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Long-Term Anoxia Tolerance in Leaves of Acorus Calamus L. and Iris Pseudacorus L

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Long-Term Anoxia Tolerance in Leaves of Acorus Calamus L. and Iris Pseudacorus L Journal of Experimental Botany, Vol. 52, No. 364, pp. 2213–2225, November 2001 Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. Urte Schlu¨ ter1 and Robert M.M. Crawford Sir Harold Mitchell Building, University of St Andrews, St Andrews KY16 9AJ, Fife, UK Received 16 February 2001; Accepted 3 July 2001 Abstract Key words: Acorus calamus, Iris pseudacorus, anoxia, carbohydrate, metabolic down-regulation, photosynthesis, Mature green leaves of Acorus calamus and Iris chlorophyll fluorescence. pseudacorus have been shown to survive at least 28 d of total anoxia in the dark during the growing season, increasing up to 75 d and 60 d in over- wintering leaves in A. calamus and I. pseudacorus, Introduction respectively. During the period of anaerobic incuba- tion the glycolytic rate is reduced, carbohydrate Oxygen deprivation resulting in either temporary or reserves are conserved and ethanol levels in the prolonged hypoxia or even anoxia is a common environ- tissues reached an equilibrium. Prolonged anoxia mental stress experienced by plants in poorly drained significantly suppressed leaf capacity for respira- soils, during long-term flooding, total submergence or tion and photosynthesis. After 28 d of anoxia, ice-encasement. The metabolic events which accompany respiratory capacity was reduced in A. calamus and the shift from aerobic to anaerobic processes have been I. pseudacorus by 80% and 90%, respectively. intensively studied in root tissues and germinating The photosynthetic capacity of leaves decreased by seedlings of crop plants. However, the length of experi- 83% in A. calamus and by 97% in I. pseudacorus mental stress application in these species is always limited after 28 d of anoxia. This reduction in photo- due to their short survival time under anoxia. The synthetic capacity was accompanied by a modifica- majority of crop plants are annual dryland species and tion of the chlorophyll fluorescence pattern indicating prolonged waterlogging during the growing season damage to the PSII reaction centre and subsequent usually leads rapidly to flooding injury and yield loss. electron transport. Chlorophyll content was only Despite the complex problems for plant life under anoxia, slightly reduced after 28 d under anoxia and dark- a number of plant species are well adapted to prolonged ness in A. calamus, whereas there was a 50% reduc- oxygen deprivation. Mostly these long-term anoxia- tion in I. pseudacorus. On return to air A. calamus tolerant species inhabit bogs, wet marshlands, pools, leaves that endured 28 d of anoxia recovered full river banks, and salt marshes or else are accustomed to photosynthetic activity within 7 d while those of survive long periods under a closed ice-layer (Crawford I. pseudacorus had a lag phase of 3–10 d. This well- and Braendle, 1996). As yet there is little information developed ability to endure prolonged periods of concerning the metabolic mechanisms involved in long- oxygen deprivation in both these species is asso- term anoxia tolerance. ciated with a down-regulation in metabolic activity For a species to be considered anoxia-tolerant it is not in response to the imposition of anaerobiosis. It necessary that every organ or tissue has to survive oxygen is suggested that when leaf damage eventually deprivation. Ecologically, all that is required is the does take place in these species after protracted survival of those organs that are essential for subsequent oxygen deprivation, it is anoxic rather than post- regeneration of the whole plant on return to air. Roots anoxic stress that is responsible. are relatively sensitive to oxygen deprivation, and the 1 Present address and to whom correspondence should be sent: Max-Planck-Institute of Molecular Plant Physiology, Am Mu¨ hlenberg 1, D-14476 Potsdam, Germany. Fax: q49 331 5678 250. E-mail: [email protected] ß Society for Experimental Biology 2001 2214 Schlu¨ ter and Crawford survival capacity of most tolerant species resides in the is high, rhizomes and shoots often overwinter totally shoots or rhizomes. The longest survival times for plant submerged and are thus liable to experience prolonged tissues under anoxia have been found in the overwintering periods of oxygen deprivation. The second species investig- rhizomes of some wetland species (Monk et al., 1984). ated, the Yellow Flag or Yellow Iris (I. pseudacorus), In a quasi-dormant state rhizomes can withstand oxygen is native to Europe and is comparable to A. calamus with deprivation for up to 3 months. During flooding, green respect to its morphology and life style. Leaves are shoots are often only partly submerged and maintain a usually present throughout the year with peak growth connection to atmospheric oxygen. In many wetland occurring from April to June. While the carbohydrate species flooding-enhanced aerenchyma develops in roots content of A. calamus consists mainly of starch, allowing the diffusion of oxygen to the flooded plant I. pseudacorus stores carbohydrate reserves in the form organs. Consequently, green plant tissues have been of fructans (Augem, 1928). largely ignored in oxygen-deprivation studies. However, In this paper, some central features of anaerobic in temperate climates prolonged waterlogging often takes metabolism including ethanol fermentation are reported place in winter or spring, when shoots are still small from leaves that were kept under prolonged anoxia. After and liable to submergence. Total submergence or ice- the switch from aerobic to anaerobic metabolism, the main encasement can also impose oxygen deprivation on green problems of long-term anoxia lie in the maintenance of shoots and, in the absence of photosynthesis or contact those cell functions that are necessary to guarantee with the atmosphere, survival depends on physiological metabolic recovery. On return to an oxygen-rich environ- adaptation to anoxia or at least hypoxia. ment, the plants have to contend with problems of post- The anoxia tolerance of leaves has recently claimed anoxic injury caused by the generation of reactive oxygen attention when it was shown that intact plants of some species or the oxidation of anaerobically accumulated arctic species survived lengthy periods of total anoxia substances (Biemelt et al., 1998). An intact anti-oxidative without suffering any visible damage to the leaf tissues defence system is therefore assumed to be advantageous (Crawford et al., 1994). The possibility that leaves can for the prevention of further damage to membrane lipids adapt metabolically to anoxia is especially interesting as and other cellular macromolecules under post-anoxia. in comparison to rhizomes, leaves possess higher meta- The functionality of the respiratory pathway and the bolic activities in addition to photosynthetic carbon photosynthetic apparatus was therefore studied in the fixation. The metabolic consequences of anaerobic leaves on return to aerobic conditions. deprivation for leaves are therefore likely to be more severe than in dormant rhizomes. Two different growth responses of shoots to anoxia have been observed. First, Materials and methods it has been shown that there are some species which are able to sustain upward shoot elongation under anoxia Plant material and anoxic incubation and secondly, there are species where the shoot can Acorus calamus plants originated from the Moossee (Bern), survive anoxia but does not grow in the absence of and were cultivated in a pond at the University of St Andrews. oxygen (Barclay and Crawford, 1982). The advantage Iris pseudacorus was collected from semi-natural sites, such as of the first group lies in the increased possibility for overgrown curling ponds, in North East Fife, Scotland. The rhizomes of these plants were cleaned from soil, cut into pieces the plant to regain contact with air. If the elongated of about 5–7 cm and potted separately in sand. The shoots of shoot, however, cannot establish a connection with the all plants were cut back to about 20–25 cm above the soil. atmosphere quickly, the plants soon die of exhaustion. To allow the plants to establish in the pots, they were kept in In the second group, green shoots seem to outlast anoxia the greenhouse for at least 2 weeks until new leaves developed. by reducing metabolic activity to a minimum until The greenhouse-conditioned plants were used as controls representing day zero of the anoxia and dark treatment. environmental changes allow re-aeration. For the anoxia experiments, plants were transferred directly The two species under investigation, Acorus calamus L. from the greenhouse into an anaerobic chamber (Forma and Iris pseudacorus L., naturally inhabit sites with high Scientific Anaerobic systems, model 1024, Marietta, Ohio, water content and high risk of oxygen deprivation stress. USA). The atmosphere in the chamber consisted of 90% The high anoxia tolerance of the Sweet Flag (A. calamus) nitrogen and 10% hydrogen with a palladium catalyst to remove any traces of oxygen. The anaerobic atmosphere was shoots has already been proven (Bucher and Kuhlemeier, checked with methylene blue indicator strips (Dry Anaerobic 1993). This monocotyledonous amphibious species is Indicator strips, Becton Dickinson Microbiology systems, native to south and eastern Asia and was introduced as Cockeysville, USA). To avoid the production of oxygen via a triploid into Europe in 1557 where it has never been photosynthesis, plants were kept in the dark. Humidity in the observed to set fruit and is entirely dependent on chamber was nearly 100% and plants were supplied with nitrogen-bubbled water if necessary. The temperature was kept vegetative propagation. The rhizomes are positioned at at 20–25 8C. After the anoxia treatment, plants were returned the water–soil interphase and as a consequence are to the greenhouse. Plant survival was checked by observing submerged for most of their lifetime. If the water table leaf development after the return to aerobic conditions in the Leaf long-term anoxia tolerance 2215 greenhouse. For comparison, experiments were repeated with than 1 mm thickness and transferred into Warburg flasks plants which were kept in the dark but under aerobic conditions.
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