Reconstitution of Photosynthesis Upon Rehydration in the Desiccated Leaves of the Poikilochlorophyllous Shrub Xerophyta scabrida at Elevated CO2

j. Nznt PhysioL ItVl. 148. pp. 345-350 (J996j

Reconstitution of Photosynthesis Upon Rehydration in the Desiccated Leaves of the Poikilochlorophyllous Shrub Xerophyta scabrida at Elevated CO2 1 ZSOLT CSINTALAN , ZOLTAN TUBA1,3, HARTMUT

K.

2 LICHTENTHALER ,

and JOHN

GRACE

3

I

Plant Physiological Section, Department of Botany and Plant Physiology, Agricultural University of G6d6115, H-2103 G6d6115, Hungary

2

Botanical Institute II (Plant Physiology and Plane Biochemistry), University of Karlsruhe, Kaisersrrage 12, D-76128 Karlsruhe, Germany

3

Institute of Ecology and Resource Managemene, University of Edinburgh, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, UK

Received June 24, 1995 . Accepted September 25, 1995

Summary

We report the resynthesis of the photosynthetic apparatus and the restoration of its function in the monocotyledonous C 3 shrub Xerophyta scabrida (Pax) Th. Our. et Schinz (Velloziaceae) following a period of 5 years in the air-dried state. Detached leaves were rehydrated at present (350 Jlmol mol-I) and at elevated CO 2 (700 Jlmol mol-I). Elevated CO 2 concentration had no effect on the rate of rehydration, nor on the de novo resynthesis pattern of the chlorophylls and carotenoids or the development of photochemical activity in the reviving desiccated leaves. The time required to fully reconstitute the photosynthetic apparatus and its function in the air-dried achlorophyllous leaves on rehydration did not differ at the two CO 2 concentrations. However, respiratory activity during rehydration was more intensive and of longer duration at high CO 2 and net CO 2 assimilation first became apparent 12 h later than in the leaves rehydrated at present CO 2, Mter reconstitution of the photosynthetic apparatus, the net CO 2 assimilation rate was higher in the high CO 2 leaves, however it rapidly declined to a value lower than that in the present CO 2 plants due to acclimation. This acclimation to elevated CO 2 occurred only after complete reconstitution of the photosynthetic apparatus. The downward acclimation of photosynthesis was accompanied by a decrease in content of photosynthetic pigments (chlorophyll a+ band carotenoids x+c) and stomatal conductance. The initial slope of the Nc; curve for the high CO 2 leaves was much lower and net CO 2 assimilation rates were lower at all c;'s than in the present CO 2 plants. The rate of respiration also decreased and the C-balance of the high CO 2 leaves therefore remained similar to that of leaves in present CO 2 ,

Key words: Acclimation, A!cijunction, carotenoids, elevated CO2, net CO2 assimilation, respiration, stomatal conductance. variable chlorophyllfluorescence decrease ratio (Rid value). Abbreviatiom: A = CO 2 assimilation rate; a + b = chlorophyll a and b; Cj = intercellular CO 2 concentration; g, = stomatal conductance; HOT = homoiochlorophyllous desiccation tolerant; PDT = poikilochlorophyllous desiccation tolerant; Rfd 690 = variable chlorophyll fluorescence ratio at 690 nm; RuBisCO = RuBP carboxylase/oxyenase; SLA = specific leaf area; x+c = total carotenoids (xanthophylls x and carotenes c). © J996 by Gustav Fischet Verlag, Stuttgart

346

ZSOLT CSINTALAN, ZOLTAN TUBA, HARTMUT K. LICHTENTHALER, and JOHN GRACE

Introduction There have been many reports on the impacts of long-term high CO 2 on plants (see ego recent reviews of Jarvis, 1993; Ceulemans and Mousseau, 1994). Dahlman (993) has reviewed the combined effects of elevated CO 2 and other environmental factors. The interaction of high CO 2 with water stress (drought) has been especially intensively investigated (Morison, 1993; Rogers and Dahlman, 1993). However, the effect of elevated CO 2 on desiccation tolerant plants has not been investigated. These species can survive years of desiccation. Desiccation tolerance is relatively infrequent in plants and is rare in angiosperms (Gaff, 1977; Gaff, 1989). However, it is important in certain vegetation zones, such as deserts and semi-deserts in the dry tropics, in dry-wet tropical vegetation formations, in temperate continental climates and in arid boreal areas. Any analysis of the impact of high CO 2 on terrestrial vegetation guarantees investigation of this rather neglected group, the desiccation tolerant (DT) plants. DT plants form two groups (Hambler, 1961; Bewley, 1979; Gaff, 1989; Tuba et al., 1993 a): a) those, which preserve their chlorophyll content and photosynthetic apparatus during desiccation, are called homoiochlorophyllous DT (HOT), and b) those, which lose their chlorophylls and thylakoids, are termed poikilochlorophyllous DT (PDT). In the latter the photosynthetic apparatus with its pigments and thylakoids is resynthesised on rehydration (Gaff, 1989; Tuba et al., 1994a). Elevated CO 2 affects photosynthesis (Sage et al., 1989; Arp and Drake, 1991; Jarvis, 1993), and the PDT mechanism itself causes profound changes in the photosynthetic apparatus during desiccation and rehydration. Therefore, it was hypothesised that high atmospheric CO 2 would influence both the reconstitution of the photosynthesis and the functional revival of the desiccated PDT plants on rehydration. Hence, we examined the reconstitution of the photosynthetic apparatus and its function including CO 2 assimilation in Xerophyta scabrida, a PDT monocot C 3 shrub, at rehydration of detached leaves at present (350 Ilmol mol-I) and at elevated (700 Ilmol mol-I) CO 2 following a period of 5 years in the air-dried state. The development of pigment resynthesis, thylakoid function, photosynthetic CO 2 assimilation and respiration was followed from the beginning of rehydration and revival through the acclimation of photosynthesis to elevated CO 2 , This is the first report on the reconstitution of photosynthesis in a desiccated (PDT) plant at elevated CO 2 ,

Materials and Methods

(Uluguru Mts., Mindu Hill, SSW of Morogoro town at 650 m altirude) by the end of rhe dry season in 1988 and were stored in airtight polythene bags.

Rehydration procedure Desiccated leaves were allowed to rehydrate as described earlier (Tuba et aI., 1994a) in 45 L plexiglass chambers, which provided rhe control of COlo air humidity, lighr and temperature. Glass jars containing the leaves (fixed in a vertical position) with one half of rheir laminae immersed in distilled warer were placed in the chambers. The measurements were made on the middle portion of upper halves of the leaves which were rehydrated and revived in air. The chambers were illuminated by a halogen light source (Osram Powerstar Mercury HQIE lamps) to provide 1000 Ilmol m- 2 s·J of photon flux density. A 5 cm thick filter of streaming water was applied between the light source and the chambers. Temperature was kept at 25 "c. The air CO 2 concentrations were maintained at 350 Ilmol mol- J in the control and at 700 Ilmol mol- 1 in the elevated CO 2 chambers. An electromagnetic valve controlled by an infrared gas analyser (Tuba et aI., 1994 b) was used to maintain the elevated CO 2 concentration and axial ventilators provided the mixing of the entering CO 2 with air. For the ambient chambers air cylinders supplied the 350 Ilmol mol-I CO2 air at a constant rate. Identical concentrations of CO 2 were continuously passed through the distilled water in which the leaves were immersed and an air pump also ensured the further aeration of the water. The water was kept at 23 "C and frequently changed.

CO2 gas exchange measurements The rates of (rehydration and dark) respiration and CO 2 exchange in the light were measured using an LCA2-type IRGA system (ADC Co. Ltd., Hoddesdon, U.K.), operated in differential mode and Parkinson LC-N leaf chamber, as previously described (Tuba et aI., 1994 a). CO 2 dependence of light saturated ner CO 2 assimilation rates (Ncj curves) were measured using the same system (Tuba et aI., 1994 b). Ambient CO 2 concentrations of 100, 350, 500, 700 and 1000 Ilmol mol- J were produced by a gas diluter (GO 600, ADC Co. Ltd., Hoddesdon, U.K.). Gas-exchange parameters (A, Cj,) were calculated according to von Caemmerer and Farquhar (1981). Stomatal conductance (g,) was measured with an AP4 type mass flow porometer (Delta-T Devices Cambridge, U.K.). Leaf area was measured by a leaf area meter (LAM 001, Delta T Devices, Cambridge, U.K.). The Mitscherlich function (Thornley and Johnson, 1990) was used to fit curves to the data on NCj.

Other methods Leaf water and photosynthetic pigment (chlorophyll a+ b and carotenoid x+c) content and the variable chlorophyll fluorescence decrease ratio (Rfd) were measured as described earlier (Tuba et aI., 1993 b, 1994 a and 1994 b). Rehydrarion, with regreening was repeated four times with 150 leaves for both CO 2 concentration. Measurements were made in at least five replicate samples.

Species examined Xerophyta scabrUUI (Pax) Th. Our. er Schinz, is a member of rhe Velloziaceae family (Velloziales, relared to Bromeliales). It is a C 3 (srable carbon isotope ratio ol3 C = -27.3 %0) PDT pseudoshrub of about 40-90 cm in height, with perennial leaves, lacking secondary thickening (Tuba et aI., 1993 b). On the top of cliffs X scabrida forms an almost semi-desertlike bush vegetation on biotite migmarire and hornblende gneiss rocks with a long dry season of 5-6 months (P6cs, 1976). Air-dried leaves were collected in Tanzania

Results

water content and specific leafarea On placing the air-dried leaves of X scabrida in water, their water uptake began instantly and they rapidly unfolded 0-1.5 h). The leaf water content increased reaching over 90 % of its maximum in 8 h (Fig. 1A) with no further in-

347

Reconstitution of photosynthesis during rehydration under elevated CO 2 crease after 12 h. The specific leaf area (SLA) increased in a similar manner from 52.6 cm -2 g-I dry weight at the beginning to 163.5 cm -2 g-I after 12 h (Fig. 1B).

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Fig. 3: Development of the variable chlorophyll fluorescence decrease ratio (Rfd690) in air-dried, achlorophyllous leaves of X scabrida during revival and regreening at present (350 !lmol mol-I) and elevated CO 2 (700 !lmol mol-I) concentration. Dark bars represent standard deviation. CO 2 concentrations exceeded a value of 2.5, which is commonly found for photosynthetically fully active leaves (Lichtenthaler and Rinderle, 1988).

CO2 gas exchange Respiration in the rehydrating leaves of X scabrida was detectable 30 min after the start of rehydration (Fig. 4 A). CO 2

348

ZSOLT CSINTALAN, ZOLTAN TUBA, HARTMUT K. LICHTENTHALER, and JOHN GRACE

evolution increased sharply and reached its maximum after 2 h. The rehydration respiration had a higher peak in the high CO 2 leaves than in the present CO 2 ones, and it required longer (48 h) for them to decrease to a stable value. For both, the present and the high CO 2 leaves, the CO 2 exchange rates measured in the dark were identical to those in the light for 18 h after rehydration (compare Fig. 4 A with Fig. 4 B). After this the CO 2 production in the light decreased gradually due to the start of CO 2 assimilation. In the leaves rehydrating at present COl> net CO 2 assimilation was first measurable 24 h after rehydration but not until 36 h for the high CO 2 leaves (Fig. 4 B). Maximum rates of light saturated net CO 2 assimilation were reached at 72 h at both CO 2 concentrations. Subsequently, the rate fell in the high CO 2 leaves but was maintained in the present CO 2 leaves. 8 days after rehydration the NCj curve for the revived leaves did not reach saturation in the high CO 2 leaves, while it was saturated at 400 /lmol mol- 1 CO 2 in the present CO 2 plant leaves (Fig. 5 A). The initial slope of NCj curve for the high CO 2 leaves was much lower than for the present CO 2 ones, and net CO 2 assimilation rates in the high CO 2 leaves were lower at all c/s than in the leaves at present CO 2 , The increase in stomatal conductance after rehydration followed a similar course at both CO 2 concentrations but was

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The photosynthetic apparatus in the air-dried leaves of the PDT X scabrida, which were collected in its natural habitat, was found to be completely destroyed and the desiccoplasts (former chloroplasts) (Tuba et a!', 1993 b) did not contain chlorophylls. Water uptake prompted an immediate response in the leaves and signalled the end of the anabiotic state and the beginning of revival processes.

water relations and SLA CO 2 concentration had no effect on the rate of water uptake and water content in the leaves, and water relations were restored as in a previous study (Tuba et a!', 1994 a). The de-

Reconstitution of photosynthesis during rehydration under elevated CO 2 velopment of SLA was also unaffected by CO 2 concentration. The over three-fold increase in SLA at both CO 2 concentrations ensured a favourable leaf area to mass ratio for gas exchange in the reviving leaves (Tuba et al., 1994 a).

Respiration Respiration began rapidly at both CO 2 concentrations and became fully operational after 6 h of rehydration before the cells had reached full turgidity (Tuba et al., 1994a). This sugges~s th~t most of t~e respiratory enzymes were preserved at desICcation and dunng long-term air-dried anabiosis in the PDT X scabrida (Tuba et al., 1994a), in a similar way to that reported elsewhere for HOT's (Bewley, 1979; Harten and Eic~meier, 1?8~; Schwab et al., 1989). The duration of rehydration reSplfatlOn was longer in the high CO 2 leaves than in t~e present .C~2 ones. Most reports on long-term exposure to high CO 2 IlldlCate a decrease in respiration (Amthor, 1991; Bunce, 1994). However, those reports refer to studies made on photosynthesising leaves. Rehydration respiration is a special type of high intensity respiration which occurs in both HOT and PDT plants on rehydration preceding CO 2 assimilation (Smith and Molesworth, 1973; Proctor, 1990; Meenks et al., 1991; Tuba e.t a!., 1:94 a). The rate of the later appearing respiration III the fully revived leaves of X scabrida was consistent with the usual pattern and was lower at high CO 2 than at the present ones.

Photosynthetic apparatus On reviving, PDT plants need to rebuild a functional photosynthetic apparatus prior to the commencement of CO 2 assimilation. The rebuilding of the photosynthetic apparatus in POTs involves the resynthesis of chlorophyll a+ b (Tuba et al., 1993 a) and the reassembly of the thylakoids (Tuba et al., 1993 b). The amount of chlorophyll a+ b resynthesised in the leaves fully revived at high CO 2 concentration was lower than that in the present CO 2 leaves and is in agreement with ear!ier reports, which suggested that high CO 2 causes a decrease In chlorophyll a+ b content (Eamus and Jarvis, 1989; Houpis et al., 1988). The resynthesis of functional thylakoids were reflected by the developing of the photochemical activity (Fig. 3).

Photochemical activity and CO2 assimilation ~low chlorophyll fluorescence kinetics (Kautsky effect) and vanable fluorescence as expressed by Rfd values indicate the potential photochemical activity (Lichtenthaler, 1988; Lichtenthaler and Rinderle, 1988). Rfd values in this study indicated that the resynthesised chlorophylls and thylakoids in the rehydrating leaves became functional after 12 hand r~a~hed full capacity in 72 h. Thylakoid activity resumed in a similar manner with no difference in its intensity at both ~02 concentrations. Over the first 2 days of rehydration there IS yet not net CO 2 assimilation which only appeared after a threshold Rfd ratio of 1.5 was reached.

349

Acclimation ofphotosynthesis to an elevated CO2 concentration T.h~ synchronous appearance of maximum net photosyntheSIS III the leaves at both CO 2 concentrations indicated that the resynthesis of the photosynthetic apparatus and its full activation required identical time, independent of atmospheric CO 2 concentration. Acclimation to high CO 2 Qarvis, 1993) occurred only after the rebuilding of the photosynthetic apparatus was complete as was indicated by a drop in net photosynthesis rate, chlorophyll a+ b content and stomatal conductance between 72 hand 120 h. The differences in the characteristics of the photosynthetic apparatus in the leaves revived at the two different CO 2 concentrat~o?~ are illustrated in Fig. 5 A. At high CO 2 the reduced Illltlal slope of the NCj curve indicates a reduced Rubisco capacity (Caemmerer and Farquhar, 1984; Sharkey, 1985; Sage et al., 1989). The decrease in stomatal conductance at high CO 2 in this study (Fig. 5 B) is yet another case where CO 2 assimilation is affected to a large extent by reduced stomatal conductance in long-term high CO 2 exposure studies (Rogers et al., 1983; DeLucia et al., 1985; Jarvis, 1993). Stomatal conductance decre~es as Cj increases (Mott, 1988), and in plants grown at high CO 2 concentrations it may be more pronounced than in those grown at present CO 2 (Eamus and Jarvis, 1989; Tuba et al., 1994 b).

Conclusions

Photosynthesis in photosynthetically active leaves of X

scabrida, which were revived and maintained at high Cab showed a downward acclimation (sensu Jarvis, 1993) of the net CO 2 assimilation rate as compared to leaves of plants ke~t ~t ~resent CO 2, It is suggested that the lower net CO 2 assimilatIOn was caused by reduced Rubisco capacity. The rate of respiration also decreased in high CO 2 plants, and the C-balance of the leaves therefore remained similar to that in ~he present ~02 plants. The revival of the leaves is of great I~portance III .the natural habitat of X scabrida at the beginlllng of the ralllY season. The leaves revive first and resume activity; the initiation of adventitious root begins only when the revival of the leaves has been completed (Tuba et al., 1993 b). Therefore the findings of in this study are of relevance for modelling the revival of X scabrida and possibly other PDT's at their natural habitat, especially in view of a future higher CO 2 environment.

Acknowledgements

The present work was funded by the ECOCRAFT Environment (EC Brussels), also supported by the Hungarian SCientIfic Research Foundation (OTKA 1/3.1545, I/4 F5359, and C0294). Financial support by Phare/Accord and Soros Foundation (Budapest) is also acknowledged (ZT). We wish to thank Professor T. Poes (E~er, Hungary - M.orogoro, Tanzania) for collecting the plant matenal and Dr. N. Smlrnoff (Exeter) for his valuable suggestions on the manuscript. R~D. Programme

350

ZSOLT CSINTALAN, ZOLTAN TUBA, HARTMUT K. L!CHTENTHALER, and JOHN GRACE

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