The Impact of Flooding Stress on Plants and
Crops
Prof.
Michael B. Jackson
School of Biological Sciences,
University of Bristol, Woodland Road, Bristol BS8 1UG, UK and Plant
Ecophysiology, Faculty of Biology, University of Utrecht, Sorbonnelaan 16, 3584
CA Utrecht, The Netherlands.
Contents
INTRODUCTION
FACTORS
FAVOURING OCCURRENCE OF WATERLOGGING AND SUBMERGENCE Increasing
water input Slow drainage through the soil
profile SOIL WATERLOGGING
Oxygen shortage and other damaging features
of waterlogged soil
How an absence of
oxygen kills root tips ATP
supply and demand Self-poisoning How
roots survive anaerobic conditions
Biochemical acclimation Anatomical acclimation
through aerenchyma formation How
above-ground shoots survive soil waterlogging and submergence Root to shoot communication and
water conservation Increased porosity of the shoot base Replacement rooting Fast upward extension WATERLOGGING AND CROP PRODUCTION Remedial measures in
crop production Improving land drainage
Direct treatment to crops Plant breeding
ACKNOWLEDGEMENTS
REFERENCES |
Note that the text contains many
live links to internet sites. Only references to papers for which such links
could NOT be established are listed at the end
INTRODUCTION
The complex
and highly developed land-based biology with which we
are most familiar, is a relatively new phenomenon in evolutionary terms. Its
existence is predicated on a successful invasion from the sea by photosynthetic
macrophytes ~ 400 million years ago (Corner, 1964). This
gave rise to organisms with the then novel ability to operate
photosynthetically in air while securing water and minerals using a
non-photosynthetic, foraging root system.
Present day representatives of the more than 300,000 plant species
presently known to science now occupy almost every terrestrial niche. However,
although, their progenitors were aquatic, the land plants derived from them are relatively intolerant of free
water in their surroundings, especially if it is slow moving or immobile. The
resulting effect is so severe that biochemical and morphological adaptations
have emerged many times during evolution (Cook, 1999) to
allow a sizeable minority of species to succeed in sporadically or permanently
flooded areas on land. These include
areas prone to ice encasement (Andrews, 1996). The ability of excess
water to damage plants may seem counter-intuitive since water is chemically
benign. However, certain physical properties of water, most notably its ability
to interfere with free gas exchange, can injure and kill plants when they are totally
submerged (Jackson
and Ram, 2003) or even
when only the soil is waterlogged (Vartapetian and Jackson, 1997).
The non-frozen permanently
wet places are known variously as bogs, mires, marshes, fens, peatlands, bottomlands, wetlands etc. These can be natural or
man-made, static or flowing, fresh, brackish or salty, seasonal or permanent.
They are widespread and contain a highly adapted and characteristic
flora that is under threat from drainage, peat extraction and re-development.
These destructive activities conflict with an increasing recognition of the
considerable economic, ecological, social and amenity value of many wetlands.
They have great significance as wildlife sanctuaries, as buffer zones that
reduce flooding intensity of surrounding areas and detoxify the drainage
water. This recognition gave rise to the
Convention on
Wetlands, an intergovernmental agreement adopted at
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Fig.1. Wetlands
in |
The extent of more or less permanently wet
places is more readily quantified than areas subjected to sporadic
waterlogging or deeper flooding. In reality, almost all the land surface
becomes flooded at some time. This is true even in deserts, such as those of central Australia.
Worldwide, it has been estimated that approximately 10 % of
all irrigated farmland suffers from frequent waterlogging, which may
decreases crop productivity 20 %. But, in addition, many rainfed regions
are also susceptible to temporary flooding. Satellite imaging
has the potential to locate these areas of temporarily flooded land but the
technique is under-utilized compared with similar work assessing the extent of
water deficient soils.
Clearly,
stress from flooding has, and remains, a major influence on species distribution
worldwide. It can be the dominant determinant of species success in wet areas (Lenssen
et al. 2003). Furthermore, along with
drought, salinity and mineral deficiency, flooding also has serious economic
consequences for productivity of much arable farmland (see later section
entitled ‘Waterlogging and crop production’). This review assesses the impact of excess water on plant growth
and development and on the underlying biochemistry and molecular biology. Particular attention is given to responses
that appear to enhance tolerance or survival. The major part deals with
waterlogging of the soil, and its impact on root systems, the aerial shoot and
on farm crops. This is preceded by an assessment of the factors that influence
the scale and occurrence of waterlogging and submergence.
FACTORS
FAVOURING OCCURRENCE OF WATERLOGGING AND SUBMERGENCE
Increasing water input
It is
self-evident that episodic waterlogging of the soil or deeper submergence
(referred to collectively as flooding when a distinction is not necessary)
occur when water enters soil faster than it can drain away under gravity. There is mounting evidence that, in several
parts of the World, inputs of water are growing. One cause may be climate
change. For example, records show an increased incidence of flooding and
rainfall in much of northern and Western
Intensive and large-scale irrigation
of farmland can also increase the incidence of waterlogging of the soil. Water
tables can rise as a result. This is especially likely in heavily irrigated dry
regions such as Sindh Province in the Indus valley of Pakistan. Here, 50 to 60
years ago, the water table was 4 m below ground. By 1984, it was less than 1.6
m over most of the irrigated region, the rising water being laden heavily with
salts. The resulting environmental catastrophe has led to a multi-million
dollar drainage project (the Left Bank
Outfall Drainage Project) of immense scale but bringing with it much controversy
and environmental
concern. The problem is exacerbated by the flatness of the topography that
inevitably slows the rate of lateral drainage.
A third contributory factor can be
change of land use. For example, conversion of meadow land to arable farming in
Germany since the 1950s, has contributed to increased surface run-off and
exacerbated flooding problems elsewhere in the landscape (Van Der Ploeg et al., 2002). Expanding urbanization of the
landscape also creates large expanses of non-absorbing hard surface that
concentrates rainwater to its periphery via surface run-off or underground
drainage systems.
Slow drainage
through the soil profile
*Remaining
soil volume is occupied by soil particles
lateral flow within and
above the soil. Obviously, it will be slower on the plains than on sloping
land. However, the impact of rate of vertical drainage through the soil profile
is critical and strongly affected by soil structure, which is highly variable.
Soil structure is a complex subject, involving both macro- and
micro-structural components. It is well-described in Soils An Introduction (5th edition) by Michael
J. Singer and Donald N. Munns. In brief, it can be said
that approximately 40 – 60 % of the soil volume is made of solid material
(mostly minerals and organic matter) that is permeated by spaces filled with
water, with gas or with roots and other living organisms. The total volume of
these spaces (pores), the size range of the pores, their interconnectivity,
stability and the relative proportions of each size class all have a major
impact on how much water is held by the soil and how readily it drains through
the profile. Small pores hold water more strongly by capillary forces than do
larger ones. Adopting the classification of (Greenland, 1977), interconnected pores with a diameter range larger than 50 μm
(transmission pores) drain under gravity. This allows air to enter (critically
oxygen) to support aerobic respiration
and also gives space for root exploration. Pores with diameters in the
range of approximately 50 – 0.5 μm (storage pores) can hold water
against the force of gravity but weakly enough for roots to extract it using
driving forces of up to -1500 kPa. However, they are not large enough to allow
roots to penetrate. Pores smaller that 0.2 μm hold water so strongly that
neither gravity nor roots can extract their contents. These are, therefore,
permanently filled with water and are termed residual pores. These
classifications are summarized in Table 1, which contrasts a sandy loam with a
more clayey soil. It is readily apparent that it will take relatively little
extra water for a clay soil to become waterlogged from field capacity compared
to a sandy loam soil. Pores in clay soils are also unstable when emptied of
water. Thus, drainage is not always followed by the entry of air because some pores
collapse. A further consideration is the interconnectedness of transmission
pores. The ease of movement of water under gravity from pore to pore is
quantified as the soil’s hydraulic conductance (mm d-1). The pores
of clay soils are less well connected than those of sandier
soils and thus drain more slowly because hydraulic conductance is low.
Drainage rates are also affected by a soil’s macro-structure. In clayey soils, the small intrinsic
hydraulic conductance can be offset to some extent by a tendency to crack
thereby opening up fissures through which water may move readily. Channels
formed by earthworms, decayed root axes, also improve the rate of drainage. The
tendency for soil particles to form aggregates (crumbs and clods) with
relatively wide channels between them also influences drainage rate. On a
larger scale, the rate of soil drainage can be affected indirectly by the
hydraulic conductivity of the sub-soil. An impermeable layer at sub-soil depth
such as that created by the soles of ploughs, or imposed naturally as in
so-called duplex soils, can cause saturation and flooding of the topsoil that,
in itself, has good drainage properties. In
duplex soils, rainwater moving readily through the sandy topsoil layers then
encounters an impermeable layer, typically rich in clay that may have been
further compacted by the use of heavy agricultural machinery. In wet weather,
the outcome is a perched water table that limits rooting depth and saturates
much of the overlying soil. In Australia, large areas used for growing wheat
and other crops in south west of Western Australia,
and in Victoria and Queensland are especially susceptible to
flooding by such perched water tables (see below).
SOIL
WATERLOGGING
Oxygen shortage and other damaging features
of waterlogged soil
In waterlogged
soil, diffusion of gases through soil pores is so strongly inhibited by their
water content that it fails to match the needs of growing roots. A slowing of
oxygen influx is the principal cause of injury to roots, and the shoots they
support (Vartapetian and Jackson, 1997). The maximum amount of oxygen dissolved in the floodwater in
equilibrium with the air is a little over 3 % of that in a similar volume of
air itself. This small amount is quickly consumed during the early stages of
flooding by aerobic micro-organisms and roots (Fig. 2). In addition to imposing
oxygen shortage, flooding also impedes the diffusive escape and/or oxidative
breakdown of gases such as ethylene (Arshad and Frankenberger, 1990) or carbon dioxide that are produced by roots and soil micro-organisms.
This leads to accumulations that can influence root growth and function. For
example, accumulated ethylene may slow root extension, while carbon dioxide in
the soil can severely damage roots of certain species e.g.,
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Fig. 2. Effect of
flooding on (i) the displacement and exclusion of aerial oxygen from the
soil, entrapment of metabolically generated gases in the soil and (ii) the
consequences, over time, of bacterial respiration for soil redox potential,
loss of free nitrate and subsequent generation of chemically reduced
end-products. (Developed from (Setter and Belford, 1990) |
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soybean (Glycine max) but not
rice (Boru
et al., 2003). Trapped carbon dioxide may form bicarbonate ions that can
accentuate the effect of high lime content, leading to iron unavailability and
chlorosis. http://cotton.crc.org.au/Publicat/Agro/Iron.htm
. Warm temperatures and ample supplies
of organic matter will inevitably accelerate the development of these
potentially damaging soil conditions. If root tips survive oxygen shortage per
se, they may be injured or killed by subsequent changes in soil
biochemistry (Ponnamperuma, 1972). These changes come about because of microbial respiration that
utilizes inorganic ions as alternative electron acceptors to oxygen in order to
sustain energy generation (Fig. 2). The changes are associated with measurable
decreases in redox potential.
Facultative anaerobes first chemically reduce nitrate, converting it to
nitrite, nitrous oxide and nitrogen gas (denitrification) rendering nitrate
unavailable to roots. As the reducing
intensity of the soil increases further obligate anaerobes chemically reduce
oxides of Mn4+, and Fe3+ to form highly soluble Mn2+
and Fe2+ (Laanbroek, 1990) that
may enter roots and interfere with enzyme activities and damage membranes. Ferrous ion toxicity can be a particular
problem for rice farming on acidic soils.
If flooding is prolonged, further, anaerobic bacteria may then convert
SO42- to H2S, a poison of respiratory enzymes
and non-respiratory oxidases. Acidic
soils that are low in iron are especially likely to contain free and
undissociated H2S (Ponnamperuma, 1972). In the most severely reducing
soils, methogenic bacteria reduce carbon dioxide to methane. Although the gas is harmless to plants it is
second in importance to carbon dioxide as a greenhouse gas contributing to
global warming. Rice paddies are globally significant methane sources.
Flooding may also increases the incidence of
soil-borne fungal diseases (Yanar, Lipps, and Deep, 1997).
Germinating seeds are particularly vulnerable to fungal colonization
(e.g., Gliocladium roseum). Infection of alfalfa, vegetables and trees by
phytophthora (wilting), pythium (damping-off) and anaerobic bacteria (e.g. Pseudomonas putida) are common problems
in practical farming (Walker, 1991). However it is not always clear whether
injury is principally the result of the microbial infection or of the direct
affects of flooding (Davison, 1997) and if infection follows rather than precedes
injury.
How an absence of oxygen kills root tips
Although an absence of
oxygen is usually fatal to growing root tips, surprisingly small amounts of
external oxygen (e.g. 0.006 – 0.01 mol m-3 in solution) are able
keep them alive (note: water in equilibrium in air contains approximately 0.25
mol m-3 of oxygen at 25 ºC). Growth arrest and death arise
principally because of (a) demand for ATP exceeds the supply (b) self-poisoning
by products of anaerobic metabolism. These and related aspects are examined
below.
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Fig. 3. Depiction of
various pathways from starch and sucrose that generate ATP and dispose of
reducing power by oxidizing NADH aerobically or anaerobically. Anaerobic fermentation
yields only 2 moles ATP from each glucose entering glycolysis. Aerobic
respiration via the TCA cycle and mitochondrial electron transport yields
>30 moles ATP. Taken
from (Jackson and Ricard, 2003) |
ATP supply and demand
Anaerobic roots generate ATP mainly by glycolysis. This pathway also
feeds pyruvic acid into ethanolic fermentation (and also into lactic acid
fermentation, especially in the first hours of anoxia before the cytosol
acidifies) (Fig. 3). Glycolysis is a cytoplasmic pathway that forms pyruvic
acid from glucose, yielding 2 ATPs from each glucose molecule. This is only
about 6 % of the ATP generated by mitochondria-based aerobic respiration. Thus,
glycolysis is highly inefficient while still requiring a plentiful supply of
glucose. It also requires pyridine nucleotide coenzyme in its oxidized form
(NAD+). The required NAD+ is generated anaerobically from
chemically reduced NADH during ethanolic or lactic acid fermentation (Fig. 3).
Unless metabolic processes that consume ATP are simultaneously suppressed, the
small yield of ATP in anaerobic cells is insufficient for survival beyond a few
hours. Suppression can be brought about if the roots are ‘trained’ beforehand
by a few hours of partial oxygen shortage (e.g., 0.04 mol m-3 in
solution or 3 % v/v in the air phase) before the supply of oxygen is finally
extinguished (Xia, Saglio, and
Roberts, 1995). Thus, an inability to restrict ATP
utilization to essential life-support processes may be at least as important a
reason for death of flooded root tips as slow ATP production. Greenway and Gibbs
(2003) conclude that early cell death can only be avoided if the small
amounts of available energy are successfully re-diverted to permit synthesis of
certain critical ‘anaerobic’ proteins (e.g., alcoholic fermentation enzymes),
that support glycolysis and fermentation and help to prevent excessive
acidification of the cytoplasm and vacuole (see below) and maintain membrane
integrity. A marked decrease of membrane
integrity may well be one of the most critical consequences of ATP imbalance
for the viability of root cells. It is a consequence of lipid hydrolysis that
is probably mediated by lipolytic acyl hydrolase (Rawyler
et al., 1999). When membrane integrity is lost, the cell is
irrecoverably damaged (Zhang et al. 1992). Unlike in some animal tissues, there
is little evidence that ion channels and carrier systems can become sealed in
response to anoxia thereby helping to retain soluble cell contents.
The modest ATP generation capability of
glycolysis/fermentation depends on a ready supply of glucose and its
precursors. Sugar shortage caused by anaerobic arrest of starch breakdown and
sugar unloading in roots can thus shorten the duration of survival. This is
illustrated by the ability of rice seeds to germinate without oxygen. Such
ability is due, in part, to its possession of an anaerobically inducible gene
coding for α-amylase, the enzyme principally responsible for degrading starch to a
range of sugars (Loreti
et al. 2003). In in vitro studies of anaerobic roots, hexose feeding
is a prerequisite for long periods of anaerobic survival of the cultures. Over
shorter time scales too (hours or several days), seedling roots have also been
found to survive longer and ferment more vigorously when given external glucose
(Webb and Armstrong, 1983), Tadege
et al., 1998). But, even when
anoxic roots are given extra hexose they die eventually, indicating causes of
death other than simply substrate-starved arrest of glycolysis. This
may be because rates of glycolysis cannot speed-up sufficiently to satisfy
demand or because ATP demand is not sufficiently down-regulated. But, other
factors also come into play. These include the absence of molecular oxygen to
support essential non-respiratory oxidative and oxygenation reactions (e.g.,
synthesis of polyunsaturated fatty acids used in membrane formation (Vartapetian, Mazliak, and Lance, 1978).
Self-poisoning
Anaerobic roots may also die from
self-poisoning by products of anaerobic metabolism;
the most notable toxin being excess protons
that acidify the cytoplasm and vacuole (Gerendás and Ratcliffe, 2002). In
support of this notion, roots of pea (Pisum
sativum), black eyed peas and navy beans, which collapse particularly
quickly when anoxic, acidify their cytoplasm more rapidly than do longer-lived
anoxic maize, soybean or pumpkin root tips. The sources of the extra protons
within the cell have proved difficult to identify (Gerendás and Ratcliffe, 2002). Another possible toxin is acetaldehyde. In
alcoholic fermentation, activity of the enzyme that converts acetaldehyde to
ethanol (alcohol dehydrogenase - ADH) usually exceeds that of the enzyme that
promotes acetaldehyde production from pyruvic acid (pyruvate decarboxylase -
PDC). Normally, this state of affairs ensures low sub-toxic concentrations of
acetaldehyde in anoxic cells. However, after such tissue is returned to air,
this control is sometimes lost and plant tissue typically generates a burst of
acetaldehyde that could be damaging (Boamfa
et al. 2003). Another potential toxin is nitric oxide (Dordas
et al. 2003). This is a free
radical gas that can be formed by the action of nitrate reductase (coded for by
an anerobically inducible gene) and possesses the ability to kill cells, as is
well-known in mammalian tissues. However,
the roles of this molecule are still very unclear and it has even been
suggested that the beneficial impact of nitrate on survival of anoxia may be an
outcome of increases in nitric oxide arising from the reduction of nitrate to
nitrite (Stoimenova et al. 2003). The
conventional view is that death of the root-tip caused by one or more of the
above-mentioned factors threatens the vigour and survival of the entire plant
since fully functional root tips are required for soil exploration, uptake of
water and mineral nutrients. However, Subiah
and Sachs, 2003 take the view that
rapid death of anoxic root tips is an adaptive response. They consider that
loss of the root tip allows the remainder of the root (with its dormant lateral
root primordia) to survive for longer, an interpretation supported by their
finding that prior removal of root tips prolongs the life of anaerobic maize
seedlings.
Although not strictly self-poisoning, cell death arising from oxidative
reactions following the re-introduction of oxygen cannot be excluded as a cause
of waterlogging injury and death. Underlying this notion is that an absence of
oxygen harms the ability of plant cells to protect themselves against the
formation and action of active oxygen species (e.g. superoxide radicals) when
the floodwater recedes and free oxygen returns to the cells. Roots of soybean
are thought to suffer in this way (Van Toai and Bolles, 1991). Most information on this phenomenon comes
from work with rhizomes and cultured cells. However, recent studies with cell
cultures do not strongly support to the view that post-anoxic damage is a major
cause of death from anoxia (Rawyler et al. 2003).
How roots survive anaerobic conditions
During natural waterlogging of the soil, anoxia will be preceded by a
period of partial oxygen shortage (hypoxia). This will last for as long as it
takes for dissolved oxygen in the floodwater to be consumed by roots and other
aerobic soil organisms. This hypoxic
interlude can act as a training period by improving the ability of the roots to
survive subsequent anoxia by inducing biochemical acclimation or anatomical
acclimation.
Biochemical acclimation
As little as 6 h prior exposure to partial oxygen shortage (typically 3
- 5 %, v/v in the gas phase) can lengthen survival time of anoxic maize root
tips from 8 h to 72 h (Saglio, Drew, and Pradet, 1988).The mechanism by which cells initially sense the partial oxygen
shortage that triggers this acclimation is unknown. One possibility is that
sensing works through a binding of oxygen to non-leguminous haemoglobin, which
is ubiquitous in plants. However, this mechanism has been ruled out on the
grounds that binding is too tight for sensitive detection of partial oxygen
shortage (Dordas
et al. 2003). Despite this, haemoglobin is undoubtedly important for anoxia
tolerance in other as yet undiscovered ways (Hunt
et al. 2002) and petunia plants transformed with a Vitreoscilla haemoglobin
gene, show remarkably enhanced tolerance to submergence (Imao et al., 2003).
Following sensing of partial oxygen deficiency,
genes coding for so-called anaerobic proteins (actually hypoxically-induced proteins
or HIPs) are up-regulated at transcriptional and post- translational levels
while others coding for many aerobic proteins remain expressed and translated
up to the point when the cells finally become anoxic. (Chang
et al. 2000; Dolferus
et al. 2003; Fennoy
and Bailey-Serres, 1995; Subiah
and Sachs, 2003; Baxter-Burrell
et al. 2003). The anaerobic proteins
(or HIPs) are necessary for the acclimation. The up-regulation of these genes
is effected by the action of proteinaceous transcription factors (e.g., Myb
factors, G-box factors, 14-3-3 proteins) that bind to promoter regions of
target genes and influence their expression. The base sequences of these
regions determine the susceptibility of a gene to any given transcription
factor. One such region is the so-called ‘anaerobic response element’
characterized by a GT/GC-rich motif. This has been associated with several
genes, such as an alcohol dehydrogenase (ADH1), that are strongly
upregulated by oxygen shortage (Dolferus
et al., 1994). HIPs can be divided into (1) enzymes involved in cytosolic
energy metabolism especially those involved in starch breakdown and the
glycolytic and fermentative pathways upon which anoxic energy generation
depends; (2) enzymes implicated in pH regulation; (3) enzymes involved in
aerenchyma formation (see later in this article); (4) enzymes with protective
functions such as scavenging for potentially damaging active oxygen species
generated when anoxic roots are returned to air; (5) proteins involved in
signal sensing and transduction (e.g., the ethylene receptor ETR), (6) others
of unidentified function. The complexity of the picture is being increased as sophisticated
methods of protein analysis such as MALDI-DE-TOF mass spectrometry (Chang
et al. 2000) become employed. Thus, HIPs play a major part in prolonging
the life of anoxic roots that previously experience at least some hours of
partial oxygen deficiency. If their synthesis is interfered with by applying
protein synthesis inhibitors or through mutations, the effect of partial oxygen
shortage on prolonging survival of subsequent anoxia is suppressed (reviewed by
(Jackson and Ricard, 2003). It is notable that translation mRNA of many ‘aerobic’ genes is
suppressed in anoxic cells.
Expression of HIP genes and production of survival
protein is complimented by a co-ordinated down-regulation of demand both for
oxygen, respirable substrates and for ATP. This suppression of demand is instigated
by modest decreases in oxygen supply and well in advance of the onset of
fermentation or any increase in NADH relative to oxidized NAD+ (Geigenberger et al., 2000). Thus, while HIP production can be seen as a preparation for anoxia,
the early down regulation of ATP and oxygen demand appears to delay the point
at which tissue anoxia actually sets in. This down regulation of ATP- and
oxygen-consuming pathways is probably underpinned by changes in gene
expression. As previously mentioned, roots that are partially deprived of
oxygen (typically 5 %) undergo marked changes in expression (Andrews et al. 1994; Klok
et al. 2002). The kinetics of the up- and down-regulation of various groups
of genes is complex with transcription factors and signal transduction pathway
genes changing soonest. The identification of gene clusters bearing common
regulatory sequences is a priority since by this means the overall
co-ordination of events will become clearer (Dolferus
et al. 2003). It will be important to understand both the down-regulation
of genes coding for energy-consuming steps and the up-regulation of genes
coding for survival proteins. Post-transcriptional processing of survival
proteins and their patterns of association will be a further priority
Anatomical
acclimation through aerenchyma formation
The presence of large interconnected intercellular gas-filled spaces that often extend from the shoots to near the root tip (aerenchyma) is feature shared by most (Justin and Armstrong, 1987b)