African Journal of Agricultural Research Vol. 7(13), pp. 1976-1981, 5 April, 2012
Available online at http://www.academicjournals.org/AJAR
ISSN 1991-637X © 2012 Academic Journals
Waterlogging stress in plants: A review
Muhammad Arslan Ashraf
Department of Botany, University of Agriculture, Faisalabad. E-mail: email@example.com. Tel: 041-9200161-67 ext. 3306.
Accepted 17 January, 2012
Waterlogging is the major obstacle for sustainable agriculture. Plants subjected to waterlogging suffer
from substantial yield losses. Under natural environmental conditions, plants often get exposed to
transient or permanent waterlogging. Flooding induces a number of alterations in important soil physio-
chemical properties like soil pH, redox potential and oxygen level. Thus, the plants growing on the
waterlogged soil face the stressful environment in terms of hypoxia (deficiency of O
) or anoxia
(absence of O
). These oxygen deficient conditions substantially hamper plant growth, development
and survival. Plants under O
-restrictive environment exhibit metabolic switch from aerobic respiration
to anaerobic fermentation. It is evident from the available literature that most of the genes expressed
under flooding stress are potentially involved in the synthesis of enzymes known to play active role in
the establishment of this fermentative pathway. Plants undergo this metabolic change in order to get
continuous supply of
Adenosine triphosphate (ATP). Under waterlogged conditions, plants exhibit
several responses including hampered stomata conductance, net CO
-assimilation rate and root
hydraulic conductivity. Furthermore, plants grown under waterlogged conditions often face the
oxidative damage induced by the generation of reactive oxygen species. These reactive oxygen species
in turn affects the integrity of membranes and induce damage to the efficiency of photosystem II,
thereby, causing considerable decrease in net photosynthetic rates. Moreover, these perturbations in
physiological mechanisms may affect the carbohydrate reserves and translocations. In fact,
waterlogging tolerant and sensitive plant species could be discriminated on the basis of their efficient
carbohydrate utilization. Waterlogging is also known to induce adverse effects on several physiological
and biochemical processes of plants by creating deficiency of essential nutrients like nitrogen,
magnesium, potassium, calcium. Apart from these waterlogging-induced alterations in physiological
mechanisms, plants growing under flooded conditions also exhibit certain morphological changes
entailing the formation of adventitious roots, initiation of hypertrophied lenticels and/or establishment
of aerenchyma. Therefore, the aim of this review is to highlight the major morphological, physiological
and biochemical adaptations of plants to tolerate the flooding stress.
Key words: Hypoxia, anoxia, fermentation, Adenosine triphosphate (ATP), reactive oxygen species (ROS),
In tropical and subtropical regions, excessive rainfall is
the major constraint for crop production. Elevated levels
of water in soil create hypoxic conditions (decrease in the
level of oxygen) within a short period of time. As a result
plant roots suffer from anoxia, complete absence of
oxygen (Gambrell and Patrick, 1978). However, plants
tolerant to waterlogging (flooding) stress exhibit certain
adaptations, for example, formation of aerenchyma and
adventitious roots. Furthermore, the formation of
adventitious roots is due to the interaction of plant
hormones, auxin and ethylene (McNamara and Mitchell,
1989). Oxygen deficiency inhibits the root respiration of
plants which results in substantial reduction in energy
status of root cells. Since oxygen is a terminal electron
acceptor in aerobic respiration, in its absence, Kreb’s
cycle and electron-transport system are blocked.
Therefore, plants under waterlogged conditions use
alternate pathway for energy extraction. This alternate
pathway uses fermentative metabolism to produce
Adenosine triphosphate (ATP), thereby, resulting in
enhanced accumulation of ethanol.
Moreover, the activity of alcohol dehydrogenase (ADH)
is also increased (Davies, 1980; Vartapetian, 1991).
In fermentation, plants could get only two ATP per
glucose molecule, whereas, 36 ATP molecules are
produced per glucose molecule in aerobic respiration.
Flood-tolerant plants are able to maintain their energy
status using fermentation. In addition, the maintenance of
cytosolic pH is of prime importance. In waterlogged
plants, initial decline in cytosolic pH has been observed
and this decline is attributed to the production of lactic
acid during fermentation. This initial decrease in pH helps
the plant to switch from lactate to ethanol fermentation by
activation of alcohol dehydrogenase and inhibition of
lactate dehydrogenase (Chang et al., 2000). As under
hypoxic or anoxic conditions oxygen is lacking, therefore,
alternative electron acceptor is required. For example,
nitrate has been considered as terminal electron acceptor
of plant mitochondria under anoxic or hypoxic conditions
(Vartapetien et al., 2003). It has also been suggested that
nitrate reduction is an alternate respiratory pathway and
is important for the maintenance and energy homeostasis
of the cell in the oxygen deficient environment
(Igamberdiev and Hill, 2004).
WATERLOGGING-INDUCED ALTERATIONS IN
One of the first plant responses to waterlogging is the
reduction in stomata conductance (Folzer et al., 2006).
Plants exposed to flooding stress exhibit increased
stomata resistance as well as, limited water uptake
leading to internal water deficit (Parent et al., 2008). In
addition, low levels of O
may decrease hydraulic
conductivity due to hampered root permeability (Else et
al., 2001). Oxygen deficiency generally leads to the
substantial decline in net photosynthetic rate (Ashraf et
This decrease in transpiration and
photosynthesis is attributed to stomata closure (Ashraf
and Arfan, 2005). However, other factors such as
reduced chlorophyll contents, leaf senescence and
reduced leaf area are also held responsible for
decreased rates of photosynthesis (Malik et al., 2001). In
this context, Yordanova et al. (2005) reported fast
stomata closure in barley plants when subjected to
flooding conditions. Similarly, when pea plants were
subjected to flooding conditions, a prompt closure of
stomata was recorded (Zang and Zang, 1994). This
stomata closure of pea plants was attributed to the
abscisic acid (ABA) transport from older to younger
leaves or denovo synthesis of this hormone.
Furthermore, prolonged exposure of plants to flooding
conditions could result in root injuries which in turn
restrict photosynthetic capacity
alterations in biochemical reactions of photosynthesis.
These biochemical alterations include restricted activity of
ribulose bisphosphate carboxylase (RuBPC),
phosphoglycollate and glycollate oxidase (Yordanova and
Popova, 2001), demolition of chloroplast membrane
inhibiting photosynthetic electron transport and efficiency
of photosystem II (Titarenko, 2000). It is evident from the
literature that flooding causes a marked reduction in
photosynthetic capacity of a number of plants, for
example, Lolium perenne (McFarlane et al., 2003),
Lycopersicon esculentum (Bradford, 1983; Jackson,
1990) Pisum sativum (Jackson and Kowalewska, 1983,
Zhang and Davies, 1987), and Triticum aestivum
(Trought and Drew, 1980). However, plants exhibit
certain adaptation under waterlogging stress to maintain
photosynthetic capacity (Li et al., 2004). Moreover, flood-
induced destruction of chlorophyll has been investigated
widely by a number of researchers (Jackson et al., 1991;
Huang et al., 1994; Ashraf et al., 2011). This decrease in
chlorophyll directly or indirectly affects the photosynthetic
capacity of plants under waterlogged conditions (Ashraf
et al., 2011).
The adverse effects of waterlogging on different gas
exchange attributes of plants have been reported in some
earlier studies. For example, Ashraf and Arfan (2005)
reported decrease in photosynthetic rate, water use
efficiency and intrinsic water use efficiency of 32-day okra
plants when subjected to waterlogged conditions. It is a
general consensus that stomata regulation controls the
exchange rate of plants under waterlogged
conditions (Ashraf and Arfan, 2005; Ashraf et al., 2011).
Furthermore, water potential of plants is also controlled to
some extent by stomata regulations (Liao and Lin, 1996).
However, there are contrasting reports on the
involvement of stomatal regulation in maintenance of
water potential. For example, waterlogging caused a
marked reduction in stomata conductance of bitter melon.
This reduction in g
resulted in increased leaf water
potential (Liao and Lin, 1994). In contrast, Ashraf and
Arfan (2005) found no significant correlation between
stomata conductance and water potential of okra plants
under waterlogged conditions. In fact, these authors were
of the view that osmotic potential and pressure potential
are the main factors that determine water potential.
Waterlogging stress is also known to cause marked
perturbation in different chlorophyll fluorescence
attributes of plants. Since chlorophyll fluorescence is an
excellent physiological marker that determine the primary
processes involved in photosynthesis such as energy
transfer due to excitation, absorption of light and
photochemical reactions occurring in the PSII
(photosystem II) (DeEll et al., 1999; Saleem et al., 2011).
Therefore, changes in chlorophyll fluorescence
parameters determine the function and stability of
photosystem II (Jimenez et al., 1997; Abdeshahian et al.,
2010). The plants subjected to waterlogged conditions
exhibit certain alterations in this physiological marker. For
example, when Cork oak (Quercus variabilis) and China
wingnut (Pterocarya stenoptera) were subjected to
1978 Afr. J. Agric. Res.
waterlogging stress, a prominent decrease in maximum
quantum efficiency (Fv/Fm) was recorded (Hua et al.,
2006). Likewise, decrease in the maximum quantum yield
of PS II photochemistry (Fv/Fm) was also recorded in
flied beans when subjected to varying days of
waterlogging stress (Pociecha et al., 2008). PSII
photochemistry was also impaired due to waterlogging in
Medicago sativa. The decrease in Fv/Fm indicated the
sensitivity of photosynthetic apparatus to abiotic stress
and also inability of the plants to regenerate rubisco
under stressful conditions (Smethurst et al., 2005).
OXIDATIVE DAMAGE INDUCED BY REACTIVE
OXYGEN SPECIES (ROS)
Despite the fact that oxygen is important for life on earth,
its reduction by any means could result in the production
of ROS perturbing several cellular metabolic processes of
plants (Ashraf, 2009; Ashraf et al., 2010). Lethal reactive
oxygen species include superoxide (O
) and the hydroxyl radical (OH). Singlet
oxygen generated due to the reaction of oxygen with
excited chlorophyll, is also considered as potential ROS
(Ashraf and Akram, 2009). These ROS are extremely
reactive in nature and induce damage to a number of
cellular molecules and metabolites such as proteins,
lipids, pigments, DNA etc (Ashraf, 2009). ROS are also
produced in plants under normal conditions or non-
stressed conditions but their concentration is very low.
However, when plants are facing some environmental
stress like waterlogging stress, the concentration of ROS
is elevated to a level that is damaging for several cellular
metabolic reactions of plants such as photosynthesis,
efficiency of PS II (Ashraf, 2009). For example, elevated
cellular levels of hydrogen peroxide result in inhibition of
calvin cycle (Ashraf and Akram, 2009).
ROS are free radicals possessing one or more
unpaired electrons. This is not a stable configuration;
therefore, the radicals react with other cellular molecules
to produce more free radicals (Foyer and Halliwell, 1976;
Hideg, 1997). Generation of reactive oxygen species
occurs via different mechanisms, for example, when
molecules of aerobic system come in contact with the
ionizing radiations, this interaction results in the
production of ROS. It is now a well established fact that
electrons flowing through electron transport chain may
leak from their proper rout and in the absence of any
electron acceptor, these electrons react with oxygen to
produce reactive oxygen species (Ashraf, 2009). Different
celluar organelles such as mitochondria, chloroplasts and
peroxisomes are considered as the sites for production of
reactive oxygen species (Sairam and Srivastva, 2002).
ANTIOXIDANT DEFENSE MECHANISM OF PLANTS
UNDER WATERLOGGED CONDITIONS
All the plants have the ability to detoxify the adverse
effects of ROS by producing different types of
antioxidants. Generally, antioxidants are categorized into
enzymatic and non-enzymatic antioxidants. Enzymatic
antioxidants include ascorbate peroxidase (APX),
superoxide dismutase (SOD), peroxidase (POD),
catalase (CAT), glutathione reductase (GR), whereas,
ascorbic acid, glutathione, tocopherols and carotenoids
are included in non-enzymatic antioxidants (Gupta et al.,
A marked alteration in the endogenous levels of
different enzymatic and non-enzymatic antioxidants has
been recorded in a number of studies. For example,
when mungbean plants were subjected to waterlogging
stress, the activities of various enzymatic antioxidants
such as glutathione reducatse (GR), superoxide
dismutase (SOD), catalase (CAT), and ascorbate
peroxidase (APX) decreased markedly (Ahmed et al.,
2002). These authors also stated that oxidative damage
was not directly involved in the impairment of
photosynthetic machinery of plants under waterlogged
conditions. Likewise, waterlogging-induced reduction in
the activity of one of oxygen processing enzyme SOD
has also been reported in corn (Yan et al., 1996). In
contrast, increase in the activities of different enzymatic
antioxidants was recorded in maize seedlings when
subjected to varying degree of waterlogging stress (Tang
et al., 2010). Similarly, when pigeon pea genotypes were
exposed to waterlogging stress, the activities of
superoxide dismutase (SOD), catalase (CAT), peroxidase
(POD) and ascorbate peroxidase (APX) increased
markedly (Kumutha et al., 2009). From these reports, it
is amply clear that plants when exposed to waterlogged
conditions employ antioxidant defense system to get
through the damaging effects of oxidative stress induced
EFFECT OF WATERLOGGING ON NUTRIENT
Waterlogging reduces the endogenous levels of nutrient
in different parts of plants (Ashraf et al., 2011). Oxygen
deficiency in the root zone causes a marked decline in
the selectivity of K
uptake and impedes the transport
to the shoots (Armstrong and Drew, 2002). It has
also been reported in the literature that hypoxic
conditions cause decrease in the permeability of root
membranes to Na
(Barrett-Lennard et al., 1999).
Generally, waterlogging causes acute deficiencies of
essential nutrients such as nitrogen, phosphorous,
potassium, magnesium and calcium (Smethurst et al.,
2005). In this context, Boem et al. (1996) reported a
marked decline in the uptake of N, P, K and Ca in canola
when exposed to short period of waterlogging stress.
Likewise, reduced endogenous levels of N, P and K have
been reported in maize (Atwell and Steer, 1990). When
M. sativa was subjected to flooding stress, a marked
reduction in leaf and root nutrient composition (P, K, Ca,
Mg, B, Cu and Zn) was recorded in plants (Smethurst et
al., 2005). Similarly, Stieger and Feller (1994) reported
reduced concentrations of P, K and Mg in wheat shoots
due to waterlogging. In contrast, the endogenous levels
of calcium remained unaffected in wheat under
waterlogged conditions. However, decrease in calcium
contents along with other nutrients (N, P, K and Mg) were
also recorded in different organs of wheat under
waterlogged conditions (Sharma and Swarup, 1989).
Similarly, Tarekegne et al. (2000) recorded a marked
reduction in Cu, Zn, P and K uptake in waterlogging
susceptible wheat genotype when compared with the
tolerant genotypes. These researchers were of the view
that genotypes that possess the ability to avoid
waterlogging-induced nutrient deficiency, particularly Zn
and P deficiency should be selected. Moreover, the
hampered efficiency of PS II is attributed to the
deficiencies of N, P, K, Mg and Ca (Smethurst et al.,
2005). It is evident from the literature that adverse effects
of waterlogging are not due to the toxic levels of Na and
Fe but reduced concentrations of N, P, K, Ca and Mg are
the major contributors (Sharma and Swarup, 1989;
Smethurst et al., 2005).
MORPHOLOGICAL AND ANATOMICAL CHANGES
Waterlogging stress is also known to cause a number of
morphological and anatomical changes in plants. For
example, the presence of hypertrophied lenticels is a
common anatomical change observed in different woody
species under flooding stress (Yamamoto et al., 1995).
Radical cell division and expansion near stem base
results in hypertrophic growth. In addition, it is also
believed to be associated with ethylene and auxin
production (Kozlowski, 1997). The lenticels are thought to
be involved in the downward diffusion of O
as well as,
the compounds produced as by-products of anaerobic
metabolism (ethanol, CO
). Although, the actual
physiological role of lenticels is still unclear, their
presence is often linked to waterlogging tolerance in
plants (Parelle et al., 2006). Moreover, the number of
hypertrophied lenticels is more under the water surface
that supports the argument stating their involvement in
maintenance of plant water homeostasis and deviating
from the argument that dictates their role as important
facilitators of oxygen entry toward the root system. Their
potential role in the plant water homeostasis is evident
from their active involvement in partially replacing the
decaying roots and facilitating water intake for the shoot
(Parent et al., 2008).
Formation of adventitious roots potentially replacing the
basal roots is considered as one of the potential
morphological adaptations depicted by plants under
waterlogging stress (Malik et al., 2001). These
specialized roots maintain the continuous supply of water
and minerals when the basal root system fails to do so
(Mergemann and Sauter, 2008). Furthermore, the
deterioration of the main root system is taken as the
sacrifice providing energy for the development of well
adapted root system (Dat et al., 2006). In addition, the
formation of adventitious roots is associated with
waterlogging tolerance of plants (Steffens et al., 2006).
Another important morphological response of plant is
the development of lacunae gas spaces (aerenchyma) in
the root cortex. The formation of aerenchyma is
considered as an adaptive response of the plant under
flooding stress (Evans, 2004). There are two types of
processes involved in the development of aerenchyma.
The first is constitutive development of aerenchyma as it
is not linked with the abiotic stress. It is formed by the
cells separated during tissue development. This type of
cell death occurring as a result of cell separation is
termed as shizogeny, regulated developmentally and
independent of external stimulus. It is formed as a result
of highly regulated tissue specific pattern of cell
separation. The second type of aerenchyma development
is known as Isogeny since it is formed due to partial
breakdown of the cortex that resembles programmed cell
death and its formation depends on the external stimulus
like abiotic stress (Pellinen et al., 1999).
GENETIC VARIATION FOR WATERLOGGING
Plants under waterlogged conditions exhibit marked up
and/or down-regulation of a number of genes. By
investigating the induced expression of these genes in
low oxygen environment, it is possible to identify certain
gene products. Then these potential genes involved in
conferring waterlogging tolerance can be isolated and
introduced into the transgenic plants in order to identify
their possible contribution in stress tolerance. Early
studies performed by isotopic labeling of maize roots with
S-methionine clearly indicated the synthesis of
anaerobic polypeptides when plants were subjected to
low oxygen environment (Sachs et al., 1980). The
anaerobic polypeptides include the enzymes involved in
fermentation, that is, pyruvate decarboxylate, alcohol
dehydrogenase and lactate dehydrogenase.
Moreover, there exists a marked variation in genetic
resources of potential crops for flooding tolerance. For
example, it has been widely reported in the literature that
genetic differences exists in wheat for waterlogging
tolerance (Gradner and Flood, 1993; Ding and Musgrave,
1995). Setter et al. (1999) showed that there exists a
significant genetic diversity among 14 wheat varieties
when exposed to flooding stress under glasshouse
conditions. Similarly, genetic variation has also been
reported in many other plant species, for example, oat
(Lemons e Silva et al., 2003), cucumber (Yeboah et al.,
2008), Soybean (VanToai et al., 1994) and maize(Anjus e
Silva et al., 2005).
1980 Afr. J. Agric. Res.
SHORTGUN APPROACHES TO INDUCE
Scientists from different geographical regions of the world
are actively involved in making the plants tolerant to
flooding stress by the use of exogenous application of
nutrient and plant hormones. For example, recently,
Ashraf et al. (2011) reported that exogenous application
of potassium in soil and as foliar spray alleviated the
adverse effects of waterlogging on cotton plants.
Likewise, Ashraf and Rehman (1999) reported that
application of nitrate in soil proved useful in mitigating the
harmful effects of waterlogging on different physiological
attributes of maize. Likewise, Yiu et al. (2009) found that
exogenous application of spermidine and spermine
provoked several biochemical and physiological
adaptations in onion when exposed to flooding stress. In
this context, exogenous application of uniconazole was
also helpful in circumventing the damaging effects of
waterlogging in wheat and oil seed rape plants (Webb
and Fletcher, 1996; Zhou et al., 1997). Therefore, the use
of these organic and inorganic compounds offers an
excellent platform for inducing tolerance to flooding
It can be inferred from the aforesaid discussion that
waterlogging is one of the major constraints for
sustainable agriculture. Its effects are evident on the
entire plant as well as, cellular levels. There is the need
to screen available germplasm for waterlogging tolerance
and use the genes responsible for inducing tolerance in
other potential crops so as to make them resistant as
well. Waterlogging causes deficiency of several essential
nutrients. Therefore, exogenous application of these
nutrient or other plant hormones could be used so as to
alleviate the adverse effects of waterlogging.
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