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WHOLE PLANT AND ECOPHYSIOLOGY

Discrimination in the Dark. Resolving the Interplay between Metabolic and Physical Constraints to Phosphoenolpyruvate Carboxylase Activity during the Crassulacean Acid Metabolism Cycle¹

Physiological Ecology Group, Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom (H.G.); Molecular Plant Physiology Group (H.G., A.B.C., M.R.B., S.v.C.) and Australian Research Council Center of Excellence, Plant Energy Biology (M.R.B.), Research School of Biological Sciences, Australian National University, Canberra, Australian Capital Territory, 2601 Australia

A model defining carbon isotope discrimination (¹³C) for crassulacean acid metabolism (CAM) plants was experimentally validated using Kalanchoe daigremontiana. Simultaneous measurements of gas exchange and instantaneous CO₂ discrimination (for ¹³C and ¹⁸O) were made from late photoperiod (phase IV of CAM), throughout the dark period (phase I), and into the light (phase II). Measurements of CO₂ response curves throughout the dark period revealed changing phosphoenolpyruvate carboxylase (PEPC) capacity. These systematic changes in PEPC capacity were tracked by net CO₂ uptake, stomatal conductance, and online ¹³C signal; all declined at the start of the dark period, then increased to a maximum 2 h before dawn. Measurements of ¹³C were higher than predicted from the ratio of intercellular to external CO₂ (p_i/p_a) and fractionation associated with CO₂ hydration and PEPC carboxylations alone, such that the dark period mesophyll conductance, g_i, was 0.044 mol m^–2 s^–1 bar^–1. A higher estimate of g_i (0.085 mol m^–2 s^–1 bar^–1) was needed to account for the modeled and measured ¹⁸O discrimination throughout the dark period. The differences in estimates of g_i from the two isotope measurements, and an offset of –5.5 between the ¹⁸O content of source and transpired water, suggest spatial variations in either CO₂ diffusion path length and/or carbonic anhydrase activity, either within individual cells or across a succulent leaf. Our measurements support the model predictions to show that internal CO₂ diffusion limitations within CAM leaves increase ¹³C discrimination during nighttime CO₂ fixation while reducing ¹³C during phase IV. When evaluating the phylogenetic distribution of CAM, carbon isotope composition will reflect these diffusive limitations as well as relative contributions from C₃ and C₄ biochemistry.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Howard Griffiths (hg230{at}cam.ac.uk).

www.plantphysiol.org/cgi/doi/10.1104/pp.106.088302

^* Corresponding author; e-mail hg230{at}cam.ac.uk; fax 44–1223–333953.

Received August 14, 2006; accepted November 8, 2006; published December 1, 2006.

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