Evolution of Photosynthetic Metabolism in Terrestrial Plants

Abstract

Two significant events in the evolution of terrestrial plants are associated with the oxygenation reaction of Rubisco. First, land plants are derived from the evolutionary line of green algae (the Charophytes) that first evolved leaf-type peroxisomes with a high-capacity photorespiratory C2 cycle. Most algae lack or have a limited capacity for photorespiration, and instead excrete excessive levels of photorespiratory metabolites into the external medium. Excretion of photorespiratory intermediates is not an option for terrestrial plants, and an efficient C2 cycle is required to prevent oxygenation products from accumulating to toxic levels. The colonization of land by just the Charophycean line, and its timing, may result from the evolution of novel photorespiratory metabolism to minimize the consequences of RuBP oxygenation. Second, C4 plant evolution likely required atmospheric conditions favoring high rates of photorespiration in C3 plants. During most of the history of land plants, atmospheric CO2 levels were too high to allow for elevated rates of photorespiration. In the past 40 million years, CO2 levels fell low enough such that photorespiration became an important limitation for C3 photosynthesis. Little evidence exists for C4 plants prior to the CO2 decline, but there is sound evidence for C4 photosynthesis beginning 20-30 million years ago. Aridity likely influenced C4 plant evolution by promoting the origin of drought-adapted features in C3 plants such as enlarged bundle sheath cells. These features in turn may have facilitated the development of a photorespiratory CO2 concentrating system, which is considered the first step in the evolution of C4 photosynthesis.