An Autoinhibitory Domain Confers Redox Regulation to Maize Glycerate Kinase

Glycerate 3-kinase (GLYK) is the terminal enzyme of the photorespiratory cycle in plants and many cyanobacteria. For several C-4 plants, notably grasses of the NADP-malic enzyme (ME) subtype, redox regulation of GLYK has been reported, but the responsible molecular mechanism is not known. We have analyzed the enzyme from the NADP-ME C-4 plant maize (Zea mays) and found that maize GLYK, in contrast to the enzyme from C-3 plants and a dicotyledonous NADP-ME C-4 plant, harbors a short carboxy-terminal extension. In its oxidized (night) form, a disulfide bridge is formed between the two cysteine residues present in this extra domain, and GLYK activity becomes inhibited. Cleavage of this bond by thioredoxin f produces the fully active thiol form, releasing autoinhibition. Fusion of the maize GLYK redox-regulatory domain to GLYK from C-3 plants confers redox regulation to these otherwise unregulated enzymes. It appears that redox regulation of GLYK could be an exclusive feature of monocotyledonous C-4 plants of the NADP-ME type, in which linear electron transport occurs only in the mesophyll chloroplasts. Hence, we suggest that GLYK, in addition to its function in photorespiration, provides glycerate 3-phosphate for the accelerated production of triose phosphate and its export from the mesophyll. This could facilitate the activation of redox-regulated Calvin cycle enzymes and the buildup of Calvin cycle intermediates in the bundle sheath of these particular C-4 plants during the dark/light transition.