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Potent Inhibition of Ribulose-Bisphosphate Carboxylase by an Oxidized Impurity in Ribulose-1,5-Bisphosphate1

Heather J. Kane, Jean-Marc Wilkin2, Archie R. Portis Jr., and T. John Andrews*

Research School of Biological Sciences, Australian National University, P.O. Box 475, Canberra ACT 2601, Australia (H.J.K., J.-M.W., T.J.A.); and Photosynthesis Research Unit, Agricultural Research Service, United States Department of Agriculture, Urbana, Illinois 61801 (A.R.P.)

Oxidation of D-ribulose-1,5-bisphosphate (ribulose-P2) during synthesis and/or storage produces D-glycero-2,3-pentodiulose-1,5-bisphosphate (pentodiulose-P2), a potent slow, tight-binding inhibitor of spinach (Spinacia oleracea L.) ribulose-P2 carboxylase/oxygenase (Rubisco). Differing degrees of contamination with pentodiulose-P2 caused the decline in Rubisco activity seen during Rubisco assay time courses to vary between different preparations of ribulose-P2. With some ribulose-P2 preparations, this compound can be the dominant cause of the decline, far exceeding the significance of the catalytic by-product, D-xylulose-1,5-bisphosphate. Unlike xylulose-1,5-bisphosphate, pentodiulose-P2 did not appear to be a significant by-product of catalysis by wild-type Rubisco at saturating CO2 concentration. It was produced slowly during frozen storage of ribulose-P2, even at low pH, more rapidly in Rubisco assay buffers at room temperature, and particularly rapidly on deliberate oxidation of ribulose-P2 with Cu2+. Its formation was prevented by the exclusion of transition metals and O2. Pentodiulose-P2 was unstable and decayed to a variety of other less-inhibitory compounds, particularly in the presence of some buffers. However, it formed a tight, stable complex with carbamylated spinach Rubisco, which could be isolated by gel filtration, presumably because its structure mimics that of the enediol intermediate of Rubisco catalysis. Rubisco catalyzes the cleavage of pentodiulose-P2 by H2O2, producing P-glycolate.

1   This work was supported by the Australian National University's Centre for Molecular Structure and Function.
2   Present address: Departement de Virologie, Institut Pasteur Bruxelles, 642 rue Engeland, 1180 Bruxelles, Belgium.
*   Corresponding author; e-mail john.andrews{at}anu.edu.au; fax 61-2-6249-5075.

Plant Physiol. (1998) 117: 1059-1069
Copyright Clearance Center:   0032-0889/98/117/1059/11
© 1998 American Society of Plant Physiologists




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