Chapter 6 Photorespiration: The Bridge to C4 Photosynthesis

Abstract

Photorespiration is one of the major highways of carbon metabolism in C-3 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 C-2 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 C-3 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 C-2 cycle intermediate Gly. C-3 plants lose much photorespiratory CO2 to the atmosphere. In contrast, photorespiration is very low in C-4 plants. C-3-C-4 intermediate plants, the phylogenetic predecessors of C-4 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 C-3-C-4 plants. Eventually, this photorespiration-driven CO2 pump was first superimposed and then replaced by the C-4 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 C-4 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 C-3-C-4 photosynthesis and discuss the workings of a photorespiration-driven CO2 concentration mechanism as one of the first steps in the evolution of C-4 photosynthesis.