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Some like it hot: the physiological ecology of C4 plant evolution

Sage, Rowan F., Monson, Russell K., Ehleringer, James R., Adachi, Shunsuke, Pearcy, Robert W.
Oecologia 2018 v.187 no.4 pp. 941-966
C3 plants, C4 photosynthesis, C4 plants, ammonia, carbon, carbon dioxide, ecophysiology, fossils, habitats, mesophyll, photorespiration, phylogeny, ribulose-bisphosphate carboxylase, selection pressure, temperature
The evolution of C₄ 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 CO₂ within the sheath cells, allowing it to be efficiently refixed by sheath Rubisco. A modest C₄ biochemical cycle is then upregulated, possibly to support the refixation of photorespired ammonia in sheath cells, with subsequent increases in C₄ metabolism providing incremental benefits until an optimized C₄ pathway is established. ‘Why’ C₄ photosynthesis evolved is largely explained by ancestral C₃ species exploiting photorespiratory CO₂ to improve carbon gain and thus enhance fitness. While photorespiration depresses C₃ performance, it produces a resource (photorespired CO₂) that can be exploited to build an evolutionary bridge to C₄ photosynthesis. ‘Where’ C₄ evolved is indicated by the habitat of species branching near C₃-to-C₄ transitions on phylogenetic trees. Consistent with the photorespiratory bridge hypothesis, transitional species show that the large majority of > 60 C₄ lineages arose in hot, dry, and/or saline regions where photorespiratory potential is high. ‘When’ C₄ evolved has been clarified by molecular clock analyses using phylogenetic data, coupled with isotopic signatures from fossils. Nearly all C₄ lineages arose after 25 Ma when atmospheric CO₂ levels had fallen to near current values. This reduction in CO₂, 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 C₄ photosynthesis.