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) although not all
species (e.g. Caltha palustris – Seago et al. 2000) that grow well
in wet places. The spaces are created by cell separations resulting from
differential rates of division or expansion by neighbouring cells or from the
death of certain cells. The radially orientated spaces of the rice root is an
example of aerenchyma formed by the death of particular cells that takes place
mostly as a part of normal constitutive development (Fig. 4). Mathematical
modelling and direct experimentation have demonstrated that sufficient oxygen
can diffuse through such tissue from the aerial shoot to satisfy the
respiratory needs of root axes up to 30-cm-long at growing temperatures. In
certain aquatic species, pressure-driven gas flow may aerate even longer
lengths of rhizomes to which roots are attached (reviewed in (Jackson and
Armstrong, 1999). Tests with wheat
plants have shown that, without aerenchyma, roots longer than 100 mm are
fatally damaged by an O2-free medium while roots of this length
equipped with 12 % porosity continue elongating. The effectiveness of oxygen
transport is increased in species like rice where oxygen losses to the soil are
inhibited by an inducible barrier to outward radial diffusion (Colmer et al., 1998). Any oxygen leaking
radially out of the roots into the anaerobic soil can oxidise the rhizosphere
thus decreasing injury from chemically reduced toxins such as ferrous ions.
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Fig. 4. Scanning electron
micrograph showing the cortex of a young rice root where radial lines of
intact living cells alternate with gas-filled space created by cell death.
Photograph by Stewart Young. |
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Fig. 5. Summary of possible stages in
aerenchyma formation in roots of Zea mays induced by partial oxygen
shortage external to the root and mediated by increased synthesis of ethylene
that in turn induces a form of programmed cell death in target cells of the
cortex. |
However, most species are intolerant of soil
waterlogging and do not possess extensive aerenchyma (e.g., arabidopsis and
tomato) but, in some (e.g. Zea mays), aerenchyma in roots can be
stimulated during the early stages of waterlogging by the associated partial
shortage of oxygen. This morphological acclimation is the result of spatially
targetted process of programmed cell death that is localized in the root cortex
and is stimulated by increases in ethylene concentration (Drew et al. 1979) brought about by entrapment and by faster biosynthesis; the latter being favoured by
low but not extinguished oxygen supply e.g. 0.68 mol m-3 or 5 % v/v
oxygen) (Fig. 5). The additional ethylene is trapped within the
flooded roots by the floodwater and acts on files of target cells in the cortex
resulting in their disassembly to create longitudinally interconnected gas
spaces. Processes of cellular disassembly that destroy the cell are only
partially understood and the state of knowledge is summarised in Fig. 5. This so-called lysigenous aerenchyma is the
outcome of an ordered set of structural degradative changes (lysis) that
commence within 6 h and destroy the cell in 2-3 d. These changes include, acidification of the
cytoplasm, possible loss of control of cytoplasmic Ca++, a loss of
microtubule orientation, plasmamembrane invagination, the formation of
membrane-bound vesicles and, the appearance of membrane bound organelles,
internucleosomal DNA fragmentation, chromatin condensation and changed patterns
of pectin methylation in cell walls (Gunawardena
et al. 2001a) and (Gunawardena et
al., 2001). The
features of those cortical cells that confer target status for ethylene
induction of programmed cell death remain elusive.
How
above-ground shoots survive soil waterlogging and submergence
It is
inevitable that, because of the close functional interdependence between roots
and shoots, stress on roots from soil waterlogging also threatens the shoot
system. One example of this is the arrest of nitrate uptake that arises from
microbial de-nitrification and damage to uptake mechanisms from an absence of
oxygen. Young leaves then take this nutrient from older leaves leading to
premature senescence in the latter (Drew and Sisworo, 1977). A second example of this knock-on effect on
shoots is the tendency of waterlogged plants to wilt severely in bright light.
This paradoxical response to waterlogging of the soil is the outcome of a
lowered conductivity to water uptake that typifies oxygen-deficient roots and
is brought about by proton induced conformational changes to water channel
proteins (Tournaire-Roux
et al. 2003).
Root to
shoot communication and shoot-water conservation
The
tendency for leaves to dehydrate irreversibly (Fig. 6) in response to increases
in root hydraulic conductivity is ameliorated by rapid signalling from roots to
shoots that results in a slowing of water loss from the foliage. This is
achieved by a prompt decrease of stomatal apertures, leaf expansion and, in
tomato at least, by marked petiolar epinasty. Epinasty is the outcome of a
downward re-orientation of whole leaves and leaflets that involves growth
promotion on the upper (i.e., adaxial) surface. Epinasty reduces the amount of
energy incident on the foliage and thus will slow the rate of water loss.
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Fig. 6. Sunflowers suffering from wilting in the sun during an
episode of summer waterlogging. (Photograph supplied by LACJ Voesenek) |
The
signals inducing these effects in the shoots have been reviewed recently (Jackson,
2002) and, in the main, comprise increases (positive messages) or decreases
(negative messages) in the flux of regulating hormones, or related substances,
carried to the shoot in xylem sap. The signalling processes controlling
epinasty in tomato are well understood, involve ethylene and can be summarised
as follows. Severely hypoxic or anaerobic roots were shown to generate a
positive message that (Bradford and
Yang, 1980) showed
later to be the ethylene precursor 1-aminocyclopropane-1-carboxylic acid
(ACC). The amounts have been estimated using
mass spectrometry and are demonstrably sufficient to enrich the shoot tissues
with enough ACC to support the faster shoot ethylene production needed to
induce epinasty (Else
and Jackson 1998). The release of
large amounts of ACC into xylem sap by anaerobic roots has two probable
causes. The first is a blocking of ACC
oxidation to ethylene by the absence of oxygen. This promotes a build-up of
ACC. Some of this enters the transpiration stream and is drawn in to the shoot
by transpiration steam as positive message. This enrichment has been shown in
tomato and in xylem sap of R.
palustris. The second putative
cause is an up-regulation, and presumed translation of one member (LE-ACS7) of the six-gene family of ACC
synthases responsible for forming ACC from its precursor S-adenosyl-L-methionine. Up-regulation occurs within 1 h and takes
place along with a rise in ACC concentration in roots and enhanced ethylene
production in the leaves (Shiu
et al. 1998). Changes in gene
expression and enzyme levels also enhance the oxidation of ACC on its arrival
in the shoot since the ability of petioles to oxidase ACC to ethylene increases
within 6 h (English
et al. 1995) along with a rise in ACC oxidase mRNA. However, it remains
unfortunate that detailed time courses of ethylene production using modern
sensors such as photoacoustics,
are not available to confirm the link between the onset of epinasty and
increased shoot ethylene production.
Fast stomatal closure is often seen in many
species soon after waterlogging begins but has proved difficult to explain. In
tomato, many potential signalling messages such as increases in delivery of the
hormone abscisic acid (ABA), sharp decreases in mineral nutrient delivery or
increased xylem sap alkalinity have received little support, although in Ricinus
communis, temporary dehydration of the leaves induced by severely decreased
root hydraulic conductivity appears to trigger stomatal closure that is
mediated by ABA (Jackson et al.,
2003). Other
less well-researched possibilities for root to shoot signalling in waterlogged
plants involve decreases in pH and in the delivery of cytokinin or gibberellin
hormones. In addition to possibly contributing to closing the stomata these
changes may also help explain other shoot responses to soil waterlogging such as
depressed stem elongation rates and faster leaf senescence.
Root to
shoot signalling is best seen as a stop-gap mechanism that rapidly reduces the
need for root-sourced supplies such as water and minerals at a time when root
activities are suppressed by inadequate oxygen. But, if the roots remain
inactive, or are killed and not succeeded by functional replacements, the shoot
will not survive and the plant will then fail in its entirety. For longer-term survival of the plant, oxygen
must be introduced into the interior of roots in amounts that support
respiration and activities such as mineral and water uptake. Alternatively,
replacement roots must develop that are better aerated than their predecessors.
In species with adaptive capacity, shoots respond to flooding in ways that
favour such changes. These are discussed briefly below.
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Fig. 7. Two examples
of reactivation of development at the shoot base caused by soil waterlogging.
A. Aerenchyma formation in the leaf base of Zea mays. B. Hypertrophic lenticels at the stem base of
young apple plants (Malus domestica) waterlogged for 40 days
(adventitious roots removed for clarity). Photographs by the author. |
Increased
porosity of the shoot base
In many
species the shoot base become morphogenetically activated when plants are
waterlogged, especially if the shoot base itself becomes water- covered. In Z. mays, the base of outer
leaves form aerenchyma (Fig 7A) and studies in rice reveal a link with
transverse veins and a distinct interconnectedness between the cells that
eventually die to create the aerenchyma (Matsukura
et al. 2000). In many dicots, swelling of submerged
portions of the lower shoot and the development of swollen stems and
hypertrophied lenticels are common. These effects probably enhance flooding
tolerance by promoting tissue gas exchange, although experimental data
demonstrating this are elusive. Swelling and hypertrophic lenticels are seen in
many herbaceous dicots and woody species (e.g., apple – Fig. 7B) (Hook and Brown, 1973). Experimental blocking hypertrophic lenticels with
lanolin grease has been shown to decrease oxygen entry into nearby roots via
intercellular spaces and aerenchyma. This oxygen is then potentially available
to support root functioning and also the formation and emergence of new
adventitious roots nearby (see next section). Hypertrophic lenticels may also
allow dissipation of metabolically generated volatiles such as ethanol,
ethylene and acetaldehyde, although the physiological significance of this for
plant performance and survival has not been examined. The leaf-base aerenchyma,
and swelling of stem-base and lenticels are probably consequences of cell
expansion promoted by endogenous ethylene trapped in the submersed tissue by
the water covering (Kawase, 1974).
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Fig.
8. Effect of approximately two weeks
waterlogging on the formation of replacement adventitious roots at the soil
surface by plants of [A] maize (Zea mays) and [B] sunflower (Helianthus
annuus). In A, the roots are outgrowths of pre-existing primordia. In B,
the original root system has been killed and replaced by newly initiated
roots formed at the shoot base and hypocotyl. Both mechanisms generate a root
system with improved access to aerial oxygen |
Replacement rooting
Species with
inherently surface-inhabiting root systems are notably tolerant of prolonged
waterlogging (Justin and
Armstrong, 1987a). However, if
those species with deeper and thus more vulnerable roots are to revive, they
must form replacement roots positioned near or at the better-aerated soil
surface. There are three mechanisms for generating these replacement root
systems. One is a stimulation of the outgrowth of root primordia already
present within the shoot base (e.g., in Zea mays - Fig.8A). A second is the induction
of a new root system that involves initiation of root primordia and their
subsequent outgrowth (e.g. in Helianthus
annuus [Fig 8B] and Rumex palustris). Ethylene seems to be involved
in both these processes. Applications of the gas to Z. mays strongly
promotes primordial emergence (Jackson et al.
1981) although
subsequent elongation is inhibited in association with aerenchyma formation. In
nature, this inhibition may be mitigated by internal ventilation of ethylene
out through the aerenchyma (Visser et al. 1997). Where
replacement rooting involves initiation of new root primordia, auxin and
ethylene are both thought to interact to bring this about (Visser et al., 1996). A third
mechanism of placing roots at the soil surface involves a re-orientation of the
root extension. Lateral roots of certain species grow upwards in waterlogged
soils (Pereira and
Kozlowski, 1977); Gibberd et al. 2001). When they
reach the surface, they offer a replacement pathway for aeration of other
attached roots provided there is adequate internally interconnected
aerenchyma.
Fast upward shoot elongation
Another
developmental effect of flooding, that supplements the aerenchyma system, is
the promotion of shoot extension and/or increased uprightness of submerged
leaves (Grimoldi et al. 1999; Cox et al. 2003, ). These responses are mostly found in aquatic
or amphibious species well-adapted to periodically flooded areas or to rising
water levels (e.g., rice and water lilies). The resulting increase in effective
plant height, that can begin after a delay of less than 2 h of inundation,
improves access to aerial or dissolved oxygen or to light for the generation of
photosynthetic oxygen. In appropriate species, this oxygen can diffuse readily
to the root elongation zone and elsewhere through aerenchyma (Waters et al.,
1989). Internodes of
the highly compressed stem in the base of the shoot of Z. mays are also
stimulated to elongate when water levels cover just the shoot base. This raises
the height of the ring of replacement roots emerging from a basal node. For the most part, the promotion of
elongation by shoot or leaf are primary responses to ethylene entrapped in the
growing tissue by the floodwater (Musgrave,
Jackson, and Ling, 1972). The hormone is
known to act in conjunction with gibberellins and/or with auxin to stimulate cell
extension. This effect is in marked contrast to the effect of ethylene on
less-well adapted species, where the gas most often strongly inhibits shoot
elongation. In stems of deepwater rice (Kende
et al., 1998) and petioles of Rumex palustris (Voesenek
et al., 2003), faster underwater elongation is strongly dependant on a
prior degradation of the growth-inhibiting hormone abscisic acid. Faster
extension is also associated with the expression of a gene encoding a member of
the family of cell-wall loosening enzymes known as expansins and with the
up-regulation of an ethylene receptor gene (Voesenek
et al., 2003). The range of species
that utilize ethylene in this depth-accommodation response is wide and includes
dicots, monocots and at least one liverwort and a tropical fern (Regnellidium
diphyllum) (Table 2). However, the mechanism is not universal. In Potamogeton
pectinatus, submerging the stem promotes elongation even though the plant
is unable to synthesise ethylene itself because of ACC oxidase activity is
lacking (Summers
et al., 1996). Leaves of rice seedlings may also respond to a signal other
than ethylene (Ella et
al., 2003). Clearly, some other signal can be generated by submergence that
is responsible for stimulating elongation. That signal may comprise accumulated
carbon dioxide or partial oxygen shortage since rice coleoptiles elongate
faster underwater in response to their collaborative effects as well as to
ethylene. In the stems of deepwater rice, these signals act more independently (Kende, 1987).
Young rice seedlings are readily submerged in water too deep for them to
escape by means of fast upward elongation. In these circumstances, the
expenditure of energy imposed by the faster growth rates may prejudice their
survival. Survival is also challenged by more extensive leaf senescence that is
promoted by accumulated ethylene (Jackson
and Ram, 2003; Ella
et al. 2003). In lowland rice types, those most tolerant to several days of
total submergence as small seedlings (e.g. FR13A) are usually those that
elongate very little underwater while retaining a full set of green leaves.
The
most severe stress that flooding can impose on the shoot is total immersion in
dark, anaerobic surroundings. Green leaves of some species tolerant of total
submergence and of icing-over in arctic environment have the ability to survive
such conditions, as do perennating organs of many temperate wetland species (Crawford
and Brändle,1996; Schlüter and Crawford, 2001). A
variety of biochemical adaptations reminiscent of those discussed earlier for
roots are involved although studies with the dicot seedlings of Arabidopsis
thaliana (Ellis
et al. 1999) indicate that the biochemical pathways involved in adaptation
to very low oxygen supply (approx. 0.1 %) may be different in roots and shoots.
In addition, a select group of species including Potamogeton pectinatus,
Potamogeton distinctus, Sagittaria pygmaea and rice can respond to a
complete absence of oxygen by elongating their stem (or coleoptile in rice)
much more quickly in an upward, gravity sensitive manner for many days. The
biochemical basis of this remarkable achievement includes being able to degrade
starch anaerobically and to sustain a fast rate of glycolysis in the growing
parts (Summers
et al. 2000). The faster growth is
principally the outcome of enhanced cell extension linked to the promoting
action of low pH and to the action of auxin that is implicated in anaerobic
gravity sensing (Summers
and Jackson, 1996). This stimulation of upward shoot elongation by a
complete absence of oxygen is coupled with a marked constitutive aerenchyma.
The two features together constitute a mechanism of survival by escape from
flooding stress by means of upward elongation. But in this case the signal
promoting fast elongation is, surprisingly, the complete absence of oxygen,
even when this most severe stress is prolonged for many days
WATERLOGGING AND CROP
PRODUCTION
·
Remedial measures in crop production
o
Improving land drainage
o
Direct
treatment to crops
o
Plant breeding
Based on soil typing, (Dudal, 1976)
estimated that 12 % of the World’s soils are likely to suffer from excess water
while (Boyer, 1982)
indicated that about 16 % of US soils
experience excess water. Clearly, considerable transient and more persistent
waterlogging of the soil and deeper submergence of crops occurs in much rainfed
farmland world-wide. The extent of its occurrence remains speculative. This is
because of a lack of useful definitions of what constitutes excess water
content. The transient nature of most farmland flooding also frustrates
accurate estimation of the extent of farmland waterlogging. One potentially
useful rule of thumb (discussed in Setter and Waters, 2003) is the SEW30
value. This value (as centimeter days) combines all the days in a growing
season when excess water is present in some or all of the top 30 cm of the soil
profile (i.e. the zone in which most roots are usually to be found). Values of
about 100 – 200 cm d are often sufficient to depress crop growth in temperate
growing conditions.
Despite the uncertainties of quantification, it is
possible to give examples to indicate the scale of the problem. Through such an
approach we can appreciate that although statistically, floods are amongst the most common and widespread of all
natural disasters and the effects are sometimes catastrophic (e.g., Mozambique in 2000), it is
the more mundane persistent inadequacies in soil drainage in the face of
near-average or modestly excessive rainfall that constrain farm productivity
year by year (e.g., Fig. 9).
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Fig. 9. Left - typical
late spring waterlogging of poorly drained field of peas (Pisum sativum)
in Cambridgeshire, UK. Right –
close-up of the injury sustained by leaves of a pea plant after several days
soil waterlogging. |
Waterlogging
damage to crops may sometimes occur when crops are irrigated. The dividing line
between adequate and excessive irrigation is not well defined and it is
probable that some of the benefits can be lost by heavy-handed irrigation. For
example, ponding on the soil surface for more than a day is known to be harmful
to wheat watered by flood-irrigation.
Prolonged irrigation over many years in dry regions can cause
waterlogging problems created by raising the water table. A well-known example,
already mentioned, is to be found in the Sindh Province in the Indus Valley of
Pakistan. Here, 50 to 60 years ago, the watertable was 4 m below ground. By
1980s it had risen to between 1 – 2 m over most of the irrigated region and the
water being highly saline. A multimillion-dollar drainage project (the Left
Bank Outfall Drainage project) intended to reverse the situation and funded by
the World Bank and the Asian Development
Bank is in place but not without causing controversy and additional environmental
concerns.
The extent of damage to yield depends heavily on the stage of development
as well as on more obvious factors such duration of waterlogging and
temperature. For most crops, seed germination is probably the most vulnerable,
reflecting both the fast metabolic rate of germinating seeds being coupled with complete inundation. Studied examples include peas (Jackson, 1983) and temperate cereals (Lynch et al., 1981), (Setter and Waters, 2003). Problems are exacerbated if germination
takes place in association with decomposing organic matter such as straw
residues from the previous crop. Microbial colonization of such residues
depletes the soil of oxygen and nitrate while discharging potentially harmful
substances such as unsaturated fatty acids and the growth-inhibiting hormone
abscisic acid. Leaking of soluble carbohydrates from seeds is stimulated by
anaerobiosis and this also encourages fungal pathogens such as Gliocladium
roseum. Seeds of rice are
exceptional in being able to germinate in flooded soil without oxygen. But the
germination is abnormal since only the coleoptile but not the root or the
mesocotyl or leaves emerge from the embryo without oxygen. Elongation by the
emerging coleoptile is stimulated under these conditions by a combination of
lack of oxygen, carbon dioxide and ethylene. Underpinning this is the ability
of rice seeds to hydrolyse endosperm starch to sugars by means of anaerobically
transcribing genes, such as the Ramy3D α-amylase gene, that are
up regulated by the associated low sugar levels (Loretti
et al. 2003).
Once
germinated, stages in subsequent development of crop plants influence
susceptibility to flooding injury. Small cereal seedlings with their shoots
below ground are highly susceptible (e.g., winter wheat – (Cannell et al. 1980) but thereafter tolerance rises until early reproductive stages when
susceptibility again increases (e.g. in soybeans - Linkemer
et al. 1998). Heightened vulnerability at or just before flowering has also
been noted for several other crops including peas, wheat, sorghum, maize and
cow peas (Cannell and Jackson, 1981) when inundated for one or more days. By contrast, several weeks of waterlogging in
winter of young plants of crops such as autumn sown wheat or oil seed rape
causes little yield loss because of compensatory growth in the following spring
and the slower metabolic demands created by cool temperatures during the period
of waterlogging.
Unlike other major crop species, rice can yield heavily when grown in waterlogged soil (paddy rice production) and specialized ecotypes are able to yield usefully even when partially submerged in several meters of water (Catling, 1992). This ability is based partly on ethylene-mediated stem elongation that is induced when the shoot base becomes submerged. However, it is less widely recognized that these do not readily escape total submergence. Small vegetative rice plants (even of the so-called deepwater ecotypes) are totally submerged for only a few days as a result of uncontrolled flooding in lowland areas, they are severely damaged or killed. Part of the problem is thought to be that stimulated leaf elongation and associated ethylene-promoted leaf senescence quickly deprive the young plants of starch and sugars, thus prejudicing their survival and re-growth potential (Jackson and Ram, 2003),
Remedial measures in crop production
A comprehensive
treatment of remedial measures is outside the scope of this review. However, a
brief account of various approaches is given. It pre-supposes that, where
appropriate, measures such as installing protective barriers against water
inflow from rivers or the sea are installed in association with high-volume
pumping systems. The creation and maintenance, by these means, of highly
productive farmland in reclaimed coastal areas of The Netherlands
represents the pinnacle of achievement in this regard. A common feature in the management of this
and other riverine farmland (e.g. The Mississippi floodplain) is the building
of dykes or levees (long high banks) along rivers to prevent them from overflowing
or at least displacing the flooding to lower reaches of the river. The approach
has its dangers.
Improving land drainage
Estimates of the areas of drained farmland that have been published for
several major arable-cropped regions. While highly approximate, they serve to
illustrate the enormous scale of the problem of farmland waterlogging and the
key role of drainage systems in supporting economically viable agriculture.
Nosenko and Zonn (1976 - quoted by Cannell and Jackson 1981) estimated that 155
million ha carried subsurface land drains. Much draining has been installed in
the last 50 years (e.g. 6 % of UK farmland received new drains between 1940 and
1970). Most of these systems have been installed to arbitrary drainage targets,
reflecting the scarcity of drainage experiments on representative soils.
According to
Trafford (1975), installation of drainage systems may be motivated by four
rather different sets of circumstances. (1) Where reclamation of flooded land
is needed before conventional agriculture is possible (see above); (2) where
farming of a given crop may have to be abandoned unless drainage is installed
(e.g., white lupin production on the south coast of Western Australia); (3)
where improved drainage is needed to support more intensive and higher-value
cropping and (4) drainage to improve the yields and profitability of an
existing cropping system. In situations (3) and (4) the availability of
subsidies to fund part of the cost of installing land drains may affect the
financial viability of installing land drains. On a clay soil in the UK, even a
28 % improvement in yields of winter wheat reported over a six year period
after installing pipe and mole drains would not have been an economic
investment unless installation was subsidized by government grants (Hunter and Trafford, 1979). Such subsidies are no longer available in the UK and much of western
Europe. However, less financially
accountable benefits such as a marked increase in the number of days the
drained land can bear heavy farm machinery without damage must not be ignored.
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Fig. 10. Example of specialized heavy equipment, often
employing laser-guided gradient sensing, to install subsurface plastic
drainage pipes in arable farmland |
Mention has already
been made of Pakistan's Left Bank Outfall Drain (LBOD) project, one of world's
largest drainage schemes. It highlights the installation of land drainage
schemes as one of the most widely adopted means of decreasing the incidence of
farmland waterlogging. At the individual
farm level, measures for improving drainage range from simple and historically
interesting ridge and furrow constructions
(basically creating raised beds for the crop - system sometimes used in Australia) to the
installation of complex subsurface land drains designed to meet target drainage
flows and installed using laser-guided drain layers that insert perforated
plastic piping to precise depths and gradients. The use of such systems is
illustrated by guidance given by the USDA-Agricultural
Research Service to sugarcane growers in Lower Mississippi River
Valley (LMRV). The machinery used in such work can be formidable (Fig.
10). In contrast the simplest subsurface
land drains are those created in clayey soils using a 'mole' that is dragged
through the soil at a depth of about 50 cm. Despite its seeming simplicity,
powerful tractors are still required for its execution (Fig. 11). A combination of the two forms of drainage
installation is especially effective. Other means of lowering the water table
include the judicious planting of waterlogging tolerant trees such as certain eucalyptus species, guava and mango that also produce a
useful crop for cash-poor
farmers in poorly developed tropical regions. Eucalyptus aggregata, E.
camphora, E. crenulata, E. gunnii & E. gunnii divaricata are
especially tolerant of waterlogging. In New Zealand and Tasmania they grow
naturally in undrained peat moors where surface water is present for at least
six months of the year. They also tolerate stagnant water just below the
surface (unlike poplar and willow). They are, however, stunted on permanently
flooded soils. Another approach aimed at reducing the rate of water input into
the lower reaches of floodplains such that of the River Rhine in northern
Europe, is to retain as much water as possible upstream. This can be improved
by preserving and improving what remains of upstream flood plains (so-called soft engineering).
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Fig. 11. A prototype, laser-guided mole
drainer built by the Agricultural Research Service of the United States Department
of Agriculture. The ‘mole’ is the bullet-shaped foot of the vertical knife
that is drawn through the soil. |
Direct treatment to crops
Remedial
effects can be observed after applying nitrogen fertilizers as a foliar spray. There
is evidence of beneficial effects of this on the yield of cotton http://cotton.crc.org.au/Publicat/Agro/waterlog.htm.
Cereals may also benefit from soil applications of N provided the plants are
only moderately damaged. In Western Australia,
100kg N ha-1 or more raised yields of
small grain cereals waterlogged for 3-7days but little benefit is seen in
more severely damaged crops. The use of additional nitrogen to offset
waterlogging damage has support from basic physiological investigations. These
show that applied nitrate may enter anaerobically damaged roots by passive means
and be translocated to the shoot. The nitrate may also act simply to replace
that leached in the drainage water or destroyed by anaerobic denitrifying
bacteria (Trought and Drew, 1981).
Germinating seeds have been identified as being especially
vulnerable to damage from soil waterlogging and the associated anaerobiosis and
injury from chemically reduced metabolites such as organic acids and
respiratory intermediates such as acetaldehyde. It is therefore not surprising
that pre-treating seeds with an oxidizing coat has been tried as an insurance
against such effects. Coatings include calcium hydroxide and calcium peroxide
(Sladdin and Lynch, 1983), although the effects on rice
have not always been positive. There are companies
selling products that promise to improve plant growth by using calcium peroxide
to ‘inject’ oxygen in to the soil. A more mundane approach in situations where
germinating seeds risk contact with undegraded crop residues in wet conditions,
is to rotovate and dice these residues or remove them before sowing, possibly
by burning if legislation allows this.
Plant breeding
As with other major abiotic stresses, breeding and selecting successful
tolerant cultivars have not yet met with notable commercial success although
Setter and Waters (2003) report that a waterlogging tolerant wheat cultivar
suitable for Australian conditions is close to being released. This has been
derived from doubled haploid (DH) lines generated by crosses with tolerant
wheat originally selected by the International Maize and Wheat Improvement
Center (CIMMYT) in Mexico. Despite this limited progress, there are numerous
indications that the production of cultivars with improved tolerance that also
retain their desirable agricultural traits is a realistic prospect for several
major food crops. The utility value of
much published work depends on the criteria used to assess tolerance. Not all
reports compare final yields, or include non-waterlogged controls in their
trials. Nevertheless, a basis for future
successful breeding can be found in reports of greater than normal tolerance in
a number of major crop species, or allied species that could perhaps be
employed to introduce tolerance traits through ‘wide hybridization’. For
example, waterlogging-tolerant accessions have identified in seven
of the eight taxonomic sections in
Trifolium when compared in terms of relative growth rates. Several
lines of soybean
and of winter
wheat have also been shown to posses unusually high
tolerance on the basis of injury levels and final yield. Comprehensive tests in
the glasshouse and in the field over several seasons and involving yield
comparisons of over 20 cultivars (Musgrave
and Ding, 1998) revealed notable tolerance in two lines of winter wheat
that was positively correlated with iron-rich surface deposits on the roots,
implying a link with increased amounts
of aerenchyma. Based on levels of chlorosis in waterlogged spring wheat, (Boru et al. 2001)
concluded that tolerance was largely controlled by four genes with beneficial
effects that could be additive. (Setter and Waters, 2003) have assessed, in detail, many other reports of inheritable variation
amongst the major small-grained cereals. Examples of variability in tolerance
in a variety of other crops are given by (Cannell and Jackson, 1981).
Linking tolerance with
identifiable phenotypic traits, such as aerenchyma may help guide evaluation
and selection processes associated with breeding. For example, Garthwaite et al. (2003)
linked tolerance in certain wild accessions of Hordeum and a modern
barley cultivar with both constitutive aerenchyma in the roots and with the
development of an effective barrier to radial oxygen loss that renders internal
oxygen transport towards root tips more efficient. Interestingly, this barrier
developed most strongly in accessions collected from naturally wet
habitats. However, in a recent survey of
spring wheat lines (Boru et al. 2003) could
not link aerenchyma and tolerance. Instead more tolerant types adopted
abnormally fast aerobic respiration rates as external oxygen supplies
decreased. Despite this finding, the possession of a highly porous aerenchyma
system in association with slow radial losses remains a high priority marker
for waterlogging tolerance that may also be introduced through wide
hybridization (Comis, 1997).
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Fig. 12. Trial illustrating the superior tolerance to 10 days complete
submergence of a line of rice (FR13A)
derived from an old Indian farmer variety (left line of green plants)
compared with two other lines of lowland rice (right). Photograph by Dr P.
Bhekasut, Thailand Department of Agriculture and previously published in Jackson
and Ram (2003). |
Breeding flood-tolerant crops would be assisted
by the development of reliable genomic markers that are linked closely to key
tolerance traits. A prerequisite is the existence of inheritable tolerance and
Quantitative Trait Locus (QTL) mapping of the traits on to a chromosome linkage
map. This is being attempted in soybean using
homozygous Random Inbred Lines (RILs) derived from crosses between tolerant
lines obtained from
backcrossings (Siangliw
et al. 2003).
Molecular markers for submergence tolerance in rice are becoming even
more dependable as fine mapping identifies sequences that are ever closer to
the actual gene(s) responsible for conferring tolerance (Toojnda
et al. 2003).
A more long-term approach, requiring prior knowledge of key traits or
pathways affecting tolerance, is genetic transformation. The limited progress
so far is not without promise. (Quimio et al. 2000) reported improvements to submergence tolerance in rice by transforming
rice with a gene (rice pdc1) coding for pyruvate decarboxylase
the presumed rate-limiting step in ethanolic fermentation. A similar result has
been obtained with arabidopsis
but not in tobacco.
According to Zhang
et al. (2000), tolerance to submergence or to waterlogging of the soil can
also be improved by transforming arabidopsis with a bacterial isopentenyl
transferase gene that enhances cytokinin hormone production when associate with
a senescence promoter sequence. Petunia
and arabidopsis transformed to over express a haemoglobin gene have also shown
remarkable resilience to submergence stress (Imao et al., 2003) or
severe hypoxia (Hunt
et al. 2002). Neither species can by
considered a major crop but similar transformations using important food crop
species are anticipated.
ACKNOWLEDGEMENTS
I thank Dr T.D. Colmer (
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