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Chapter 6 Photorespiration: The Bridge to C4 Photosynthesis

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C4 Photosynthesis and Related CO2 Concentrating Mechanisms

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 32))

Summary

Photorespiration is one of the major highways of carbon metabolism in C3 plants and hence in the biogeosphere. By mass flow, excelled only by photosynthesis, it actually constitutes the second-most important process in the land-based biosphere. The underlying biochemical pathway, the photorespiratory carbon oxidation or C2 cycle, compensates for the oxygenation of ribulose 1,5-bisphosphate by serving as a carbon-recovery system reconverting 2-phosphoglycolate to 3-phosphoglycerate. While this ancient ancillary metabolic process enables C3 plants to thrive in an oxygen-containing environment, it also sacrifices a significant part of the freshly assimilated carbon to the atmosphere. Biochemically, this sacrifice is made by the decarboxylation of the C2 cycle intermediate Gly.

C3 plants lose much photorespiratory CO2 to the atmosphere. In contrast, photorespiration is very low in C4 plants. C3-C4 intermediate plants, the phylogenetic predecessors of C4 plants, use Gly as a vehicle to transport freshly assimilated carbon from the mesophyll to the bundle sheath where it is released as photorespiratory CO2. Possibly, this extra CO2 supply was a pacemaker for the subsequent substantial accumulation of chloroplasts in the bundle sheath cells of C3-C4 plants. Eventually, this photorespiration-driven CO2 pump was first superimposed and then replaced by the C4 cycle, another auxiliary pathway to the Calvin cycle, which creates even more favorable photosynthetic conditions within the bundle sheath. It thus appears as if photorespiration triggered C4 plant evolution not only indirectly by exerting selective pressure in favor of low-photorespiration carbon assimilation, but primarily by providing the first strategy on how to improve the intercellular CO2 distribution in leaves.

This chapter will review molecular aspects of photorespiration and introduce some measurement techniques. It will then briefly describe current knowledge about C3-C4 photosynthesis and discuss the workings of a photorespiration-driven CO2 concentration mechanism as one of the first steps in the evolution of C4 photosynthesis.

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Abbreviations

BSC:

Bundle sheath cells;

CAT:

Catalase;

CCM:

CO2-concentrating mechanism;

GGT:

Glu:glyoxylate aminotransferase;

GS:

Gln synthetase;

GOGAT:

Gln:2-oxoglutarate amidotransferase (Glu synthase);

GDC:

Gly decarboxylase;

GLYK:

Glycerate 3-kinase;

3PGA:

Glycerate 3-phosphate;

GOX:

Glycolate oxidase;

2PG:

Glycolate 2-phosphate;

PGLP:

Glycolate 2-phosphate phosphatase;

3HP:

Hydroxypyruvate;

IRGA:

Infrared gas analyzer;

MC:

Mesophyll cell;

HPR1:

NADH-dependent hydroxypyruvate reductase;

HPR2:

NADPH-dependent hydroxypyruvate reductase;

2OG:

2-Oxoglutarate;

PIB:

Post-illumination CO2 burst;

RubP:

Ribulose 1,5-bisphosphate;

Rubisco:

RubP carboxylase/oxygenase;

SHMT:

Ser hydroxymethyltransferase;

SGT (AGT):

Ser:glyoxylate aminotransferase;

S:

Specificity factor of Rubisco;

THF:

Tetrahydrofolate

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Acknowledgments

My apologies to the many authors whose research was not specifically mentioned owing to space constraints. Special thanks to two anonymous reviewers who helped to improve this article. Part of this manuscript was prepared during a visit to the Murray Badger laboratory at the Australian National University, Canberra, which was generously supported by the Plant Energy Biology ARC Center of Excellence. Our own research received much financial support from the Deutsche Forschungsgemeinschaft.

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Bauwe, H. (2010). Chapter 6 Photorespiration: The Bridge to C4 Photosynthesis. In: Raghavendra, A., Sage, R. (eds) C4 Photosynthesis and Related CO2 Concentrating Mechanisms. Advances in Photosynthesis and Respiration, vol 32. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9407-0_6

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