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C Values of Crassulacean Acid Metabolism Plants Reflect the Proportion of CO2 Fixed During Day and Night?1

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C Values of Crassulacean Acid Metabolism Plants Reflect the Proportion of CO2 Fixed During Day and Night?1 How Closely Do the ␦13C Values of Crassulacean Acid Metabolism Plants Reflect the Proportion of CO2 Fixed during Day and Night?1 Klaus Winter* and Joseph A.M. Holtum Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Ancon, Republic of Panama (K.W.); and Department of Tropical Plant Sciences, School of Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia (J.A.M.H.) ␦13 The extent to which Crassulacean acid metabolism (CAM) plant C values provide an index of the proportions of CO2 fixed during daytime and nighttime was assessed. Shoots of seven CAM species (Aloe vera, Hylocereus monocanthus, Kalanchoe beharensis, Kalanchoe daigremontiana, Kalanchoe pinnata, Vanilla pauciflora, and Xerosicyos danguyi) and two C3 species (teak [Tectona grandis] and Clusia sp.) were grown in a cuvette, and net CO2 exchange was monitored for up to 51 d. In species ␦13 exhibiting net dark CO2 fixation, between 14% and 73.3% of the carbon gain occurred in the dark. C values of tissues formed inside the cuvette ranged between Ϫ28.7‰ and Ϫ11.6‰, and correlated linearly with the percentages of carbon gained in the light and in the dark. The ␦13C values for new biomass obtained solely during the dark and light were Ϫ Ϫ estimated as 8.7‰ and 26.9‰, respectively. For each 10% contribution of dark CO2 fixation integrated over the entire experiment, the ␦13C content of the tissue was, thus, approximately 1.8‰ less negative. Extrapolation of the observations to plants previously surveyed under natural conditions suggests that the most commonly expressed version of CAM in the field, “the typical CAM plant,” involves plants that gain about 71% to 77% of their carbon by dark fixation, and that the isotopic signals of plants that obtain one-third or less of their carbon in the dark may be confused with C3 plants when identified on the basis of carbon isotope content alone. ␦13 Ϫ Soon after the discovery that C4 plants differ dis- ited a C value of 25.5‰, and plants supplied 13 12 ␦13 tinctively from C3 plants in their C/ C compo- with CO2 only during the dark exhibited a C value Ϫ sition (Bender, 1968, 1971), it was proposed that, in of 10.6‰, whereas plants supplied with CO2 dur- Crassulacean acid metabolism (CAM) plants, the 13C ing the day and the night exhibited an intermediate to 12C ratio may be an indicator of the extent to which ␦13C value of Ϫ15‰. Subsequent theoretical and ex- their biomass was derived from nocturnal CO2 fixa- perimental evidence demonstrated that fractionation tion relative to diurnal CO2 fixation (Bender et al., in CAM plants reflects both carboxylation and diffu- 1973; Osmond et al., 1973; Allaway et al., 1974). The sion limitations (O’Leary and Osmond, 1980; O’Leary, 13 12 Cto C ratio is an indicator because the enzyme 1981; Holtum et al., 1983, 1984), which, in turn, are responsible for net CO2 uptake in the dark, PEP modified by temperature (Deleens et al., 1985), envi- 13 carboxylase, discriminates less against C than does ronmental stresses (Osmond et al., 1976), and the leak- Rubisco, the enzyme responsible for most net CO 2 age of CO2 from the tissues (O’Leary, 1988; Broad- uptake during the light. CAM plants, which gain CO2 meadow et al., 1992; Borland and Griffiths, 1996). almost exclusively at night via PEP carboxylase, This interpretation of whole-plant carbon isotope ␦13 would, thus, be expected to show C values similar contents provided the theoretical basis for the use of ␦13 13 to C4 plants, whereas the C values of plants in ␦ C values to screen plants for CAM, particularly in which dark CO2 fixation contributes only little to the tropics (Rundel et al., 1979; Winter, 1979; Teeri et carbon gain should resemble those of C3 plants. The al., 1981; Griffiths and Smith, 1983; Winter et al., postulate was supported by evidence such as that of 1983; Earnshaw et al., 1987; Arroyo et al., 1990; Kluge Nalborczyk et al. (1975) who reported that well- et al., 1991; Zotz and Ziegler, 1997). In recent analyses watered young Kalanchoe daigremontiana plants sup- on the evolution of CAM in the Bromeliaceae and the plied for 24 d with CO2 solely during the light exhib- ␦13 closely related, reportedly C3 Rapateaceae, the C values of about two-thirds of the 2,800 known species 1 This research was supported by the Andrew W. Mellon Foun- of bromeliads and 85 of the approximately 100 spe- dation through the Smithsonian Institution, by the Smithsonian cies of the Rapateaceae were determined (Crayn et Tropical Research Institute, by the Australian Research Council, al., 2001; D.M. Crayn, J.A.C. Smith, and K. Winter, and by Dr. Rosemary G. Dunn. *Corresponding author; e-mail [email protected]; fax unpublished data). The survey of Bromeliaceae ␦13 507–212–8148. yielded a bimodal distribution of C values, with Article, publication date, and citation information can be found frequency peaks around Ϫ13‰ (indicating strong Ϫ at www.plantphysiol.org/cgi/doi/10.1104/pp.002915. CAM) and 26‰ (indicating C3 species). The rap- Plant Physiology, August 2002, Vol. 129, pp. 1843–1851, www.plantphysiol.org © 2002 American Society of Plant Biologists 1843 Winter and Holtum ateads exhibited a broad but unimodal distribution of fixation were grown inside a gas-exchange cuvette for ␦13 Ϫ Ϫ C values between 37.7‰ and 19.8‰. From such up to 51 d, during which time the proportions of CO2 and other studies, it has been estimated that more than fixed in the light and dark were quantified. The rela- 6% of vascular plant species have some ability to tionships between the proportions of CO2 fixed in the exhibit CAM (Smith and Winter, 1996; Winter and light and dark and the ␦13C value of the biomass Smith, 1996). accumulated were then assessed. A shortcoming of using whole-tissue carbon iso- tope surveys to obtain an integrated value of the RESULTS contributions of dark and light CO2 fixation to total carbon gain is that, in the absence of measurements Plant Growth and Carbon Gain of acidity, CO exchange, or instantaneous carbon 2 During the 12 to 51 d inside the gas-exchange isotope discrimination, it is unclear where C3 ends 13 cuvette, tissues exhibited increases in dry mass of and CAM begins. In general, surveys of plant C/ between 2.6- and 10.3-fold, indicating that between 12C composition indicate a least negative limit for C 3 61% and 99% of the material harvested from the species of around Ϫ23‰ to Ϫ20‰, values that can cuvette at the end of the experiments was formed also indicate some CAM activity. Confirmed CAM during the experiments (Table I). Leaf areas ex- species such as Tillandsia usneoides, Didierea madagas- panded up to 17.3-fold (Table I). The smallest in- cariensis Microsorium punctatum H. Baill., and (L.) crease in leaf area, a 1.2-fold increase by leaves from Copel. have been reported to exhibit values of Xerosicyos danguyi, was compensated for by an ex- Ϫ19.8‰ (Griffiths and Smith, 1983), Ϫ21.2‰ (Win- Ϫ pansion in leaf thickness that was reflected in a 290% ter, 1979), and 22.6‰ (Holtum and Winter, 1999), increase in dry mass. The length of the stem of Hy- respectively. Moreover, diel acid fluctuations have locereus monocanthus in the cuvette extended from 0.5 been measured in Tillandsia elongata H.B.K. var sub- to 17.3 cm. imbricata (Baker) L.B. Sm. and Guzmania monostachia (L.) Rusby ex Mez var monostachia, species for which 13 ␦ C values of Ϫ26.4‰ and Ϫ26.5‰, respectively, Patterns of Net CO2 Exchange have been reported (Griffiths and Smith, 1983). The species examined exhibited a variety of pro- O’Leary (1988) predicted a linear relationship be- portions of light and dark CO uptake, with net tween ␦13C values of CAM plants and the propor- 2 carbon gain in the dark ranging between 0% and tions of CO2 fixed at night and during the day. Sur- 73.7% of the cumulative net carbon gain (Table I). prisingly, given the number of isotopic surveys of The diversity of C3 and CAM patterns of CO2 ex- vegetation that have been published, O’Leary’s pre- change observed is depicted during the final 24 h of diction has never been tested experimentally. each experiment (Figs. 1–4). The proportion of dark O’Leary cautioned that his qualitative model did not fixation by K. pinnata responded to the thermoperiod take into account environmental interactions. If one (Fig. 1). At a high night temperature of 25°C, 100% of assumes that, for a given species subject to a given set Ϫ the net CO2 fixation occurred during the light, of conditions, 28‰ is the isotope composition whereas at a night temperature of 17°C, up to 33% of when 100% of the CO2 is fixed by Rubisco in the light the total carbon gain was derived during the dark then, theoretically, any ␦13C value less negative than Ϫ (Fig. 1; Table I). When the night temperature was 28‰ indicates that some dark fixation occurs. decreased from 25°Cto21°C, the 12-h net carbon However, in the real world, chemical and diffusional gain remained negative, although a low rate of net processes contribute to the isotopic composition of CO fixation was observed during the latter one-half ␦13 2 plants, such that integrated tissue C values are of the dark period. Low temperature-associated in- affected by plant biochemistry, plant-environment creases in net carbon gain during the dark by K. 13 12 interactions and the C/ C composition of the pinnata were accompanied by reductions in the source air, all of which exhibit variation (O’Leary, amounts of CO2 assimilated during the light and a 1981; Farquhar et al., 1989; Griffiths, 1992).
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