Evolutionary physiology and transcriptomics of crassulacean acid metabolism (CAM) in the Agavoideae (Asparagaceae)
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Crassulacean acid metabolism (CAM) is a mode of photosynthesis found in ~6% of flowering plants and serves as an adaptation to water-limited habitats. CAM plants open their stomata for gas exchange at night, when transpiration rates are lower, and fix CO2 via an alternative pathway. Carbon is stored as organic acids during the night, then decarboxylated during the day behind closed stomata. CAM results in high levels of CO2 around RuBisCO, the primary carbon-fixing enzyme in all green plants, with minimal water loss. Although CAM occurs in at least 35 separate lineages, its evolutionary trajectory from C3 is unknown. Here we explore the evolutionary patterns of CAM across the Agavoideae, a subfamily of species that includes Agave and Yucca. Anatomical observations paired with character evolution show that species of the Agavoideae may have been preadapted to the CAM syndrome, with many C3 species showing CAM-like morphology. Comparative physiology was explored in more detail in a Yucca hybrid system, where a CAM and C3 species hybridized to form a C3-CAM intermediate. The parents and hybrid offspring were characterized for anatomical and physiological traits and show the hybrid is able to convert from C3 carbon fixation to 100% CAM uptake under periods of drought stress. Finally, the hybrid system in Yucca was used to understand the transcriptional regulation of the CAM pathway; despite lacking any CAM anatomy or physiology, the C3 parental species shows similar gene expression patterns as the CAM species, indicating perhaps an ancestral gene expression pattern that enabled the evolution of CAM in a subset of Yucca species.