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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). Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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). Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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 Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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 Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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 Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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 Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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). Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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. Downloaded from https:/www.cambridge.org/core. IP address: 88.99.165.207, on 17 Jun 2017 at 12:32:51, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0269727000013932 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. References Armstrong, J., & Armstrong, W. 1994. A physical model involving nuclepore membranes to investigate the mechanism of humidity-induced convection in Phragmites australis. Proceedings of the Royal Society of Edinburgh 102B, 529-39. Barclay, A. M , & Crawford, R. M. M. 1982. Plant growth and survival under strict anaerobiosis. Journal of Experimental Botany 33, 541-9. 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