adaptation strategies in wetland plants: links between ecology and physiology. proceedings of a...

Some Aspects of the Extreme Anoxia Tolerance of the Sweet Flag, Acorus calamus L.Author(s): Michel Weber and Roland BrändleSource: Folia Geobotanica & Phytotaxonomica, Vol. 31, No. 1, Adaptation Strategies in WetlandPlants: Links between Ecology and Physiology. Proceedings of a Workshop (1996), pp. 37-46Published by: SpringerStable URL: http://www.jstor.org/stable/4181414 .

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Folia Geobot. Phytotax. 31: 37-46, 1996

SOME ASPECTS OF THE EXTREME ANOXIA TOLERANCE OF THE SWEET FLAG, ACORUS CALAMUS L.

Michel Weber & Roland Brandle

Institute of Plant Physiology, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland; tel. +41 31 631 49 56; fax +41 31 332 20 59, E-mail RBRAENDLE@ PFP UNIBE.CH

Keywords: Ammonia, Energy metabolism, Fermentation, Macromolecule synthesis, Membrane stability, Oxygen deprivation, Sulphide

Abstract: Acorus calamus L. is a neophyte in Europe with remarkable properties. Among other things, it is the most anoxia tolerant species and a competitive invader at eutrophic sites. The following overview presents the most recent work on these subjects. Carbohydrates of the rhizomes sustain anaerobic ATP production for very long periods. Ethanolic fermentation naturally occurs in winter and produces rather low, but sufficient amounts of ATP for survival, as shown by adenylate energy charge and total adenylate content. Fermentation energy is mainly used for the synthesis and preservation of essential macromolecules, such as proteins and membrane lipids. The extent of these processes is unique. Moreover, ammonia and sulphide uptake is maintained during the cold season. Both ions are detoxified to alanine and thiols which are translocated into the rhizome, where the nitrogen of alanine is used to form arginine. Overwintering leaves contain asparagine instead of arginine. Recycled nitrogen compounds from the rapidly degrading summer leaves return into the rhizomes. Therefore, the nitrogen nutrition consists of an external and internal cycle. The abundance of carbohydrates and nitrogen compounds allows spring shoot growth earlier than other species. These strategies could contribute markedly to the competitive power of A. calamus at its natural site.

INTRODUCTION

The sweet flag (A. calamus L.) is a neophyte in Europe. It derived probably from the Himalaya region, and it is very likely that in Europe (except Northern Europe) all plants have a single ancestor rhizome. This belonged in 1574 to the famous Clusius in Vienna. From here it spread out into Central Europe, Belgium, France, Germany and later on England (SCHROTER 1908). Originally it was introduced for medicinal purposes because of its content of drugs, such as a- and 1-asarone, pinen, camphen, eucalyptol, eugenol, and sesquiterpenes. The ethereal oils are located in spherical oil cells (Fig. 1, AMELUNXEN & GRONAU 1969). The plant has been used to cure opthalmic and stomach complaints, hysteria, epilepsy, chronic rheumatism and as scent in the perfumery industry as well as for liqueurs and beers. Nowadays its importance has decreased, although it is also known to improve intelligence! However, an overdose can lead to irrepressible vomiting, hallucinations, and may even be carcinogenic.

The European race is triploid and sterile (2n=3x=36, WULFF 1941). Outside Europe there are races with 2n=24 and 2n=48 chromosomes. Rhizomes provide vegetative propagation. Nevertheless, once introduced, A. calamus is highly productive and able to displace many other amphibious species at eutrophic sites (DYKYJOVA 1980, KvfT J., pers. comm.).

The plant has dorsiventral rhizomes with many thickened adventitious roots that grow out of the ventral part. The rhizome itself lies on the sediment surface, and only the voluminous



38 M. Weber & R. Brandle

Fig. I Aerenchyma of the A. calamus rhizome. Note the abundance of starch grains in the cells. The big, spherical cell without starch is an oil cell. Bar = 10 gm.

roots penetrate deeper into the mud. The rhizome bears many buds to fonn leaves and young rhizomes. The amphibious leaves decay very quickly at the end of the growing season. They are replaced by short, green overwintering leaves, which remain submerged from November to April.

The whole plant body is very porous. This property allows an efficient internal ventilation from aerated parts of the leaves down to the roots. There is sufficient oxygen available to meet more than 90% of the maximum respiration capacity (BRANDLE 1991). Furthermore, the cortex and stele of the rhizome contain throughout the year considerable amounts of carbohydrates, mainly starch (Fig. 1).

Although the rhizomes are not really buried in the mud, and therefore the plants do not experience strict anoxia, A. calamus is the most flood and anoxia tolerant marsh plant known so far except some Arctic species (CRAWFORD, pers. comm.). It can survive several months without any oxygen (WEBER & BRANDLE 1994). In addition, it is perfectly adapted to re-aeration following periods of oxygen shortage.

Hence, the species is an excellent example with which to demonstrate the efficient strategies that have evolved to cope with oxygen deprivation and re-aeration stress. Among the most important strategies may be:

(1) The adaptation and regulation of energy metabolism. (2) The efficient use and detoxification of a surplus of reduced nitrogen and sulphur. (3) Synthesis and persistance of essential macromolecules and their protection against

postanoxic-induced oxidative stress. In the following, the significance and the underlying components of the points mentioned

above will be presented.



Anoxia tolerance of Acorus calamus 39

Table 1. Adenylate energy charge (A.E.C.) and tissue concentrations of adenosine nucleotides of summer and winter rhizomes (A. calamus) under anoxia. From SIEBER & BRANDLE (1991)1) and JOLY & BRANDLE (1995)2). Mean of 5 independent experiments ? standard deviation.

Summer rhizomel) Winter rhizome2) Anoxic treatment (hours) A.E.C. ATP+ADP+AMP A.E.C. ATP+ADP+AMP

(nmol/mg protein) (nmol/mg protein)

Oh 0.96?0.02 81 ?32 0.85 ?0.07 45 ?4 24 h 0.87 ? 0.08 0.56 ? 0.02 25 ? 1 48 h 0.88 ?0.09 82 ? 23 0.51 ?0.02 29 ? 1

The adaptation and regulation of energy metabolism

Survival of hypoxia and anoxia requires abundant energy reserves and sufficient ATP production for cell maintenance at least. The energy metabolism of A. calamus obviously fulfills these conditions (SIEBER & BRANDLE 1991). Mainly ethanolic fermentation generates adequate amounts of ATP in order to keep adenylate energy charge values and total adenylate contents high enough for prolonged survival. However, there are some distinct differences between the seasons. Whereas energy charge values and adenylate pools remain high and constant in anoxic summer rhizomes, both decrease in anoxic winter rhizomes to lower, but also constant levels, indicating a kind of "anaerobic retreat" (Tab. 1). The trigger for this behaviour is not yet known. Calculations show that the carbohydrate reserves last for about half a year under low temperatures and low oxygen (Tab. 2). It is also noteworthy that the calculated carbohydrate demand differs only about 30% between fermentation and respiration. Fermentative glucose consumption is less than 42 mg per month at 5 ?C, and about 30 mg glucose per month at 5 ?C under normoxic conditions. This behaviour signifies more or less a lack of a "Pasteur effect". These values confirm also the onset of the anaerobic retreat in cold winter rhizomes by the reduction of ATP formed. The whole ATP dependent metabolism is slowed down, and probably growth by cell proliferation is completely stopped (PRADET & RAYMOND 1983). Furthermore, carbohydrate consumption at the natural site might be even less because the seasonal difference between maximum and minimum content is only 70 mg/g fw (HALDEMANN & BRANDLE 1986).

The sensors which induce growth in spring are not known, but probably the trigger is oxygen itself and not directly light or temperature. Northern blot analysis of mRNAs for glycolytic and fermentative gene expression indicate high transcript levels under submergence and very little when the leaves reach the water surface (BUCHER & KUHLEMEIER 1993, BUCHER et al. 1996). It could be that the small oxygen production of the submersed leaves during the increasing day length is high enough to start re-growth and to stop fermentation later on.

However, Fig. 2 clearly demonstrates that fermentation processes occur in rhizomes at the natural site during the cold season and it is obvious that winter rhizomes are metabolically active. ADH activity levels increase to high values and some ethanol can be detected within the rhizomes. Moreover, the ethanol contents cannot be taken to estimate production because of the release by diffusion. Nevertheless, they are markers to demonstrate metabolic activity in winter when the water temperatures are rather low around the rhizome, e.g. 2-6 ?C (WEBER



40 M. Weber & R. Brandle-

Table 2. Calculated glucose consumption of maximum fermentation and maximum respiration capacity at 20-25 ?C, and estimated need at 5 ?C (see STUDER & BRANDLE 1984). Under field conditions the seasonal difference between maximum summer and minimum winter carbohydrate content was only 70 mg/g fw (HALDEMANN & BRANDLE 1986). Results of 4 different authors ? standard deviation.

Temperature 20-25 ?C 5 ?C

Ethanol-production Glucose-consumption Glucose consumption (rmol/g fw d) (mg/g fw d) (mg/g fw month)

Fermentation 62 ? 7 5.6 ? 0.6 < 42

Respiration (jimol 02/g fw d)

Respiration 129 ? 25 3.9 ? 0.8 < 30

& BRANDLE 1994). The actual rhizome temperature might be somewhat higher because of the tight contact of roots and rhizomes with the warmer sediment.

The efficient use and detoxification of a surplus of reduced sulphur and nitrogen

Besides energy demand for maintenance, it is very likely that some energy is also used to detoxify the surplus of ammonia and sulphide by the synthesis of amino acids.

Sulphur and nitrogen occur in eutrophic sediments predominantly in their reduced forms as sulphide and ammonia which are known to be toxic for plants (MEHRER & MOHR 1989, PEZESHKI et al. 1988).

Increased sulphide, but not sulphate, concentrations in the surroundings of the roots and the rhizome lead to the formation of thiols, mainly glutathione (Fig. 3). Most of the thiols are stored in the rhizome, much less in the roots, and none in the leaves. The rhizome acts as a buffer between the toxic sulphide in the soil and the sensitive leaves. Hence, it is at the same time the organ of detoxification and storage. Sulphide is probably bound to o-acetylserine to form cysteine that is used to synthesise the tripeptide glutathione (GSH). Besides its role as a storage and transport compound of reduced sulphur, GSH plays an additional role in many detoxification processes, such as the detoxification of active oxygen species formed at the onset of re-aeration of anoxic tissues.

The detoxification of ammonia is very similar to sulphide removal. It is known that, for example, the internal concentration of free ammonia never reaches toxic levels in roots, rhizomes and leaves of A. calamus (WEBER & BRANDLE 1994). External ammonia is fixed into alanine in roots and in rhizomes, at the natural site as well as under laboratory conditions (Fig. 4). Usually, the value under natural conditions at the water/sediment interface is 0.21 mM. More precisely, ammonia is fixed by the GS-GOGAT cycle to form in a first step glutamate (VANLERBERGHE et al. 1991, MENEGUS et al. 1993). This occurs also under anaerobiosis. In a second step, the amino group is transferred to glycolytic pyruvate by the enzyme alanine aminotransferase (GOOD & MUENCH 1992). But alanine seems to be only an interim storage compound.

Long term storage in A. calamus is different since in winter huge amounts of arginine are present in rhizomes that allow a more efficient nitrogen storage than alanine (Fig. 5). During




* ADH * ethanol 3000 vLDH lactate 30

1 ~~~~~~~~~~~~~~25 o

2 2000 20 -0

C ~~~~~~~~~~~~~~1 5 E

aug oct dec feb apr jun aug oct dec feb apr jun

Fig. 2. Season dependent activity changes of alcohol dehydrogenase (ADH) and lactate dehydrogenase (LDH), aind concentrations of the corresponding products in the rhizome of A. calamus. From HALDEMANN & BRANDLE ( 1986).

4000 1

2001~~~~~~~~~~~~~~

E T I I I

24 h 48 h 72 h 24 h 48 h 72 h 24 h 48 h 72 h

root dic leaf

Fig.2. easo deendet ativiy cange ofalcholueyrsogenashie feedHing lcat eyrgeae(D)

and 3 coctaion soful theiorrsp(S)ondin prouctathionte (S)cnetiros,rhizomeadlae of A. calamus.FoHADMN BRDE

4 001

200

CD

24 h 48 h72 h 24 h 48 h 72 h 24 h 48 h 72 h

Fig.3. Aid slubl thils (H) adrgltatin GH otn nros rhizome landlaeffA aau

treated with@* = 0 mM, * = 1 mM and A = 4 mM sulphide in the nutrient solution. [02] < 0.4%. Mean of 5 independent experiments ? standard deviation.

spring shoot growth, arginine can be transformed into glutamate, a transformation that may already happen under anaerobic conditions. The anaerobic arginine degradation has been

140

shown using 4C-arginine. It was transformed mainly to glutamate (WEBER unpubl.). Bleeding sap analysis revealed that the main transported amino acids during spring growth are glutamine and asparagine (WEBER & BRANDLE 1994).




2 I\ , \I 2

J M M J S N J M M J S N 0 8 16 24

month hours

Fig. 4. Seasonal variation of alanine concentrations in the root tissue (left) and effect of ammonia nutrition (3.3 mM) on alanine production under anoxia in tissue discs (right) of A. calamus rhizomes. * = anoxia, 0 = aerobic control. Mean of 5 independent experiments + standard deviation. Each point represents three plants. The data were prepared with the help of a polynomial regression curve of 10th order (DRAPER & SMITH 1981). The confidence limits, shown by dashed lines, are 98% (SAKAI & THOMPSON 1974).

40 o0 H3N-C-H

I ~~~~~~H 2 NH

3 0 lo,,N NH2

J M M J1 S N J MA M J S N

Fig. 5. Seasonal variation of the arginine concentrations in the rhizome of A. calamus. The molecule has 4 N atoms. From WEBER & BRANDLE 1994. The same statistical methods as in Fig. 4 were used.

Arginine is the most common amino acid in the rhizome, but not in the roots and leaves. Additionally, asparagine occurs in considerable amounts in the rhizome. Obviously, the bulky rhizome is the most important storage organ for carbohydrates and nitrogen compounds with respect to the whole plant. The short overwintering leaves contain asparagine that serves only for their own growth at the beginning of spring. The roots are not a storage organ but, as mentioned before, they are able to fix ammonia in winter in order to detoxify ammonia and to replenish the nitrogen reserves at the same time.

Besides ammonia uptake, there is a season-dependent, internal cycling of nitrogen from the storage organ into growing parts in spring and back in autumn. Thus, the internal cycling, in addition to the uptake, allows A. calamus an impressive use of nitrogen. The same strategy is also known from competitive land plants (BOERNER

1984). Hence, the total nitrogen pool increases constantly, and, consequently, biomass production is intensified in nutrient rich, sapropelic sediments, e.g. of fishponds (DYKYJOVA 1980). For example, at higher degrees of eutrophication in Phragmites stands, internal cycling of nutrients is replaced by external cycling, e.g. nitrogen loss during leaf decomposition (KOHL & KOHL

1993). Although this species exhibits a luxurious, above-ground growth for a few seasons, the external cycling represents a continuous loss of energy e.g. for below-ground biomass and growth. The carbohydrate reserves of rhizomes decline gradually and could become too low to survive further oxygen deprivation at a given time. Therefore, A. calamus with its




Table 3. Content of polar lipids and free fatty acids under air and under anoxia in rhizomes of A. calamus (wetland species) following 70 d of anoxia treatment and Iris germanica (dryland species) following 14 d of anoxia. From HENZI & BRANDLE (1993).

Polar lipids (jg g-I fw) Fatty acids (,ug g- fw)

Control Anoxia Control Anoxia

A. calamus 695 ?44 651 ? 38 < 10 < 20

I germanica 891 ? 37 425 ? 29 < 10 138 ? 17

huge carbohydrate content and reserves of reduced nitrogen in the rhizomes and the preformed shoots occupies and invades sites earlier in the year than other species, and thus may be able to outcompete most of them.

Synthesis and persistance of essential macromolecules and their protection against postanoxia-induced oxidative stress

One of the most striking differences between A. calamus and less tolerant plants is both the anaerobic synthesis and the persistance of macromolecules. Both strategies are important in this species. For example, as shown in Fig. 6, labelled amino acids are still used to synthesise proteins under anoxia following one day of anoxic pretreatment. Although total protein synthesis is hindered by 46% under anoxia, many of the "normoxic" proteins are synthesised, in addition to a set of "anaerobic proteins" that are able to intensify glycolysis and related processes (for reference see: ARMSTRONG et al. 1994).

On the other hand, polar lipids remain astonishingly stable, since 70 days of anoxia induces hardly any degradation; almost no free fatty acids occur. The dryland species Iris germanica L., for example, is less resistant. Already after 14 days, considerable amounts of free fatty

I Iarxoda air control

ID 8 0 ir Cu

60 -

4 0

.- 20

a p r a p r

fraction

Fig. 6. Incorporation and allocation of a 14C-labeled amino acid mixture into different fractions: a = amino acids, p = proteins, r = residual. Rhizome discs were incubated anaerobically for 24 hours before and for another 24 h during the addition of the 14C-amino acids.

acids are present (Tab. 3). In non-tolerant species, lipids

are degraded within a few hours or days. However, in all species investigated so far, and thus also in adapted wetland species, lipid saturation takes place. Desaturases need molecular oxygen in order to introduce double bonds, and therefore lipid saturation is inevitable. But with regard to membrane injury, it is a question of the time span needed for these processes. A. calamus proved to be very insensitive to saturation processes compared to other species. Hence, we concluded that lipid turnover is rather slow




I. germanica 1. gemianica

o T

50 500

O ~~~~~~~~~~~~~~~~~~~~E 25 A.calamus A.calamus CD

20

35 d70 d 7 d 14 d 35 d70 d 7 d 14 d

Fig. 7. Accumulation of peroxidation products (MDA - malondialdehyde) and ethane in rhizomes of A. calamus (wetland species) and Iris germanica (dryland species) during the first 6 hours of postanoxia. Note the different time scale between the species. From HENZI & BRANDLE (1993).

in this species. Membrane lipids are preserved and compartmentation remains intact under anoxia for a long time (HENZI & BRANDLE 1993).

However, anoxia survival is only part of the resistance. Many tissues are damaged only upon re-aeration. The underlying components are peroxidation processes, and eventually the action of acetaldehyde formed by the degradation of anoxically accumulated ethanol (CRAWFORD 1992). In the first case, reactive oxygen species (superoxide anions, hydrogen peroxide and hydroxyl radicals) are able to destroy all of the macromolecules, provided that the enzymatic (superoxide dismutases, catalases and peroxidases) or non-enzymatic (glutathione, ascorbate a-tocopherol and others) defence systems are not appropriately working (ELSTNER 1990). This happens in plant tissues as well as in animal and human tissues after periods of oxygen deprivation, e.g. reperfusion injuries. The most sensitive molecules are the unsaturated fatty acids which are split in chain reactions to form typical peroxidation products, for example ethane, ethylene, malondialdehyde. These products can easily be detected chemically or by GC. It turned out that A. calamus produced only very few postanoxic peroxidation products in comparison to the dryland species L germanica, as shown for malondialdehyde and ethane (Fig. 7, HENZI & BRANDLE 1993, PFISTER-SIEBER & BRANDLE 1994). To date, there is little evidence about the toxicity of acetaldehyde (PERATA & ALPI 1993). However, considerable amounts are formed in sensitive tissues, and acetaldehyde is also known to attack essential macromolecules, mainly proteins (PFISTER-SIEBER & BRANDLE 1994, SCHAUENSTEIN et al. 1977).

CONCLUSIONS

(1) A. calamus is the most outstanding plant with regard to its properties to withstand long-term flooding compared to plants with similar ecological behaviour (e.g. Sparganium spp., Carex spp., Glyceria maxima). An exception are Arctic plants which are able to survive for years (CRAWFORD, pers. comm.). Besides morphological adaptations, a set of physiological




strategies improve flooding and anoxia tolerance. Underlying components are different adaptation strategies of metabolism, e.g. ATP production, anoxic protein synthesis and preservation of lipids and membranes.

(2) Roots, rhizomes and overwintering leaves contribute in common to the pronounced tolerance, although the rhizome probably is the most tolerant organ. But it is also very likely that the thickened roots survive oxygen limitation in the natural habitat.

(3) The ATP demand of rhizomes under oxygen limitation can be covered by ethanolic fermentation. Rhizomes contain considerable amounts of carbohydrates. Furthermore, energy metabolism is subject to a control mechanism. ATP formation capacity in winter is lower than in summer, indicating an "anaerobic retreat".

(4) However, the roots are able to take up ammonia and sulphide from the anaerobic sediment during the whole year, and to fix both of them into alanine or thiols. Thus, the ions are detoxified and the nutrients are available when needed. Both compounds are quickly displaced into the rhizomes which appear to be the main store of assimilated and recycled nitrogen (arginine) and sulphur (glutathione).

(5) Overwintering leaves are rich in asparagine that is used up during the initial steps of growth. They do not grow in winter. Growth starts in early spring. It might be that the winter leaves act as sensors or produce the signal to initiate growth. It might be that a given oxygen concentration acts as a threshold.

(6) A. calamus is not able to survive indefinitely without any oxygen. Its rhizomes also die after about 3 months. Nevertheless, A. calamus is a strong competitor at eutrophic sites because of its favourable growth behaviour, e.g. early start in spring, and efficient use of nutrients by external uptake and internal cycling.

Acknowledgements: The authors thank Dr. A. Fleming for improving the style of the manuscript.

REFERENCES

AMELUNXEN F. & GRONAU G. (1969): Elektronenmikroskopische Untersuchungen an den Olzellen von Acorus calamus L. Z. Pflanzenphysiol. 60: 156-168.

ARMSTRONG W., BRANDLE R. & JACKSON M.B. (1994): Mechanisms of flooding resistance in plants. Acta Bot. Neerl. 43: 307-358.

BRANDLE R. (1991): Flooding resistance of rhizomatous amphibious plants. In: JACKSON M.B., DAVIES D.D. & LAMBERS H. (eds.), Plant life under oxygen deprivation, SPB Academic Publishing, The Hague, pp. 35-46.

BOERNER R.E.J. (1984): Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to site fertility. J. Appl. EcoL 21: 1029-1040.

BUCHER M. & KUHLEMEIER C. (1993): Long-term anoxia tolerance. Multi-level regulation of gene expression in the amphibious plant Acorus calamus L. Pl. Physiol. 103: 441-448.

BUCHER M., BRANDLE R. & KUHLEMEIER C. (1996): Glycotic gene expression in amphibious Acorus calamus L. under natural conditions. Pl. & Soil 178: 75-82.

CRAWFORD R.M.M. (1992): Oxygen availability as an ecological limit to plant distribution. Advances Ecol. Res. 23: 93-185.

DYKYJOVA D. (1980): Production ecology of Acorus calamus. Folia Geobot. Phytotax. 15: 29-57. DRAPER N.R.& SMITH H. (1981): Applied regression analysis. John Wiley & Sons, New York. ELSTNER E.F. (1990): Der Sauerstoff Biochemie, Biologie, Medizin. B-I-Wissenschaftsverlag, Mannheim,

Wien, Zurich. GOOD A.G. & MUENCH D.G. (1992): Purification and characterisation of anaerobically induced alanine

aminotransferase from barley roots. Pl. Physiol. 101:1520-1525.




HALDEMANN C. & BRANDLE R. (1986): Seasonal variations of reserves and of fermentation processes in wetland plant rhizomes at the natural site. Flora 178: 307-313.

HENZI T. & BRANDLE R. (1993): Long tenn survival of rhizomatous species under oxygen deprivation. In: JACKSON M.B. & BLACK C.R. (eds.), Interacting stresses on plants in a changing climate, NATO Series vol. 1 (16), Springer Verlag, Berlin, pp. 305-314.

JOLY C.A. & BRANDLE R. (1995): Fermentation and adenylate metabolism of Hedychium coronarium J.G. KOENIG (Zingiberaceae) and Acorus calamus L. (Araceae) under hypoxia and anoxia. Funct. Ecol. 9: 505-5 10.

KOHL H. & KOHL J.-K. (1993): Seasonal nitrogen dynamics in reed beds (Phragmites australis (CAV.) TRIN. ex STEUDEL) in relation to productivity. Hydrobiologia 251: 1-12.

MEHRER I. & MOHR H. (1989): Ammonium toxicity: description of the syndrome in Sinapis alba and the search for its causation. Physiol. Pl. 77: 545-554.

MENEGUS F., CArrARUZZA L., MOLINARI H. & RAGG E. (1993): Rice and wheat seedlings as plant models of high and low tolerance to anoxia. In: Mechanisms of adaptation and control, CRC Press, Boca Raton, pp. 53-64.

MONK L.S., BRANDLE R. & CRAWFORD R.M.M. (1987): Catalase activity and post-anoxic injury in monocotyledonous species. J. Exp. Bot. 38: 233-246.

PERATA P. & ALPI A. (1993): Plant responses to anaerobiosis. Pl. Sci. 93: 1-17. PEZESHKI S.R., PAN S.Z., DELAUNE R.D. & PATRICK W.H. (1988): Sulfide-induced toxicity: Inhibition of

carbon assimilation in Spartina alternifolia. Photosynthetica 22: 437-442. PFISTER-SIEBER M. & BRANDLE R.(1994): Aspects of plant behaviour under anoxia and postanoxia. Proc.

Roy. Soc. Edinburgh, Ser. B, 102: 313-324. PRADET A. & RAYMOND P. (1983): Adenine nucleotide ratios and adenylate energy charge in energy metabolism.

Annual Rev. P1. Physiol. 34: 199-224. SAKAI H. & THOMPSON W. (1974): Comparisons of approximation to the percentile of t, X ,and F distribution.

J. Statist. Comp. Sim. 3: 81-93. SCHAUENSTEIN E., ESTERBAUER H. & ZOLLNER H. (1977): Aldehydes in biological systems. Their natural

occurrence and biological activities. Pion Ltd., London. SCHROTER C. ('1908): Lebensgeschichte der Blutenpflanzen Mitteleuropas. Ulmer, Stuttgart. SIEBER M. & BRANDLE R. (1991): Energy metabolism in rhizomes of Acorus calamus (L.) and in the tubers

of Solanum tuberosum (L.) with regard to their anoxia tolerance. Bot. Acta 104: 279-282. STUDER C. & BRANDLE R. (1984): Oxygen consumption and availability in the rhizomes of Acorus calamus

L., Glyceria maxima (HARTMANN) HOLMBERG, Menyanthes trifoliata L., Phalaris arundinacea L., Phragmites communis TRIN. and Typha latifolia L. Bot. Helv. 94: 23-31.

VANLERBERGHE G.C., KENNETH W.J. & TURPIN D.H. (1991): Anaerobic metabolism in the N-limited alga Selenastrum minutum. Pl. Physiol. 95: 655-658.

WEBER M. & BRANDLE R. (1994): Dynamics of nitrogen-rich compounds in roots, rhizomes, and leaves of the Sweet Flag (Acorus calamus L.) at its natural site. Flora 189: 63-68.

WULFF H.D. (1941): Uber die Ursache der Sterilitat des Kalmus (Acorus calamus L.). Planta 31: 478-491.



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