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Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms

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Abstract

Regulation of the Calvin–Benson cycle under varying light/dark conditions is a common property of oxygenic photosynthetic organisms and photosynthetic glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is one of the targets of this complex regulatory system. In cyanobacteria and most algae, photosynthetic GAPDH is a homotetramer of GapA subunits which do not contain regulatory domains. In these organisms, dark-inhibition of the Calvin–Benson cycle involves the formation of a kinetically inhibited supramolecular complex between GAPDH, the regulatory peptide CP12 and phosphoribulokinase. Conditions prevailing in the dark, i.e. oxidation of thioredoxins and low NADP(H)/NAD(H) ratio promote aggregation. Although this regulatory system has been inherited in higher plants, these phototrophs contain in addition a second type of GAPDH subunits (GapB) resulting from the fusion of GapA with the C-terminal half of CP12. Heterotetrameric A2B2-GAPDH constitutes the major photosynthetic GAPDH isoform of higher plants chloroplasts and coexists with CP12 and A4-GAPDH. GapB subunits of A2B2-GAPDH have inherited from CP12 a regulatory domain (CTE for C-terminal extension) which makes the enzyme sensitive to thioredoxins and pyridine nucleotides, resembling the GAPDH/CP12/PRK system. The two systems are similar in other respects: oxidizing conditions and low NADP(H)/NAD(H) ratios promote aggregation of A2B2-GAPDH into strongly inactivated A8B8-GAPDH hexadecamers, and both CP12 and CTE specifically affect the NADPH-dependent activity of GAPDH. The alternative, lower activity with NADH is always unaffected. Based on the crystal structure of spinach A4-GAPDH and the analysis of site-specific mutants, a model of the autonomous (CP12-independent) regulatory mechanism of A2B2-GAPDH is proposed. Both CP12 and CTE seem to regulate different photosynthetic GAPDH isoforms according to a common and ancient molecular mechanism.

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Abbreviations

BPGA:

1,3-bisphosphoglycerate

CTE:

C-terminal extension of subunits GapB

GapA and GapB:

subunits A and B, respectively, of photosynthetic glyceraldehyde-3-phosphate dehydrogenase

GAPDH:

glyceraldehyde-3-phosphate dehydrogenase

NADP-MDH:

NADP-dependent malate dehydrogenase

PRK:

phosphoribulokinase

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Acknowledgements

Work in the laboratory of the authors has been supported by the Italian Ministry of University (grants FIRB 2004 and PRIN 2005).

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Authors and Affiliations

  1. Laboratory of Molecular Plant Physiology, Department of Evolutionary Experimental Biology, University of Bologna, Via Irnerio 42, Bologna, 40126, Italy

    P. Trost, L. Marri, M. Zaffagnini, S. Scagliarini, P. Pupillo & F. Sparla

  2. Department of Chemistry “G. Ciamician”, University of Bologna, Bologna, Italy

    S. Fermani & G. Falini

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  1. P. Trost
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  2. S. Fermani
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Trost, P., Fermani, S., Marri, L. et al. Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms. Photosynth Res 89, 263–275 (2006). https://doi.org/10.1007/s11120-006-9099-z

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