Download Oxygen and environmental stress in plants

Proceedings of the Royal Society of Edinburgh, 102B, 1-10, 1994
Oxygen and environmental stress in plants - an overview
George A. F. Hendry
NERC Unit of Comparative Plant Ecology, Department of Animal and Plant
Sciences, The University, Sheffield S102TN, UK
and
R. M. M. Crawford
Plant Science Laboratories, Sir Harold Mitchell Building, The University,
St Andrews, Fife KY169AJ, UK
Introduction
The Galileo satellite during its recent passes close to the Earth recorded a planet
with an unusual red-absorbing pigment, a poisonous atmosphere, simultaneously
rich in oxygen and in methane, with strong, modulated, narrow-band, radio emissions in the MHz frequencies (Sagan et al. 1993). To an observer visiting the solar
system, these features; the photo-oxidisable pigment chlorophyll, abundant atmospheric oxygen, the existence of reducing conditions and intelligent life might well
appear self-contradictory. While intelligent life is a recent event, the presence of
other forms of life based on photosynthesis and survival under both oxygen-rich
atmospheres and reducing conditions go back to the earliest times (Table 1). Life
on Earth has evolved over nearly 4 G years under atmospheric environments ranging
from anoxia, to hypoxia, to hyperoxia (relative to the present day), and not always
in that sequence.
Table 1. Major steps in oxygen evaluation.
M years ago
Origin of earth
Organic chemical evolution
Indirect evidence of biological processes
Evidence of widespread oxidation
Photosynthetic stromatolites
Trace amounts free atmospheric oxygen
Extensive bands oxidised deposits
Permanent atmospheric O2 (< 1% present)
Emergence eukaryotic cell (algae)
First land plants
Late Silurian atmosphere < 10 kPa O 2
Late Carboniferous atmosphere > 30 kPa O2
Late Permian atmosphere < 15 kPa O 2
Late Cretaceous > 27 kPa O 2
Evolution C4 photosynthesis
Emergence distinct Homo
4400
>4100
3800
3500
3400 (or earlier)
3000
2300
2000
2100
420
400
290
250
65
7
2.5
Sources: Frakes (1979); Schopf (1983); Berner & Canfield (1989); Berner
(1991); Ceding ^ al. (1993).
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2
G. A. F Hendry and R. M. M. Crawford
Oxygen and evolution
Evidence from extensive sedimentary and other deposits found in all major palaeocontinents (Table 1) shows that oxygen has formed a significant part of the global
atmosphere for at least 2 G years. Atmospheric oxygen may have played an important role in sulphur oxidation as early as 3.4 G years (Ohmoto et al. 1993). However,
our information on past atmospheric oxygen has changed in recent years; the notion
of land plants evolving 400 M years ago under an atmosphere of low but steadily
rising concentrations of oxygen is, undoubtedly, too simple. The further assumption,
still pictured in some textbooks, of oxygen rising from a low value, more or less
without interruption, from the newly colonised harsh sun-baked mud-flats of the
Silurian to the high value today of 21 kPa is over simplistic. Data ranging from
rates of burial and weathering of organic carbon, as well as ratios of carbon
deposition to FeS oxidation, to the evidence of deposits of fire-derived fusinites, and
analyses of palaeogases trapped in amber, have revealed a much more complex
picture of oxygen (and CO2) in the atmosphere over the past 400 M years (Table 2;
and see studies of Berner & Canfield 1989; Chaloner 1989; Robinson 1991; Landis
& Snee 1991). The greater part of land plant and later angiosperm evolution and
subsequent speciation occurred under atmospheres considerably richer in both of
these gases than at present (Hendry 1993). Upper Carboniferous and Upper
Cretaceous values for atmospheric oxygen as high as 30 kPa, or more, have been
calculated (Berner & Canfield 1989) and supported by independent, though still
controversial, evidence (e.g. Landis & Snee 1991). It would seem that the atmosphere
of today with 21 kPa O2 and 30-40 Pa CO2 is actually untypical of past atmospheres
where higher concentrations of O2 and CO2 and higher CO2/O2 ratios will have had
Table 2. Changes in climates, plant productivity and atmospheric oxygen (partial
pressures at sea level) over the Phanerozoic
Period
(M years
before present)
Climate
and plant
productivity
Past partial pressures
of O2 in relation to
to present day values*
Devonian
(410-360)
Carboniferous
(360-285)
Dry to arid
0.8-1.2 x
Warm, wet with
high photosynthetic
productivity
Mass extinctions,
cold
Warm to tropical,
dry to arid
Warm, cycad gymnosperm
fern forests
Tropical temperatures,
high photosynthetic
productivity
Warm, wet tropical
vegetation
Cooling, dry grassland.
C4 plants from 7 M years ago
Declining temperatures
up to 2.0 x
Permian
(285-245)
Triassic
(245-210)
Jurassic
(210-145)
Cretaceous
(145-65)
Lower Tertiary
(65-30)
Upper Tertiary
(30-2)
Quarternary
(2-present)
down to 0.7 x
0.8 to 1.0 x
0.9 to 1.2 x
up to 1.5 x
declining to 1.3 x
declining to 1.1 x
l.Ox
* After Berner & Canfirld (1989).
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Oxygen and environmental stress in plants
3
a considerable influence on past rates of photosynthesis, nitrogen processing, plant
productivity (Raven & Sprent 1989; Raven 1991) and plant evolution (Hendry 1993).
Oxygen and plants
Regardless of the partial pressures of atmospheric oxygen today or in the past, land
plants are unique in biology; while the chloroplast is the site of oxygen released
from water giving rise to a measurable degree of hyperoxia during high rates of
photosynthesis (at least in bundle sheath cells of C4 plants and in some CAM plants,
Raven et al. (this volume; 1994), the same plant can, simultaneously, have its
underground parts bedded in an oxygen-depleted environment. The plant has, simultaneously, to cope with conditions of potential oxygen toxicity in the chloroplast of
the actively photosynthesising leaf and face the problems of survival of whole
underground structures such as the root or rhizome systems under low oxygen
supplies for days or weeks (Barclay & Crawford 1982). Land plants seem to have
adapted to both conditions with varied success. Tolerance of conditions approaching
photosynthetically-induced hyperoxia is likely to be obligatory to most land plants,
at least to those able to achieve even moderately high rates of photosynthesis.
Tolerance of hyperoxia or even oxygen formation in the chloroplast is both a feature
and function of the healthy green leaf. Disease, mineral deficiencies, metal and
gaseous pollutants, water and temperature stress can upset this tolerance, to varying
degrees, resulting in loss of tolerance of oxygen leading to oxidative damage (see
below). Survival of anoxia (or near anoxia) for any prolonged period is an adaptation
achieved by plants on a much more limited scale. What determines the form of
anoxia survival is a complex adjustment of anatomy and biochemistry (see in this
volume: Armstrong & Armstrong, Joly, Pfister-Sieber & Brandle, Sorrell et al.). The
relief from anoxia that rapidly accompanies restoration of supplies of oxygen to
anoxia tolerant rhizome tissues (post-anoxia) has analogies (or even homologies) to
reperfusion injury following ischaemic heart failure in animals (see Crawford et al.,
this volume). The analogies are particularly close because the heart, the rhizome
and the leaf obey identical physical laws of thermodynamics; all three are dependent
for function or prolonged survival on oxygen while accommodating its potentially
reactive and destructive unpaired electrons (see below); all three rely for protection
from oxidative damage on exactly the same suite of radical scavengers (anti-oxidants)
known in human nutrition as (pro)vitamins A, C and E or in chloroplast biology
as carotenoids, ascorbic acid and tocopherols.
Oxygen toxicity
Oxygen is both essential to almost all eukaryotic life and yet is also intimately linked
to ageing, disease and death. These two faces of oxygen have been commented on
many times. Oxygen is directly involved as a substrate or product in several hundred
enzyme-catalysed reactions in biology (see table 1 in Hendry, this volume). The
same oxygen is, chemically, highly reactive; its reactivity residing in its electronic
configuration. The oxygen atom O and the molecule O2 each have two unpaired
electrons and both are therefore, by definition, free radicals. Fortunately for biology,
these particular free radicals are not as reactive as their status implies; the two
unpaired electrons are of parallel spin (in the ground state) so in order to fill the
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4
G. A. F Hendry and R. M. M. Crawford
vacant orbitals pairs of electrons from other atoms or molecules are required but
only provided they too are of parallel spin, whereas the laws of spin restriction
demand that pairs of electrons from the same orbital have opposite spins. For this
reason ground state O2 tends to accept additional electrons one at a time. It is the
one unpaired electron form of O2, superoxide (O2~) or its protonated form HO',
which is widely associated with oxygen reactivity in biology. This readiness to share
or accept single electrons allows oxygen to react readily with transition metals such
as Fe 3+ and Cu 2+ . In a world where both Fe and O2 are so abundant, Fe-catalysed
free radical reactions of a purely chemical nature are inevitable and widespread. In
biology large numbers of oxidation reactions are coupled to transition metals, such
as the Fe of cytochromes or Cu of phenol oxidases, and involve the controlled
transfer of single electrons to O2, so overcoming the spin restriction. The major
source of HO' in animal systems, is thought to be through the reduction of H2O2
by Fe2 + and this is assumed to be so in plants, particularly from the Mehler reaction
during photosynthesis:
H2O2 + Fe 2 + ->HO'+HO~+Fe 3 +
(1)
The immediate source of Fe 2+ in plants is more problematic. While iron is taken
up from the soil in the Fe 2+ form, it is probably transported and stored in the Fe3 +
state. The immediate source of Fe 2+ for the above reaction (Equation 1) is likely
to be through the reduction of Fe3 + by superoxide also formed during photosynthesis
(and in other reactions):
Fe 3 + -O 2 ~->Fe 2 + +O 2
(2)
Transition metals are then closely associated with free radical reactions and
oxygen reactivity in biology.
Research into the three states, oxygen excess, oxygen sufficiency and oxygen
deficiency has generated a plethora of terms which imply, or have come to imply,
the toxicity of oxygen. At its simplest, oxygen toxicity is no more than the inexorable
operation of the second law of thermodynamics, where life, that is order, is maintained by the expenditure of energy or, more exactly, reducing power. The opposite
state death, or disorder, is for much of biology no more or less than oxidation. The
living condition of almost all biological organisms (with the possible exception of
encysted bacteria) involves a continuous consumption of reductants, much of it used
to maintain, replace and repair damage at the cellular and molecular level.
Accumulated damage ultimately shows up as natural ageing (or senescence) or, on
a shorter time scale, as injury from the hostile external environment or from pathogen
challenge.
The plant literature on hyperoxia (and oxygen sw/nciency) include such terms as
oxidative stress, photo-oxidative stress, free radical damage, oxygen inhibition, reactive oxygen-mediated injury or activated oxygen damage. All of these are used to
indicate that oxygen (in its several forms) has, as a result of a particular external
environmental condition, reacted adversely with one or more structures, endogenous
metabolites or processes. The reaction may involve the incorporation of a molecule
of oxygen into a lipid or nucleic acid or a protein, strictly an oxygenation or
peroxygenation. The reaction may incorporate an oxygen atom, protonated oxygen
anion or an electron into a molecular structure thereby altering its function. The
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Oxygen and environmental stress in plants
5
literature on oxygen deficiency is often more restricted in its usage and discusses
oxygen toxicity in terms of re-aeration injury or post-anoxic or re-exposure damage.
However, all of these and similar terms indicate the toxicity of oxygen. Because life
is a reductive process, the opposite - oxidation - is equated with damage and death.
This appears to be the origin of the term oxidative stress.
Oxygen and environmental stress
Plants show the widest range of responses to oxidative stress. In this volume examples
can be seen in the responses of different species to ozone (O3) (Cape et al.), or
different defences against O3 at the molecular level (Eckey-Kaltenbach et al.;
Schraudner et al.), or the same species under different concentrations of dioxygen
(O2) (Wroblewska & Poskuta) and in response to photo-induced high energy singlet
oxygen (1AgO2) (Krasnovsky) or to ionising radiation (Triantaphylides et al). As
has been observed by Elstner & Osswald (this volume) the very different events
which determine the way O2 is processed within the plant vary with both species
and organ. It is hardly surprising that responses to otherwise unrelated environmental
stresses such as chilling, UV-B exposure, drought, post-anoxic injury, salt stress as
well as changes associated with natural (full-term) senescence or disease should be
all too clearly visible at the molecular level as perturbations in O2 processing.
Examples of these varied responses at the level of O2 processing can be seen in the
contributions to this volume by Burdon et al., Creissen et al., Leprince et al.,
Merzlyak & Hendry 1994, Navari-Izzo et al., Pfister-Sieber & Branele, Schraudner
et al., and Wollenweber-Ratzer & Crawford.
Can an evolutionary approach produce some order into the apparent mixture of
unrelated stress-induced perturbations at the molecular level? Much of our contemporary flora can be traced back through the fossil record, at least at the level of
families, to atmospheric environments very different from those of today (Hendry,
this volume). On theoretical grounds alone there is little likelihood that long-evolved
responses to oxidative stress will be the same in all species. A more pertinent question
might be to ask why oxygen? Why are so many otherwise unrelated but hostile
environmental pressures repeatedly seen as having significant effects on O2 processing? The all-embracing and obvious answer is that mortal life is a process which
staves off the inevitable call of oxidation, degeneration, decay and chaos. This
explanation is adequate to explain events post mortem. It may go some way to
explaining some of the events surrounding senescence (Hillman et al., this volume;
Merzlyak & Hendry, this volume). It does not explain oxidation events ante mortem
at the sub-lethal level. Clearly further research is needed into the varied responses,
not just at the level of the numerous O2-dependent reactions, but also the O2sensitive reactions. Direct perturbation of oxygen supply rapidly changes the rate
of these reactions and, on a slower time scale, may result in molecular and structural
sub-lethal damage. If the damage is severe enough, oxygen can be lethal.
Oxidative damage - cause or effect?
The immediate problem with considering oxygen as having both sub-lethal and
lethal effects is to expose the uncertainty of what is cause and what is effect. Some
years ago Halliwell & Gutteridge (1984) warned of the dangers of considering
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G. A. F Hendry and R. M. M. Crawford
6
activated oxygen necessarily as the cause of tissue damage, or death, whereas it
could, without further enquiry, also arise as the result of death or disease.
1.
Disease
->
stress
Activated
forms
of O2
Disease
or
stress
-»
Tissue
damage
or death
or
->
Increased
lipid
->
peroxidation
Tissue
damage
or death
Activated
O2 or
->
other radicals
Increased
lipid
peroxidation
or
2.
->
Although the original article was addressed to a medical readership, plant scientists
are by no means exempt from these warnings. Unfortunately an element of the
literature persists in assuming that oxidative damage is without further question the
mechanism by which much environmental stress has its initiating effect. Consequently
more and more current research is concerned to demonstrate (for example) the
sequence in time of phenomena such as drought-induced wilting, K-efflux, root
browning and leaf necrosis with oxidative damage (such as lipid peroxidation) or
impaired electron transport, or generation of free radicals, or consumption of glutathione or increased activity of ascorbate peroxidase. The fact remains that radicalmediated damage ramifies into so many different events and processes that it will
always be difficult to distinguish cause from effect. Three examples will serve as
illustrations.
First, it has been shown repeatedly that the severity of an external environmental
stress, e.g. drought, can be correlated quantitatively with the formation of lipid
hydroperoxides which themselves are well characterised products of free radicalmediated reactions. In turn, the same hydroperoxides (or their precursors) can
consume tocopherols or ascorbate or reduced glutathione or can further interact
with iron or copper ions to form yet other (or more) lipid, or protein or nucleic
acid radicals or may generate yet more reduced forms of oxygen ad infinitum. Which
among these readily measurable molecular markers is closest to the initiating reaction
and how much is a consequence of other forms of damage? Where is cause and effect?
Secondly, there is in addition the uncertainty of routes by which transient species,
such as the hydroxyl radical, might produce their damaging effects. Although many
authorities state that the hydroxyl radical is the destructive form of oxygen in
biology, there is much less authoritative experimental evidence to show how the
radical is formed and how it makes selective contact with say the nucleus or the
'wrong' side of a lipid bilayer. The role of Fe 3 + , a relatively mobile promoter of
free radical reactions, deserves much more investigation, particularly in plants under
stress. Iron uptake by plants increased several fold in a matter of hour or days
under conditions of root anoxia, in recovery from drought and during senescence
(Hendry 1993).
Thirdly, extending Halliwell & Gutteridge's warning, oxidative stresses, or free
radical reactions, differ greatly in quality and quantity in living tissues from those
in dead material. The problem arises, how to define living and dead, in plants or
plant parts? Loss of viability in seeds, for example, follows after several months,
years or decades of accumulated sub-cellular and tissue damage. The damage that
occurs in vivo is, in substantial part, almost certainly due to the ravages of oxygen
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Oxygen and environmental stress in plants
1
(Hendry 1993), particularly in seeds rich in unsaturated fatty acids (M. M. Khan,
N. M. Atherton & G. A. F. Hendry, unpublished data). At some unknown point
in time, the seed dies, or more precisely it has lost its ability to germinate in
germination viability tests. Thereafter, with time the seed structure degenerates and
the remaining seed tissues record more and more the purely chemical processes of
oxidation involved in decay and disintegration of the seed fat reserves and other
lipid structures. When can it be concluded that the damage recorded at one moment
in time is due to the reactivity of oxygen in life or the destructive powers of oxygen
in death? This is a problem which runs deep in studies of oxygen toxicity.
Plant survival under anoxia
Anoxic conditions are inimical to higher plant growth and deprival of oxygen is
eventually fatal to all higher plant organs. Despite this generalisation there are
enormous variations between species, and between organs within species, in the
speed with which the deleterious effects of anoxia are manifested. Although the
eventual outcome of oxygen deprivation, namely death, is predictable for all angiosperms, the manner and speed with which it takes places is so varied that the actual
outcome of a similar stress can act very differently depending on the species or
organ that is being deprived of oxygen. Paradoxically, the alleviation of oxygen
deprivation is also a moment of danger to most plant tissues. Prolonged absence of
oxygen creates in many species an inability to defend their tissues against the
oxidative effects of oxygen when they are once again restored to normal air (Crawford
et al., this volume). However, again there are variations, with some species able to
maintain during a prolonged period of anoxia the defence mechanisms necessary
for the moment when the oxygen supply is restored. As death from oxygen starvation
takes place at different rates, depending on the species and organs involved, it is not
surprising that attempts to find a primary sensitive site for the onset of anoxic (or
post-anoxic) injury has so far proved an elusive goal. As in the case of oxidative
injury discussed above, uncertainties between cause and effect make generalisations
about primary sites of injury almost impossible.
As a consequence of the universal demand by all plant tissues for oxygen for their
normal growth and development, any species that can minimise this dependence,
even temporarily, will gain a substantial competitive advantage over those that
cannot suffer any reduction or interruption of their oxygen supply. To be able to
'do without' an essential resource longer than your competitor places the 'deprivation-tolerant' species in a very strong competitive position. Once the stress has
passed the intolerant individuals will have disappeared and access is then gained to
resources that could not be reached by intolerant competitors (Crawford et al. 1989).
Thus, so-called anoxia-tolerant plants are only plants that can last a little longer
than their competitors without oxygen. The common reed (Phragmites australis) and
the bulrush {Schoenoplectus lacustris) often have sole occupancy of nutrient-rich lake
muds as there are few species that can match their tolerance of anoxia. In spring,
when water tables are high and shoots have not yet emerged into air, tolerance of
anoxia is essential for survival. Other wetland species which do not have this
tolerance of anoxia in their submerged rhizomes, such as the many common sedges
and rushes, are confined to areas of reduced flooding where there is no interruption
of the air supply to the underground organs (Studer-Ehrensberger et al. 1993).
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8
G. A. F Hendry and R. M. M. Crawford
Intolerance of anoxia as caused by flooding injury has made drainage a prerequisite
for the cultivation of most crops, a fact which has been evident since the Neolithic
beginnings of agriculture. The intolerance of winter wheat to spring flooding, was
noted already in the second century BC by the Roman agricultural writer Cato
(White 1970). Flooding still remains an economic threat to agriculture and continues
to be actively researched (Crawford 1992; Kennedy et al. 1992, Kozlowski 1984).
Any review of the effects of flooding on agricultural crops provides endless examples
of the many ways in which plants can be killed as a consequence of root-oxygen
deprivation. As with most scientific enquiries, research into the responses of plants
to flooding is often motivated by the desire to elucidate a primary cause for the
injury (Jackson et al. 1990; Kozlowski 1984). However, many of the injuries that
plants receive as a result of flooding and root hypoxia are of a secondary nature
and follow as a consequence of some undefined primary injury to oxygen-starved
cells. Disruption of carbohydrate supplies, water relations and hormonal balance
are just some of the facets of plant physiology that are disturbed by flooding,
particularly in crop species which as a whole are limited in their tolerance of anoxia.
These deleterious effects are so many and varied however, that cataloguing their
various aetiologies does little to improve our understanding of the fundamental
nature of the injury suffered by plants sensitive to water-logging.
Crop plants are likely to remain the ultimate research for studying oxygen deprivation, due to the need to understand more about the mechanisms of flooding
tolerance. However, modern improved crop varieties do not provide the most suitable
material for studying tolerance mechanisms as species in cultivation have been
selected over millennia for properties such as rapid germination and growth, both
characteristics which are incompatible with flooding-tolerance. Therefore, if new
insight is to be gained into the mechanisms of anoxia tolerance, a greater knowledge
is needed of the adaptations to be found in the native species of wetland areas. The
remarkable examples of normally aerobic species which possess organs that are
highly tolerant of anoxia can be found in the perennating organs such as rhizomes
and stolons and dwarf over-wintering shoots (turions) of aquatic plants. These
organs are frequently able to survive months without oxygen and even have the
capacity to extend pre-formed shoots during lengthy periods of anoxia (Crawford
1992).
A more positive approach, in which emphasis is placed on examining how plant
organs can either avoid suffering from oxygen deficits (Armstrong & Armstrong,
this volume) or else tolerate prolonged periods of oxygen deprivation and still be
able to return to air without suffering post-anoxic injury is discussed in several
contributions in this volume (Pfeister-Sieber & Brandle; Crawford et al;
Wollenweber-Ratzer & Crawford). The study of tolerant species in this way brings
to light adaptations which may have existed in the wild ancestors of many of our
cultivated plants but have been lost in the quest for higher yields and greater
productive efficiency. As will be seen in some of the following chapters there are
cogent reasons for broadening the scope of the examination of oxygen stress in
plants, to include those species that are not placed beyond their limits of survival
by oxygen deprivation. An awareness of the many evolutionary responses shown by
plants to variation in their oxygen supply will inevitably give a better understanding
of the nature of anaerobic injury which may in turn help to solve the age-old
problem of agricultural over-dependence on drainage.
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Oxygen and environmental stress in plants
9
Conclusions
Because there are so many untested, maybe even untestable, assumptions associated
with the presence or absence of oxygen and its activated forms, there is a danger
that such uncertainties will promote scepticism and sterile argument. These difficulties
should not obscure the fact that on this planet, oxygen has for nearly 4 G years
played a paramount role in determining the beginning, the middle and the end of
the lives of most biological organisms, in almost all Earthly environments. In many
aspects the dangers of oxygen are so all-pervasive that anyone unfamiliar with the
inner workings of life on earth might question the sustainability of life in an
atmosphere with 21% oxygen. The observer on the Galileo spacecraft might have
recorded, with complete justification, that life on this planet could not be sustained
without considerable protection from its hostile atmosphere. However, as with other
hostile elements of the Earth's environment, such as high or low temperatures and
uncertain water supplies, the evolutionary power of living organisms apparently
thrives on the challenge of physical adversities and uncertainties. Due to the unending
resourcefulness of evolution the dangers of oxygen either by its presence or temporary
absence have only added to the biodiversity of this planet.
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