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Crassulacean Acid Metabolism Influences D/H Ratio of Leaf Wax in Succulent Plants

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Crassulacean Acid Metabolism Influences D/H Ratio of Leaf Wax in Succulent Plants This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Organic Geochemistry 41 (2010) 1269–1276 Contents lists available at ScienceDirect Organic Geochemistry journal homepage: www.elsevier.com/locate/orggeochem Crassulacean acid metabolism influences D/H ratio of leaf wax in succulent plants ⇑ Sarah J. Feakins a, , Alex L. Sessions b a University of Southern California, Department of Earth Sciences, Los Angeles, CA 90089-0740, USA b California Institute of Technology, Department of Geological and Planetary Sciences, Mail Stop 100-23, Pasadena, CA 91125, USA article info abstract Article history: This study sought to characterize hydrogen isotopic fractionation during biosynthesis of leaf wax n- Received 19 March 2010 alkanes in succulent plants capable of crassulacean acid metabolism (CAM). The metabolic and physio- Received in revised form 15 June 2010 logical features of CAM represent crucial strategies for survival in hot and dry climates and have been Accepted 10 September 2010 hypothesized to impact hydrogen isotope fractionation. We measured the stable carbon and hydrogen Available online 17 September 2010 isotopic compositions (d13C and dD, respectively) of individual n-alkanes in 20 species of succulent plants from a global collection of the Huntington Botanical Gardens, San Marino, California. Greenhouse condi- tions and irrigation with water of constant dD value enabled determination of interspecies differences in net D/H fractionation between source water and leaf wax products. Carbon isotope ratios provide con- 13 straints on the extent of CAM vs. C3 photosynthesis and indicate a wide range of CAM use, with d C val- ues ranging from À33.01‰ to À18.54‰ (C27–C33 n-alkanes) and À26.66‰ to À17.64‰ (bulk tissue). Despite the controlled growth environment, we observed ca. 90‰ interspecies range in dD values from 13 2 13 À193‰ to À107‰. A positive correlation between d Cbulk and dDC31 values with R = 0.60 (d CC31 and 2 dDC31 values with R = 0.41) implicates a metabolic isotope effect as the dominant cause of interspecies variation in the hydrogen isotopic composition of leaf wax n-alkanes in CAM-intermediate plants. Ó 2010 Elsevier Ltd. All rights reserved. 1. Introduction CAM, including cycling between C3 and CAM pathways, and the degree of CAM use can be monitored by way of the carbon isotopic Succulent plants using crassulacean acid metabolism (CAM) ex- discrimination recorded in plant tissue (Osmond et al., 1973; hibit substantial flexibility in metabolic pathways, particularly for Sternberg et al., 1984b,c). Several studies have reported effects of carbon fixation. Carbon isotopes in plant bulk tissue and leaf waxes CAM on the composition of hydrogen isotopes in cellulose (Stern- can be used to evaluate the use of differing carbon fixation path- berg et al., 1984c) and individual n-alkyl lipids (Chikaraishi and ways. C3 plants, using the Calvin–Benson cycle, produce leaf wax Naraoka, 2007). An early study of bulk lipids did not reveal differ- 13 n-alkanes with d C values of À35 ± 5% and C4 plants, using the entiation of dD values between C3 and CAM plants (Sternberg et al., Hatch-Slack cycle, generate values of À20 ± 5% (Collister et al., 1984a), and this might be attributable to the large isotopic offsets 1994; O’Leary, 1981). Succulent plants capable of CAM have extre- between acetogenic and isoprenoid lipids (Chikaraishi et al., 2004; mely variable d13C values for bulk tissue, typically intermediate Sessions et al., 1999; Zhang and Sachs, 2007) that are necessarily between those of C3 and C4 plants, although the ranges partially conflated in bulk analysis. overlap (Osmond et al., 1973). This carbon isotope variability de- In contrast, there is limited evidence for a difference in dD values rives from the ability of CAM-enabled plants to use CAM or C3-like of individual n-alkanes between C3 plants and CAM plants. Data are pathways to varying degrees (Osmond et al., 1989). Thus, CAM available for three species: Ananas comosus (pineapple, dDC31, 13 13 plants provide an opportunity to investigate hydrogen isotopic À194‰, d Cbulk, À13.6‰, d CC31, À20.5‰) from Thailand, Lycoris 13 13 fractionation associated with changing metabolic pathways. radiata (red spider lily, dDC31, À186‰, d Cbulk, À21.9‰, d CC31, 13 CAM metabolism is an adaptation to drought and is distin- À27.8‰) and Colocasia esculenta (coco yam, dDC31, À179‰, d Cbulk, 13 guished by the night time fixation of CO2 into malic acid, allowing À27.1‰, d CC31, À34.0‰) from Japan (Chikaraishi and Naraoka, 13 stomata to open only at night when the relative humidity is higher 2003). We note that d Cbulk values indicate that these are C3-CAM (Osmond et al., 1989). Decarboxylation and net CO2 fixation then intermediates displaying a wide range of CAM use; A. comosus, dis- proceed in the light while stomata are closed. CAM effectively min- plays the least negative and most CAM-like d13C value. Comparison 13 13 imizes water loss, but also slows photosynthesis and growth. Suc- of the d Cbulk and d CC31 values yields a positive correlation with 2 13 culent plant species may therefore employ variable degrees of R = 0.99, indicating that d CC31 represents a valid proxy for CAM activity. The dD values reported for these CAM plants are more neg- ative than for C3 and C4 plants sampled in the same study, although ⇑ Corresponding author. Tel.: +1 213 740 7168. unknown source waters make comparisons of net fractionation E-mail address: [email protected] (S.J. Feakins). 0146-6380/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.orggeochem.2010.09.007 Author's personal copy 1270 S.J. Feakins, A.L. Sessions / Organic Geochemistry 41 (2010) 1269–1276 between water and lipids uncertain. Another study in Guangzhou, gen isotopic fractionation recorded in individual leaf wax n-al- China by Bi et al. (2005) reported data for three species: Euphorbia kanes to varying degrees of CAM metabolism. 13 trigona (African milk tree, dDC31, À182‰, d CC31, À29.4‰), Opuntia 13 dillenii (prickly pear, dDC31, À152‰, d CC31, À25.1‰) and Hylocere- 2. Sample selection 13 us undatus (night blooming cactus, dDC31, À171‰, d CC31, À21.8‰). We have recently reported data for a single CAM plant from the Leaf samples were collected from a variety of specimens from 13 Mojave Desert, Opuntia basilaris, with d Cbulk, À13.5‰, indicating the global collection of succulents cultivated in the ‘desert green- full CAM expression under drought stress, and affording a dD value house’ at the Huntington Botanical Gardens, San Marino, Califor- more positive than for C3 plants sampled in the same study. The dD nia (hereafter ‘the Huntington’; Table 1). The collection includes value of the C33 n-alkane was À124‰ and the value for the environ- specimens from several continents representing species that are mental water was À79‰ (Feakins and Sessions, 2010). The calcu- rare, endangered or of special historical or economic importance. lated net fractionation of À47‰ is smaller than the À91 ± 32‰ Most are succulents and all are <1 m tall. We chose plants in a net fractionation for C3 plants (C27,29,31 n-alkanes). Comparison is greenhouse environment where all water for growth is supplied tenuous given the limited data, so we initiated a study to test by irrigation from an on-site well (dD À45.09 ± 0.24‰). This min- whether increasing CAM use alters net hydrogen isotopic imizes variation in water dD value that might otherwise influence fractionation. the plant leaf wax lipids. In addition, the greenhouse environment Hydrogen isotope studies of non-CAM plants have identified greatly reduces the environmental variability experienced by large (up to 100‰) interspecies variability in net isotopic fraction- plants, including factors such as rooting depth, canopy position ation (e.g. Chikaraishi and Naraoka, 2003; Hou et al., 2007b; Krull and microclimate, as well as isotopic disequilibrium between soil et al., 2006; Liu and Huang, 2005). In some cases the variability has water and water vapor. All the plants experience the same semi- been linked to variation in life form (i.e. tree, shrub and grass), with controlled environmental conditions in a covered greenhouse. the largest offset observed for grass (Hou et al., 2007b; Liu et al., Temperature ranges between 3 and 42 °C annually, with an aver- 2006). Other studies have linked variation in dD values to differ- age diurnal temperature range of 25 °C. Relative humidity aver- ences between C3 and C4 pathways (Chikaraishi, 2003; Smith and aged lows of 26% during June and July 2005. No long term Freeman, 2006). Given the large interspecies variability reported monitoring of relative humidity was available, but all species 13 for non-CAM species and the known range of variability in d C val- experienced equivalent environmental conditions. Leaf samples ues for CAM plants, we anticipated variable net hydrogen isotopic were collected to assess interspecies variation in chain length fractionation in CAM plants. and carbon and hydrogen isotopic composition of leaf wax n- Most CAM plants are succulents and form a significant compo- alkanes. nent of many arid sub-tropical environments. However, the nature of arid climates – with intermittent rain, large inter-annual vari- 3.
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