Some Like It Hot: the Physiological Ecology of C Plant Evolution

The evolution of C photosynthesis requires an intermediate phase where photorespiratory glycine produced in the mesophyll cells must flow to the vascular sheath cells for metabolism by glycine decarboxylase. This glycine flux concentrates photorespired CO within the sheath cells, allowing it to be efficiently refixed by sheath Rubisco. A modest C biochemical cycle is then upregulated, possibly to support the refixation of photorespired ammonia in sheath cells, with subsequent increases in C metabolism providing incremental benefits until an optimized C pathway is established. 'Why' C photosynthesis evolved is largely explained by ancestral C species exploiting photorespiratory CO to improve carbon gain and thus enhance fitness. While photorespiration depresses C performance, it produces a resource (photorespired CO) that can be exploited to build an evolutionary bridge to C photosynthesis. 'Where' C evolved is indicated by the habitat of species branching near C-to-C transitions on phylogenetic trees. Consistent with the photorespiratory bridge hypothesis, transitional species show that the large majority of > 60 C lineages arose in hot, dry, and/or saline regions where photorespiratory potential is high. 'When' C evolved has been clarified by molecular clock analyses using phylogenetic data, coupled with isotopic signatures from fossils. Nearly all C lineages arose after 25 Ma when atmospheric CO levels had fallen to near current values. This reduction in CO, coupled with persistent high temperature at low-to-mid-latitudes, met a precondition where photorespiration was elevated, thus facilitating the evolutionary selection pressure that led to C photosynthesis.