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BIOENERGETICS AND PHOTOSYNTHESIS

Comparative Proteomics of Chloroplast Envelopes from C₃ and C₄ Plants Reveals Specific Adaptations of the Plastid Envelope to C₄ Photosynthesis and Candidate Proteins Required for Maintaining C₄ Metabolite Fluxes^1,[W],[OA]

Institute for Plant Biochemistry, Heinrich-Heine-University, D–40225 Duesseldorf, Germany (A.B., A.P.M.W.); Graduate Program in Genetics, Michigan State University, East Lansing, Michigan 48824 (A.B.); and Department of Biochemistry, Michigan State University, East Lansing, Michigan 48824 (S.H.-B.)

C₄ plants have up to 10-fold higher apparent CO₂ assimilation rates than the most productive C₃ plants. This requires higher fluxes of metabolic intermediates across the chloroplast envelope membranes of C₄ plants in comparison with those of C₃ plants. In particular, the fluxes of metabolites involved in the biochemical inorganic carbon pump of C₄ plants, such as malate, pyruvate, oxaloacetate, and phosphoenolpyruvate, must be considerably higher in C₄ plants because they exceed the apparent rate of photosynthetic CO₂ assimilation, whereas they represent relatively minor fluxes in C₃ plants. While the enzymatic steps involved in the C₄ biochemical inorganic carbon pump have been studied in much detail, little is known about the metabolite transporters in the envelope membranes of C₄ chloroplasts. In this study, we used comparative proteomics of chloroplast envelope membranes from the C₃ plant pea (Pisum sativum) and mesophyll cell chloroplast envelopes from the C₄ plant maize (Zea mays) to analyze the adaptation of the mesophyll cell chloroplast envelope proteome to the requirements of C₄ photosynthesis. We show that C₃- and C₄-type chloroplasts have qualitatively similar but quantitatively very different chloroplast envelope membrane proteomes. In particular, translocators involved in the transport of triosephosphate and phosphoenolpyruvate as well as two outer envelope porins are much more abundant in C₄ plants. Several putative transport proteins have been identified that are highly abundant in C₄ plants but relatively minor in C₃ envelopes. These represent prime candidates for the transport of C₄ photosynthetic intermediates, such as pyruvate, oxaloacetate, and malate.

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: Andreas P.M. Weber (andreas.weber{at}uni-duesseldorf.de).

^[W] The online version of this article contains Web-only data.

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www.plantphysiol.org/cgi/doi/10.1104/pp.108.121012

^* Corresponding author; e-mail andreas.weber{at}uni-duesseldorf.de.

Received April 10, 2008; accepted June 23, 2008; published July 3, 2008.