Photorespiration - Rubisco's repair crew

The photorespiratory repair pathway (photorespiration in short) was set up from ancient metabolic modules about three billion years ago in cyanobacteria, the later ancestors of chloroplasts. These prokaryotes developed the capacity for oxygenic photosynthesis, i.e. the use of water as a source of electrons and protons (with O₂ as a by-product) for the sunlight-driven synthesis of ATP and NADPH for CO₂ fixation in the Calvin cycle. However, the CO₂-binding enzyme, ribulose 1,5-bisphosphate carboxylase (known under the acronym Rubisco), is not absolutely selective for CO₂ and can also use O₂ in a side reaction. It then produces 2-phosphoglycolate (2PG), the accumulation of which would inhibit and potentially stop the Calvin cycle and subsequently photosynthetic electron transport. Photorespiration removes the 2-PG and in this way prevents oxygenic photosynthesis from poisoning itself. In plants, the core of photorespiration consists of ten enzymes distributed over three different types of organelles, requiring interorganellar transport and interaction with several auxiliary enzymes. It goes together with the release and to some extent loss of freshly fixed CO₂. This disadvantageous feature can be suppressed by CO₂-concentrating mechanisms, such as those that evolved in C₄ plants thirty million years ago, which enhance CO₂ fixation and reduce 2PG synthesis. Photorespiration itself provided a pioneer variant of such mechanisms in the predecessors of C₄ plants, C₃-C₄ intermediate plants. This article is a review and update particularly on the enzyme components of plant photorespiration and their catalytic mechanisms, on the interaction of photorespiration with other metabolism and on its impact on the evolution of photosynthesis. This focus was chosen because a better knowledge of the enzymes involved and how they are embedded in overall plant metabolism can facilitate the targeted use of the now highly advanced methods of metabolic network modelling and flux analysis. Understanding photorespiration more than before as a process that enables, rather than reduces, plant photosynthesis, will help develop rational strategies for crop improvement.