Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

Summary The photorespiratory pathway, in short photorespiration, is a metabolic repair system that enables the CO2 fixation enzyme Rubisco to sustainably operate in the presence of oxygen, that is, during oxygenic photosynthesis of plants and cyanobacteria. Photorespiration is necessary because an auto‐inhibitory metabolite, 2‐phosphoglycolate (2PG), is produced when Rubisco binds oxygen instead of CO2 as a substrate and must be removed, to avoid collapse of metabolism, and recycled as efficiently as possible. The basic principle of recycling 2PG very likely evolved several billion years ago in connection with the evolution of oxyphotobacteria. It comprises the multi‐step combination of two molecules of 2PG to form 3‐phosphoglycerate. The biochemistry of this process dictates that one out of four 2PG carbons is lost as CO2, which is a long‐standing plant breeders' concern because it represents by far the largest fraction of respiratory processes that reduce gross‐photosynthesis of major crops down to about 50% and less, lowering potential yields. In addition to the ATP needed for recycling of the 2PG carbon, extra energy is needed for the refixation of liberated equal amounts of ammonia. It is thought that the energy costs of photorespiration have an additional negative impact on crop yields in at least some environments. This paper discusses recent advances concerning the origin and evolution of photorespiration, and gives an overview of contemporary and envisioned strategies to engineer the biochemistry of, or even avoid, photorespiration. Significance Statement This paper discusses recent advances concerning the function, origin and evolution of photorespiration, and gives a critical overview of contemporary and envisioned strategies to engineer the biochemistry of, or even avoid, photorespiration.