Juhász, A.

Lichtenthaler, H. K.

Takács, Z.

Tuba, Z.

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Acta Acad. Paed. Agriensis, Sectio Biologiae XXV (2004) 153-126Pentose-phosphate pathway as the possiblebackground of resaturation respiration in thedesiccation-tolerant lichen Cladonia convoluta Tuba, Z.1'2, Takács, Z.1, Juhász, A.2, Lichtenthaler, H. K.3'Plant Ecology Departmental Research Group of the Hungarian Academy of Sciences at the 2Department of Botany and Plant Physiology, Faculty of Agricultural and Environmental Sciences, Szent István University,H-2100, Gödöllő, Páter K. u. 1.3 Botanisches Institut der Universitat Karlsruhe, Lehrstuhl II, D-76128, Karlsruhe, Germany Abstract. Respiration rates in the re-wetted desiccated thalli of a desiccation-tolerant lichen Cladonia convoluta were measured duringrehydration and revival. Treatment with bromoxynil as uncoupler ofoxidative phosphorylation showed that the high intensity of resaturationrespiration rate is not entirely caused by the uncoupled mitochondrialmembrane. Treatments with KCN or absence of 0 2 obtained by applying N2resulted in the same effect indicating the possible role of the pentose-phosphate shunt in the boosted C02 efflux of the rehydrating and revivingdesiccated lichen thalli.Keywords: basic respiration, bromoxynil, Cladonia, uncoupling,desiccation tolerance, mitochondrion, potassium cyanide, rehydration,wetting burstIntroductionDesiccation tolerant plants can survive the loss of 80-95% of their cellwater, so that the plants appear completely dry and no liquid phase remainsin their cells; after a shorter or longer period in the desiccated state, theyrevive and resume normal metabolism when they are re-moistened (Proctoret al., 2002). In a dehydrated desiccation tolerant plant an intense C02154 Tuba, Z. et al.emission can be observed in the very first minutes after re-wetting, which isconsidered to be a physical process; i.e. water replaces C02 moleculesabsorbed on the cell walls (Brown et al., 1983). However, this wetting burstis followed for a few hours by a respiration which has been termedresaturation respiration and which has a higher intensity than that ofconstantly metabolically active lichens (Smith & Molesworth, 1973). Thiselevated respiration does not serve the replenishment of the ATP poolbecause the latter is already completed within 5-10 minutes after rewetting(Krochko et al., 1979). Gordy and Hendrix (1982) considered theresaturation respiration of mitochondrial origin because they could eliminatecompletely the 02 uptake during this phase with the simultaneous usage ofcyanide and salicylhydroxamic acid. The increasing evidence of membranedestruction in desiccated lichens led to the conclusion that resaturationrespiration is a result of the uncoupled inner mitochondrial membrane(Farrar & Smith, 1976).The initially high rehydration respiration rate is also occurring in thehigher/flower desiccation-tolerant higher flowering plants, like in themonocot Xerophyta scabrida where it lasts up to 30 hours (Tuba et al.,1994). In the lichens and mosses the resaturation respiration lasts only fromfew minutes up to 5 h (e.g. Smith & Molesworth 1973; Bewley et al. 1978).In order to reveal the biochemical background of the resaturationrespiration, we treated a highly desiccation tolerant cryptogamic species, thelichen Cladonia convoluta (see: Tuba et al., 1996) with uncouplers, withpotassium cyanide (KCN) and bromoxynil (Kerr and Wain, 1964 and Hocket al., 1995) or we deprived them of oxygen by applying inert N2 gas. Ouraim was to identify the possible cause of the boosted C0 2 efflux during therehydration of the desiccated C. convoluta lichen thallus.Materials and MethodsThe foliose green algae lichen thallus Cladonia convoluta (Lam.) P.Cout. were used in the experiment after being collected from a semi-desertsand grassland (Fekete at al., 1997) near Fülöpháza (Hungary, Great Plain).The samples were cleaned by rinsing in deionized water and placed on wetfilter paper. The upper green part of the moss and the separated healthy lobesof lichen thallus were used. Prior to desiccation plants spent 24 hours in a metabolically active state (20 °C, 100% Rh, 200 jiM m"2 sec 1 PhAR for 14hours). Slow desiccation was carried out on the next day when Rh waslowered to 70%. For rehydration deionized water (control, N2-treatment), 10"3 M KCN, and 10~3 M bromoxynil (4-hydroxy-3,5 dibromo benzonitrile)were applied. Rehydration was conducted in small Plexiglas chambers(20 °C, 100% Rh, 200 pM m"2 sec"1 PhAR). C02 gas exchangemeasurements were carried out according to Tuba et al. (1996) in five Pentose-Phosphate Pathxay as the Possible Background. 155replications with a ADC LCA2 (Hoddesdon, UK) infrared gas analyser inthe first 30 minutes after rewetting.Results and DiscussionThe basic respiration rate of the continuously wet lichen C. convoluta was 2.6±0.29. However, the resaturation respiration rateof the wetted lichenwas three times higher (Fig. 1.). The high intensity rehydration('resaturation') respiration was terminated within 30 minutes and during theremaining 90 min of the experiment the respiration declined to a steady level(data not shown).Treatment with bromoxynil, an uncoupler of oxidative phosphorylation,increased this already high C02 emission by 66% indicating that theextraordinarily massive C02 efflux does not come entirely from themitochondria, which has lost adenylate control due to uncoupled innermembranes. Nitrogen exposure (anaerobic conditions) and KCN treatmentresulted in a surprising coincidence. They both decreased C02 emission rateby 30% in the lichen. This fact suggests that there is a component, which isnon-sensitive to both cyanide and also oxygen deprivation. The onlybiochemical process, which can produce a significant amount of C02 in notsenescing plant cells under anaerobic conditions, is the pentose-phosphatepathway. This pathway can play an essential part in the restoration of theplant's redox status by producing NADPH (Kranner & Grill, 1994).This observation also infers that the alternative mitochondrial pathway isnot engaged after rehydration of the desiccated tissues, because C02emission was not decreased more by the lacking of 0 2 than by cyanide,which clogs cytochrome pathway selectively. Due to the Bahr-Bonner model(Lambers, 1982), which considers the alternative oxidative pathway as anoverflow, operating the alternative pathway would not make too much sensein desiccation tolerant plants spending its resources for recovery from thedesiccated stage.Based on the above findings we would like to emphasise that thepreponderance of resaturation respiration of the desiccated lichen thalliprobably originates from the pentose-phosphate pathway.AcknowledgementsThe support to Zoltán Tuba by a DAAD (Bonn) professorial fellowshipand a NATO senior fellowship at Botanical Institute II of the KarlsruheUniversity is gratefully acknowledged.156 Tuba, Z. et al.Fig. 1. Rates of resaturation respiration and basal respiration (as percentage of the control plants) of the rehydrating desiccated lichen C. convoluta thalli in the control, and in the KCN ( I f f 3 M), bromoxynil ( I f f 3 M) and N2 treated lichen (n = 5, bars represent standard deviations). Note that the rate of resaturation respiration was four times higher than the so-called basal (basic) respiration. ReferencesBEWLEY, J . D., HALMER, P., KROCHKO, J . E., WINNER, W . E. (1978): Metabolism ofa drought- tolerant and a drought-sensitive moss. Respiration, ATP synthesisand carbohydrate status. In: Dry biological system, pp. 185-203, Crowe, J.H., Clegg, J. S., eds. Academic Press, New York.BROWN, D. H., MACFARLANE, J . D., KERSHAW, K . A. (1983): Physiologicalenvironmental interactions in lichens. XVI. A reexamination of resaturationrespiration phenomena. New Phytologist 93, 237-246.FARRAR, J. F., SMITH, D. C. (1976): Ecological physiology of the lichen Hypogymniaphysodes. III. The importance of the rewetting phase. New Phytologist. 77,115-125.FEKETE, G. , TUBA, Z . AND MELKÓ, E. ( 1 98 8 ) : Background processes at the populationlevel during succession in grasslands on sand. Vegetatio, 77, 33-41.GORDY, V. R., HENDRIX, D. L. (1982): Respiratory response of the lichensRamalina stenospora Miill. Arg. and Ramalina complatana (Sw.) Ach. toazide, cyanide, salicylhydroxamic acid and bisulfite during thallus hidration.The Bryologist 85, 361-374.Pentose-Phosphate Pathxay as the Possible Background. 157HOCK, B. , FEDTKE, C., SCHMIDT, R. R. ( 1 9 9 5 ) : Herbizide, Entwicklung,Anwendung, Wirkungen, Nebenwirkungen. Thieme Verlag StudtgartKERR, M . W . , WAIN, R . L. (1964): The uncoupling of oxidative phosphorylation inpea shoot mitochondria by 3,5- diiodo-4-hydroxy benzonitrile (ioxynil) andrelated compounds. Ann. Apl. Biol. 54, 441-446.KRANNER, I., GRILL, D . ( 19 9 4 ) : Rapid changes of the glutathione status and theenzymes involved in the reduction of glutathione-disulfide during the initialstage of wetting of lichens. Cryptogamic Botany 4, 203-206.KROCHKO, J .E . , WINNER, W.E., BEWLEY, D. ( 1 9 7 9 ) : Respiration in relation toadenosine triphosphate content during desiccation and rehydration of a desiccation-tolerant and a desiccation-intolerant moss. Plant Physiology 64,1 3 - 1 7 .LAMBERS, H. ( 1 9 82 ) : Cyanide-resistant respiration: A non-phosphorilating electrontransport pathway acting as an energy overflow. Physiologia Plantarum 55,4 7 8 - 4 8 5 .PROCTOR, C. F., TUBA, Z. (2002): Poikilohydry and homoihydry: antithesis orspectrum of possibilities? Transley review no. 141, New Phytologist 156,327-349.SMITH, D . C . , MOLESWORTH, S. ( 1973 ) : Lichen physiology. X I I I . Effects ofrewetting dry lichens. New Phytologist. 72 , 525—533.TOMLIN, C. (ed) (1994): The Pesticide Manual, 10th edition, British Crop ProtectionCouncil, Farnham / U.K. , pp. 121-123.TUBA, Z., CSINTALAN, ZS. AND M . C. F. PROCTOR ( 1 9 9 6 ) : Photosynthetic responsesof a moss, Tortula mralis (Hedw.) Gaertn. et al. ssp. ruralis, and the lichensCladonia convoluta (Lam.) P. Cout. and C. furcata (Huds.) Schrad. to waterdeficit and short periods of desiccation, and their eco-physiologicalsignificance: a baseline study at present-day C02 concentration. NewPhytologist 133, 3 5 3 - 3 6 1 .TUBA, Z., LICHTENTHALER, H . K . , CSINTALAN, ZS., NAGY, Z. AND SZENTE, K.(1994): Reconstitution of chlorophylls and photosynthetic C02 assimilationin the desiccated poikilochlorophyllous plant Xerophyta scabrida uponrehydration. Planta 192, 414-420.

Pentose-phosphate pathway as the possible background of resaturation respiration in the desiccation-tolerant  lichen Cladonia convoluta

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Pentose-phosphate pathway as the possible background of resaturation respiration in the desiccation-tolerant lichen Cladonia convoluta

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