Plant Adaptation to Multiple Stresses during Submergence and

Following Desubmergence
Bishal Gole Tamang and Takeshi Fukao
Additional article information

Abstract
Plants require water for growth and development, but excessive water negatively
affects their productivity and viability. Flash floods occasionally result in complete
submergence of plants in agricultural and natural ecosystems. When immersed in
water, plants encounter multiple stresses including low oxygen, low light, nutrient
deficiency, and high risk of infection. As floodwaters subside, submerged plants
are abruptly exposed to higher oxygen concentration and greater light intensity,
which can induce post-submergence injury caused by oxidative stress, high light,
and dehydration. Recent studies have emphasized the significance of multiple
stress tolerance in the survival of submergence and prompt recovery following
desubmergence. A mechanistic understanding of acclimation responses to
submergence at molecular and physiological levels can contribute to the
deciphering of the regulatory networks governing tolerance to other environmental
stresses that occur simultaneously or sequentially in the natural progress of a flood
event.
Keywords: flooding, oxidative stress, dehydration, starvation, salinity, disease

1. Introduction
Over the past six decades, flooding events have increasingly occurred throughout
the world as a consequence of global climate change [1]. Flooding is a major
natural disaster that has a detrimental effect on plant growth and fitness in natural
and agricultural ecosystems [2]. Although prolonged flooding substantially impacts
their productivity and viability, plants are equipped with the acclimation
mechanisms to cope with a transient influx of water into their environment. Such
adaptive responses include energy generation through fermentative metabolism in
the absence of oxygen, development of aerenchyma and adventitious roots for
improved aeration, a reduction in cuticle and epidermal cell wall thickness for
decreased diffusion resistance, activation of internode and petiole elongation to
outgrow submergence water, and restriction of growth for the conservation of
precious energy until floodwater subsides [3,4]. These species-specific or common
responses to flooding allow plants to endure or avoid excess water, conferring
enhanced adaptation and survival under the stress.
Submergence is a type of flooding stress and is defined as a condition where the
entire plant is fully immersed in water (complete submergence) or at least part of
the shoot terminal is maintained above the water surface (partial submergence).
This review mainly focuses on plant responses to complete submergence and its
associated stresses at the molecular and physiological levels. Under submergence
and subsequent desubmergence, plants face multiple external challenges
simultaneously or sequentially, which generate various internal stresses that affect
plant growth and survival (Figure 1). Submergence substantially decreases the rate
of gas diffusion, limiting oxygen uptake and compelling carbon inefficient
anaerobic metabolism [5]. Turbid floodwaters reduce light availability, inhibiting
underwater photosynthesis. Limitation of efficient gas exchange also restricts
transpiration severely [6], possibly impeding the absorption and transport of
nutrients from the soil. Under prolonged submergence, these conditions induce
energy starvation and nutrient deficiency in plants. Continuous anaerobic
metabolism can result in the accumulation of phytotoxic end-products [3]. When
floodwaters subside, submerged plants encounter the rapid entry of oxygen,
causing oxidative damage through overproduction of reactive oxygen species
(ROS) and toxic oxidative products [7,8]. Likewise, sudden exposure to higher
light can induce photooxidative damage to photosystem II reaction centers, leading
to reduced photosynthetic capacity (photoinhibition) [9]. Desiccation of leaves
following desubmergence is also observed due to a marked reduction in hydraulic
conductivity in shoots [10]. Nutrient deficiency can persist after desubmergence
because of mineral leaching from the soil. Submergence and post-submergence
stresses can increase the probability of pathogen infection since high humidity and
heavy rainfall favor pathogen development and disease transmission [11,12]. It has
been shown that submergence attenuates plant resistance to insect herbivores
[13,14], which raises the risk of insect damage upon desubmergence. In low-lying
lands of coastal regions, plants can be submerged in seawater as a result of high
tides, storm surges, and tsunami. Inundation of seawater can lead to salinization of
arable soils, which may last for long periods of time after flooding. From the
above, it is obvious that plants suffer from multiple external and internal stresses
during the natural progression of a flood event. In this review, we discuss how
plants coordinate multiple adaptation mechanisms to cope with various stresses
that occur concurrently or subsequently during submergence and following
desubmergence.
Figure 1
External and internal stresses induced during submergence and following desubmergence
in plants. When immersed in water, plants encounter drastic changes in environmental
parameters (external stresses), triggering a variety of internal stresses. When ...

2. Molecular Mechanisms of Submergence Tolerance

and Escape
A mechanistic understanding of molecular regulation underlying submergence
tolerance and escape in plants has been advanced through functional
characterization of key genes responsible for acclimation to these stresses in rice
(Oryza sativa). Rice is a wetland plant that is well adapted to partially flooded
conditions (root waterlogging). However, most rice accessions die when
completely immersed in water for 7–10 days [15]. A limited number of rice
varieties can tolerate a deep transient flash flood through economization of energy
reserves (quiescence strategy) or escape from a slow progressive flood through
rapid internode elongation (escape strategy) [1,16]. Quantitative trait locus (QTL)
analysis and map-based cloning revealed that the SUBMERGENCE1 (SUB1) locus,
encoding a variable cluster of two or three tandem-repeated group VII of
ETHYLENE RESPONSIVE FACTOR (ERF-VII), regulate the quiescence
response [15]. All rice accessions surveyed contained SUB1B and SUB1C genes at
the SUB1 locus, whereas SUB1A was limited to some indica and aus varieties
[15,17]. Conditional and constitutive expression of SUB1A conferred survival of
complete submergence for 14–16 days [17,18,19]. Remarkably, the submergence
escape response, contrasting with the quiescence response, is also primarily
regulated by the locus containing tandem-repeated ERF-VIIgenes,
designated SNORKEL1 (SK1) and SNORKEL2 (SK2) [20]. Allelic surveys revealed
that SK genes are present only in deepwater rice accessions that exhibit rapid
internode elongation in response to submergence.
We propose that SUB1A and SKgenes differentially regulate the hormonal network
conserved in rice, modulating the two antithetical responses to submergence,
respectively (Figure 2). Submergence promotes biosynthesis and entrapment of
ethylene, which stimulates mRNA accumulation of SUB1A [18].
However, SUB1Aultimately limits ethylene production, leading to the suppression
of ethylene-mediated production of gibberellic acids (GA). SUB1A also increases
the abundance of brassinosteroids (BR), which enhances degradation of bioactive
GA [21]. Increased BR levels also contribute to the accumulation of SLENDER
RICE1 (SLR1), a DELLA protein that negatively regulates GA signaling. Positive
feedback regulation of SUB1A and BR can further augment SUB1A-dependent
hormonal regulation, resulting in the restriction of GA-mediated elongation growth
and carbohydrate consumption under submergence (quiescence response). Similar
to SUB1A, the abundance of SKtranscripts is elevated by submergence-induced
ethylene [20]. SKs promote accumulation of bioactive GA in submerged internodes
[22]. It has been recognized that ethylene increases biosynthesis of and
responsiveness to GA under submergence, triggering internode elongation in
deepwater rice [23,24]. However, Hattori et al. [20] had demonstrated that SKs are
not involved in ethylene production during submergence. As observed in other
hormonal regulation, it is expected that the regulatory roles of BR in degradation
of bioactive GA and accumulation of SLR1 are conserved within the same species
(i.e., O. sativa). Based on the contrasting roles of SUB1A and SKs in submergence
responses, SKs could downregulate BR synthesis in deepwater rice, promoting
GA-mediated elongation growth caused by increased production and signaling of
GA.

Figure 2
Model of the regulatory mechanisms underlying the quiescence and escape responses to
submergence in rice. (a) Quiescence response: Under submergence, the level of
endogenous ethylene quickly rises due to physical entrapment and increased
biosynthesis,...

The Arabidopsis (Arabidopsis thaliana) genome encodes five ERF-VII genes;

two HYPOXIA RESPONSIVE ERF (HRE) genes, HRE1(ERF73)
and HRE2 (ERF71), and three RELATED TO AP2 (RAP2)
genes, RAP2.2 (ERF75), RAP2.3(ERF72/EBP), and RAP2.12 (ERF74) [1,25].
Investigation of overexpression lines and loss-of-function mutants has
demonstrated that all Arabidopsis ERF-VIIs are involved in adaptation to
submergence and oxygen deprivation. Both hypoxia and anoxia dramatically
increased the abundance of HRE1 and HRE2mRNAs [26,27]. On the other
hand, RAP2.2, RAP2.3, and RAP2.12 mRNAs were accumulated even under
normoxia in association with polysomes, suggesting that these proteins are
constitutively synthesized [1,28]. Constitutive expression of each of these genes
enhanced induction of the core hypoxia-responsive genes under oxygen
deprivation, which were positively correlated with survival of seedlings under
hypoxia and adult plants under submergence [26,27,29,30,31,32]. Consistently, a
double-knockout mutant of HRE1and HRE2 (hre1hre2) and single knockout
mutants of RAP2 genes (rap2.2, rap2.3, and rap2.12) exhibited reduced tolerance
to hypoxia or submergence [27,29]. A recent study has revealed
that RAP2.12 promotes expression of a hypoxia-inducible trihelix transcription
factor gene, HYPOXIA RESPONSE ATTENUATOR 1 (HRA1), but HRA1 protein
physically interacts with RAP2.12 protein to restrict its transactivation capacity
[33]. Interestingly, HRA1 also downregulated activation of its own promoter. It
was proposed in Giuntoli et al. [33] that these two feedback loops contribute to the
fine-tuning of RAP2.12-mediated gene expression, providing adequate
consumption of energy reserves during oxygen deprivation and submergence.
Two independent studies have demonstrated that the N-end rule pathway of
targeted proteolysis regulates the turnover of Arabidopsis ERF-VII proteins in an
oxygen-dependent manner (Figure 3) [30,34]. ERF-VII proteins contain a
conserved motif at their amino terminus starting with methionine-cysteine [25],
which is widely conserved in higher plants [30,35]. The N-terminal methionine of
ERF-VIIs is constitutively removed by methionine aminopeptidases so that the
second amino acid, cysteine, is exposed [36]. In the presence of oxygen and nitric
oxide, the exposed cysteine is oxidized by plant cysteine oxidases (PCOs) to
produce cysteine sulfinic or cysteine sulfonic acid [37,38]. The oxidized cysteine is
subsequently conjugated with an arginine residue by arginyl tRNA transferases
(ATEs), which is recognized and ubiquitinated by an E3 ubiquitin ligase,
PROTEOLYSIS6 (PRT6), and then degraded by the 26S proteasome [1,36].
Because molecular oxygen is a co-substrate of PCO, oxidization of cysteine is
restricted under oxygen deprivation. Thus, hypoxia inhibits the oxygen-dependent
branch of the N-end rule pathway, leading to the escape of ERF-VII proteins from
targeted proteolysis and the activation of ERF-VII-mediated acclimation responses
to the stress.

Figure 3
Oxygen-dependent stabilization and localization of ERF-VII proteins. Under
oxygen-replete conditions (normoxia), ERF-VII proteins are degraded via the N-
end rule pathway of proteolysis (NERP). All ERF-VII proteins contain methionine
and cysteine (MC) ...

Besides the N-end rule pathway, the participation of ERF-VII proteins in

transcriptional activation is controlled via sequestration of the transcription factor
to the plasma membrane (Figure 3) [30]. Under aerobic conditions, RAP2.12
protein interacts with plasma membrane-localized acyl-CoA-binding proteins,
ACBP1 and ACBP2. Translocation analysis of photoconverted RAP2.12:mEos
protein suggested that oxygen deprivation promotes relocalization of RAP2.12
from the plasma membrane to the nucleus [39]. This mechanism can allow the
protection of RAP2.12 against the N-end rule-mediated proteolysis under
normoxia, which could enable the immediate activation of acclimation responses
when an internal oxygen concentration reached to a critical level.
In Arabidopsis, double-knockout mutants of genes encoding arginine
transferases, ate1ate2, and a single knockout mutant of an E3 ubiquitin
ligase, prt6, displayed enhanced survival under low oxygen, submergence, and
prolonged darkness [34,40]. In addition, the key regulator for submergence
tolerance in rice, SUB1A, is not an N-end rule substrate based on in vitro data [34].
These results suggest that stabilization of ERF-VII proteins via genetic
manipulation of the N-end rule components may result in the improvement of
flooding tolerance in plants. In barley (Hordeum vulgare), reduced accumulation
of PRT6 transcript by RNAi technology triggered expression of hypoxia-
responsive genes and retained chlorophyll degradation under root waterlogging,
resulting in the enhancement of biomass production and grain yields as compared
to wild type plants [41]. When exposed to submergence and hypoxia, oxygen
uptake is severely restricted in the entire plant, whereas shoot tissues still have
access to oxygen under waterlogged conditions. It is likely that downregulation
of PRT6enabled the stabilization of ERF-VII proteins even in the presence of
oxygen in shoots of the transgenic plants under waterlogging, contributing to the
activation of transcriptional and physiological acclimation in aerial tissues. In wild
type plants, however, ERF-VIIs may not be involved in the acclimation to
waterlogging in shoot tissues because the targeted proteolysis can degrade these
proteins in aerial tissues. Nevertheless, stress-inducible and tissue-specific
regulation of the N-end rule components must be an effective approach to enhance
tolerance to submergence, waterlogging, and their related stresses without adverse
effects on other agronomic traits.
3. Submergence, Reoxygenation, and Dehydration
The quiescence survival strategy is successful when submergence water subsides
within 14–16 days and plants gain access to the resources (O2, light, and nutrients)
sufficient to recommence photosynthesis, aerobic respiration, and other metabolic
activities. However, re-aeration induces other environmental stresses in plants. For
example, sudden exposure to atmospheric oxygen results in oxidative injury
[42,43,44]. Reoxygenation stress also triggers a significant drop in hydraulic
conductivity in shoots, causing leaf desiccation even in the presence of sufficient
soil water [8,10]. The degree of post-submergence stresses depends on the duration
of submergence. Reoxygenation following seven days of submergence induced
irreversible cellular damage in rice leaves, but desubmergence from three days of
inundation did not affect ROS accumulation and lipid peroxidation, resulting in
quick recovery from the stress [8,45].
Interestingly, the key regulator of submergence tolerance, SUB1A, is involved in
the adaptation to post-submergence stresses in rice. Evaluation of genotypes with
or without SUB1A revealed that SUB1Aenhances recovery from dehydration
through enhanced responsiveness to abscisic acid (ABA), elevated accumulation of
mRNAs associated with acclimation to dehydration, and reduction of leaf water
loss and lipid peroxidation [8]. Similarly, in the same study, SUB1Aaugmented the
abundance of gene transcripts encoding ROS scavengers, limiting accumulation of
ROS in aerial tissues and enhancing tolerance to oxidative stress. SUB1Aalso
contributed to the maintenance of non-photochemical quenching immediately
following de-submergence [45]. Such a SUB1A-mediated mechanism can provide
protection against sudden exposure to higher light upon reoxygenation, promoting
photosynthetic recovery from submergence.
A recent study has revealed that another ERF-VII gene, EREBP1, is associated
with the adaptation to both submergence and drought in rice [46]. Constitutive
expression of EREBP1 elevated mRNA accumulation of genes associated with
ABA biosynthesis and the content of ABA in leaves even under non-stressed
conditions. Genotypes with overexpressed EREBP1displayed enhanced recovery
from submergence stress, with restricted underwater elongation and ROS
accumulation. These transgenic plants were more vigorously recovered from
drought at vegetative and reproductive stages as compared with wild type plants,
presumably due to upregulation of drought-responsive genes and increased
accumulation of ABA.
Additional evidence for the involvement of ERF-VIIs in the tolerance to post-
submergence-related stresses has been reported in Arabidopsis. Accumulation
of HRE2mRNA was upregulated by osmotic and oxidative stress
in Arabidopsisseedlings [31]. Overexpression of HRE2 enhanced tolerance to
osmotic and oxidative stresses, whereas osmotic stress induced hyperaccumulation
of superoxide anion in hre2 mutant leaves, reducing seedling survival under the
stress. Likewise, inducible expression of each of RAP2.2, RAP2.3,
and RAP2.12 conferred tolerance to oxidative and osmotic stresses through
increased responsiveness to ABA and activation of a subset of dehydration-
responsive genes [27]. Based on these results in rice and Arabidopsis, it is
anticipated that members of ERF-VII genes play a prominent role for acclimation
to multiple environmental stresses that occur during submergence and following
desubmergence. In addition to ERF-VII transcription factors, a sunflower
(Helianthus annuus) WRKY transcription factor, HaWRKY76, functions as a
positive regulator for tolerance to submergence and drought [47]. The level
of HaWRKY76 transcript was elevated in response to drought and re-aeration
following submergence in leaves of sunflower. Overexpression
of HaWRKY76 in Arabidopsis contributed to the conservation of carbohydrate
reserves during submergence and the suppression of ROS accumulation following
desubmergence, resulting in higher seed production. Under water deficit
conditions, the transgenic plants maintained more water in leaves and produced
more seeds than wild type.

4. Submergence and Starvation

Due to limited availability of oxygen and light under water, aerobic respiration and
photosynthesis are severely restricted in submerged plants. It has been shown that
many terrestrial wetland plants form gas films on the super-hydrophobic leaf
surface under submergence, facilitating exchange of O2 and CO2with surrounding
water [48]. In rice, this mechanism enables the maintenance of underwater
photosynthesis for 4–5 days [49]. However, prolonged submergence decreases the
thickness of gas films, which declines gas exchange and net photosynthesis.
Comparative analysis of near-isogenic lines demonstrated that SUB1A is not
involved in the regulation of underwater photosynthesis in rice. Rather, it appears
that SUB1Acontributes to rapid recovery of photosynthesis following
desubmergence [45]. Carbohydrate starvation and an energy crisis are major issues
that impact plant growth and survival during submergence. Indeed, the
conservation of carbohydrate reserves during submergence is positively correlated
with the degree of submergence tolerance [50]. In rice, SUB1A economizes
carbohydrate reserves in aerial tissue under submerged conditions through
suppressed accumulation of mRNAs encoding sucrose synthases and α-amylases
[18]. The ability of SUB1A to maintain stored carbohydrates was also confirmed in
plants exposed to prolonged darkness [51]. SUB1A restrained production of
ethylene and responsiveness to methyl jasmonate, key hormones involved in the
onset of leaf senescence, causing a marked delay of carbohydrate and chlorophyll
breakdown in aerial tissue under constant darkness. Recent characterization
of prt6mutants in Arabidopsis has confirmed the link between tolerance to
submergence and prolonged darkness [40]. Loss-of-function mutants
of PRT6, greening after extended darkenss1 (ged1) and prt6-1, preserved starch in
leaves of adult plants during submergence, contributing to the enhancement of
survival under the stress. It was also shown that both of these mutants are
significantly more tolerant to prolonged darkness than wild type plants at the seed
germination and seedling stages. These results suggest that stabilization of ERF-
VII proteins via inhibition of the N-end rule pathway can lead to the economization
of carbohydrate reserves under starvation conditions such as submergence and
constant darkness in Arabidopsis.
As observed in mature plants of deepwater rice, some non-deepwater accessions
can escape from submergence through rapid emergence and elongation of
coleoptiles at the seed germination and early seedling stages [52]. This trait is a
determinant for successful seedling establishment in direct-seeded systems in areas
prone to flooding or where fields are not levelled [53]. It was reported that a
carbohydrate starvation/energy depletion sensor, sucrose-nonfermenting1-related
protein kinase1A (SnRK1A), plays a critical role in the regulation of seed
germination and early seedling growth in rice under both aerobic and anaerobic
conditions (Figure 4) [54,55]. SnRK1s are structurally and functionally analogous
to their yeast and mammalian orthologs, sucrose nonfermenting1 (SNF1) and
adenosine monophosphate-activated protein kinase (AMPK), respectively, all of
which are crucial elements for transcriptional, metabolic, and developmental
regulation in response to nutrient and energy starvation [56]. At the initial stage of
seed germination, soluble carbohydrates are quickly exhausted to support energy
demand for repair and synthesis of organelles and other metabolic processes. Sugar
starvation promotes protein accumulation of SnRK1A, which stimulates gene
expression of MYBS1 and likely phosphorylates MYBS1 protein [54]. MYBS1
directly up-regulates transcription of α-amylase genes, contributing to the
activation of starch breakdown in endosperms. Under oxygen deprivation, a
calcineurin B-like protein-interacting protein kinase15 (CIPK15) enhances
accumulation of SnRK1A protein and directly interacts with the kinase to trigger
the SnRK1A-dependent signaling cascade, promoting anaerobic starch degradation
during seed germination and early seedling growth [55].
Figure 4
Molecular regulation of germination and early seedling growth in rice under aerobic and
anaerobic conditions. Rapid consumption of soluble carbohydrates at the early stage of
germination and seedling growth leads to sugar starvation, which stimulates ...

Taking advantage of genetic diversity for the vigor of anaerobic germination

within rice accessions, several QTLs affecting survival of submergence at the
seedling establishment stage have been identified [57,58]. Of these QTLs, qAG-9-
2 on chromosome 9 was fine-mapped and a trehalose-6-phosphate phosphatase
gene, OsTPP7, was identified as the genetic determinant on the locus [59].
Introgression of qAG-9-2 into an intolerant rice variety, IR64, further enhanced
mRNA accumulation of submergence-inducible CIPK15 and MYBS1 in the tissue
containing embryos and coleoptiles, resulting in increased activity of α-amylase
and vigorous elongation of coleoptiles under the stress. Trehalose-6-phosphate
(T6P) inhibits SnRK1 activity in growing sink organs [60,61,62]. It was proposed
in Kretzschmar et al. [60,62,63,64,65,66,67,68,69]. Further studies are required to
determine whether the SnRK1 and T6P signaling pathways are associated with the
escape response to submergence in other growing tissues such as internodes and
petioles.

5. Submergence and Disease

In general, prolonged exposure to abiotic stresses such as drought, salinity, and low
temperature attenuates defense responses to pathogens and increases severity of
diseases in plants [70,71]. Indeed, a number of studies have demonstrated an
antagonistic relationship between ABA-mediated stress signaling and disease
resistance at the molecular and physiological levels
[72,73,74,75,76,77,78,79,80,81]. These results may reflect a lack of necessity for
simultaneous resistance to dehydration and pathogen attack in natural
environments because successful pathogen infection requires relatively high
humidity [79]. However, other reports identified genes that negatively affect both
disease resistance and drought tolerance in rice and tomato (Solanum
lycopersicum) [82,83], indicating the existence of the pathways co-regulating
defense responses to biotic and abiotic stresses.
In contrast to drought, plants are exposed to high humidity conditions over a flood
event, which favor pathogen development and disease transmission [11,12]. At the
molecular level, mRNA accumulation of R genes is restricted in response to high
humidity, resulting in increased susceptibility to Cladosporium fulvum in tomato
[84,85]. In addition, high humidity suppresses gene expression and kinase
activities of mitogen-activated protein kinase3(MPK3) and MPK6 along with
reduced accumulation of salicylic acid and hydrogen peroxide, compromising
defense responses in lesion-mimic mutants of Arabidopsis [86,87,88]. It is
expected that submergence and post-submergence injury also impacts plant
resistance to pathogens. A recent study has revealed that plants activate defense
responses to prepare for the high risk of pathogen infection during and after
submergence [89]. Microarray analysis showed that submergence stimulates
mRNA accumulation of innate immunity marker genes and WRKY transcription
factors in Arabidopsiseven under pathogen-free conditions. Consistently,
pretreatment of Arabidopsisseedlings with submergence enhanced resistance
to Pseudomonas syringae pv. tomato in a WRKY22-dependent manner under high
humidity conditions. The contribution of ERF-VIIs to disease resistance has been
evaluated [46,90]. Arabidopsis and rice ERF-VIIgenes, RAP2.2 and EREBP1,
which are involved in adaptation to submergence, positively regulate disease
resistance through increased expression of defense-related genes. Stabilization of
ERF-VII proteins via inhibition of the N-end rule pathway under low oxygen may
be part of the mechanisms to enhance innate immunity at a high probability of
pathogen infection during submergence.

6. Submergence and Salinity

Coastal flooding occurs when seawater flows over low-lying areas as a
consequence of high tides, storm surges, and tsunami, which can exposendation
[91]. Limitation of Na+ and Cl− transport into salinity-sensitive tissues/cell-
types/organelles and maintenance of local K+ concentrations are key factors
affecting tolerance to high salt [92,93,94]. When waterlogged with saline water,
oxygen deprivation in the root systems restricts energy production required for the
regulation of ion transport and homeostasis, leading to increases in Na+ and
Cl−concentrations and decreases in K+concentrations in shoots [91,95]. It has been
recently demonstrated that oxygen availability in root cells is associated with
management of cell type-specific ion concentrations in adventitious roots of barley
when treated with the combined stresses of salinity and waterlogging [96].
The effect of complete submergence on the adjustment of ion transport under high
salt conditions is poorly understood. It was suggested in Colmer and Flowers [91]
that the inhibition of transpiration under submergence presumably declines the
root-to-shoot transport of ions, but salts might be taken up by leaves due to direct
contact with saline water. Indeed, when flooded in water containing 25–100 mM
NaCl, accumulation of Na+ and Cl− in shoots was greater in submerged plants than
waterlogged plants in Melilotus siculus [97]. Consistently, removal of gas films on
the leaf surface elevated the concentrations of Na+ and Cl− in shoots under
submergence. Prevention of Na+ and Cl− transport from roots to shoots is a critical
mechanism to protect salt-sensitive leaves when only the root system is inundated
in saline water. However, this strategy is unlikely to be beneficial for plants
completely submerged in seawater because salt ions can directly enter their leaves.
Gas films may serve as an alternative mechanism to hamper the salt entry into
leaves in terrestrial wetland plants that occasionally encounter complete
submergence in saline water.
Recent molecular analysis suggests that an Arabidopsis SnRK1, KIN10, functions
as a convergence point that coordinates the antagonistic interactions between
salinity and hypoxia tolerance [98]. KIN10 is an upstream component of genes
associated with energy starvation induced under darkness, hypoxia, and senescence
[67] and positively regulates seedling survival under submergence [99]. AtMYC2
is a transcription factor that activates expression of genes involved in ABA-
dependent drought response pathways through direct binding to the ABA-
responsive element (ABRE) domain [81]. Im et al. [98] has demonstrated that
phosphorylation of AtMYC2 protein by KIN10 decreases the stability of the
transcription activator, resulting in a reduction in ABRE promoter activity.
Consistently, overexpression of KIN10 reduced tolerance to the combined stresses
of submergence and salinity in Arabidopsis seedlings. Despite its biological,
agricultural, and ecological importance under changing climates, the regulatory
mechanism of adaptation to saline submergence has been rarely studied in tolerant
species and crops. Comparative genomic and physiological analyses of halophyte
and non-halophyte species adapted to wet environments will facilitate the
identification of key components and pathways associated with tolerance to the
combined stresses.

7. Conclusions and Future Perspectives

Plants undergo multiple environmental stresses during submergence and following
desubmergence (Figure 1), necessitating the activation of manifold hormonal and
signaling pathways coordinating acclimation responses to each challenge. On the
basis of genetic and molecular studies, it seems that plant tolerance to submergence
and its associated stresses is commonly governed by the core regulatory
components encoding transcription factors, protein kinases, and their upstream
components (Table 1). For example, rice ERF-
VII genes, SUB1A and EREBP1 and Arabidopsis ERF-
VIIgenes, HRE1, HRE2, RAP2.2, RAP2.3, and RAP2.12 are positive regulators for
plant survival under submergence, most of which also confer tolerance to oxidative
and osmotic (dehydration) stresses [8,18,19,27,31,32,46]. It is anticipated that
ERF-VIIs are generally degraded under oxygen-replete conditions via the N-end
rule pathway [30,34]. However, SUB1A protein is not an N-end rule substrate
despite containing the conserved N-terminal motif [34]. The escape of SUB1A
from the oxygen-dependent proteolysis pathway may enable accumulation of the
ERF-VII protein even after reoxygenation, triggering the activation of acclimation
responses to post-submergence stresses such as oxidative stress and dehydration.
Loss-of-function mutants, hre2 and rap2.3rap2.12, displayed reduced tolerance to
osmotic stress in Arabidopsisseedlings [2724,79,103]. It appears that the core
genes conferring multiple stress tolerance under submergence and post-
submergence act as molecular hubs to connect the signaling cascades regulating
individual stress responses. Elucidation of the regulatory mechanisms underlying
stability and localization of ERF-VII proteins and their transcriptional activation
with partner and effector proteins in different cell types/tissues x stress conditions
will facilitate the dissection of the intricate signaling networks governing multiple
stress tolerance in plants.
It has been recognized that plants release a large variety of volatile organic
compounds (VOCs) into the surrounding atmosphere in response to various abiotic
and biotic stresses such as drought, salinity, low light, high light, oxidative stress,
pathogen infection, and insect attack, which function as signaling molecules to
trigger acclimation and defense responses to these stresses [104]. Recent studies
have suggested that catabolism and degradation of VOCs are associated with plant
carbon balance and stress tolerance [105]. Because some of these stresses
stimulating emission of VOCs occur during submergence and following
desubmergence, these compounds may influence the regulation of adaptation to
excess water. It is expected that constitutively and conditionally synthesized VOCs
are highly accumulated in submerged tissues due to physical entrapment.
Submergence-tolerant species and genotypes may have specific mechanisms to
cope with hyperaccumulation of VOCs under water. Future studies will determine
the positive and negative effect of submergence-inducible VOCs on adaptation
responses and the role of ERF-VIIs in VOC accumulation, catabolism, and
degradation under the stress.
Acknowledgments
Abiotic stress research in the Fukao group is supported by the Thomas F. and Kate
Miller Jeffress Memorial Trust, Bank of America, Trustee, Virginia Soybean
Board, Virginia Small Grains Board, the Virginia Agricultural Experiment Station,
and the Hatch Program of the National Institute of Food and Agriculture, U.S.
Department of Agriculture (1001192).

Author Contributions
Bishal Gole Tamang and Takeshi Fukao designed the structure of the manuscript,
screened the literature, and wrote the main text. Bishal Gole Tamang
created Figure 1, Figure 2, Figure 3 and Figure 4 and Table 1. Takeshi Fukao was
responsible for final revision of the manuscript.

Conflicts of Interest
The authors declare no conflict of interest.

Article information
Int J Mol Sci. 2015 Dec; 16(12): 30164–30180.
Published online 2015 Dec 17. doi: 10.3390/ijms161226226
PMCID: PMC4691168

Bishal Gole Tamang1 and Takeshi Fukao1,2,3,*

Jianhua Zhu, Academic Editor

Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg, VA 24061,
1

USA; [Link]@gnamatgb
2 Translational Plant Sciences Program, Virginia Tech, Blacksburg, VA 24061, USA
3 Fralin Life Science Institute, Virginia Tech, Blacksburg, VA 24061, USA
Correspondence: [Link]@oakuf; Tel.: +1-540-231-9527
*

Received 2015 Nov 1; Accepted 2015 Dec 10.

Copyright © 2015 by the authors; licensee MDPI, Basel, Switzerland.

This article is an open access article distributed under the terms and conditions of the Creative
Commons by Attribution (CC-BY) license ([Link]

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