Maintaining enhanced glycolysis
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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
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Figure legends
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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.