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Plant Physiol, November 1999, Vol. 121, pp. 889-896

Metabolite Control Overrides Circadian Regulation of Phosphoenolpyruvate Carboxylase Kinase and CO2 Fixation in Crassulacean Acid Metabolism1

Anne M. Borland,* James Hartwell, Gareth I. Jenkins, Malcolm B. Wilkins, and Hugh G. Nimmo

Department of Agricultural and Environmental Science, University of Newcastle, Newcastle upon Tyne NE1 7RU, United Kingdom (A.M.B.); and Plant Molecular Science Group, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom (J.H., G.I.J., M.B.W., H.G.N.)

Phosphoenolpyruvate carboxylase (PEPc) catalyzes the primary fixation of CO2 in Crassulacean acid metabolism plants. Flux through the enzyme is regulated by reversible phosphorylation. PEPc kinase is controlled by changes in the level of its translatable mRNA in response to a circadian rhythm. The physiological significance of changes in the levels of PEPc-kinase-translatable mRNA and the involvement of metabolites in control of the kinase was investigated by subjecting Kalanchoë daigremontiana leaves to anaerobic conditions at night to modulate the magnitude of malate accumulation, or to a rise in temperature at night to increase the efflux of malate from vacuole to cytosol. Changes in CO2 fixation and PEPc kinase activity reflected those in kinase mRNA. The highest rates of CO2 fixation and levels of kinase mRNA were observed in leaves subjected to anaerobic treatment for the first half of the night and then transferred to ambient air. In leaves subjected to anaerobic treatment overnight and transferred to ambient air at the start of the day, PEPc-kinase-translatable mRNA and activity, the phosphorylation state of PEPc, and fixation of atmospheric CO2 were significantly higher than those for control leaves for the first 3 h of the light period. A nighttime temperature increase from 19°C to 27°C led to a rapid reduction in kinase mRNA and activity; however, this was not observed in leaves in which malate accumulation had been prevented by anaerobic treatment. These data are consistent with the hypothesis that a high concentration of malate reduces both kinase mRNA and the accumulation of the kinase itself.

1 Financial support was provided by the Natural Environment Research Council and the Biological and Biotechnological Science Research Council, United Kingdom.

* Corresponding author; e-mail a.m.borland{at}ncl.ac.uk; fax 191-222-5228.

© 1999 American Society of Plant Physiologists


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