Transcript, protein and metabolite temporal dynamics in the CAM plant Agave

Already a proven mechanism for drought sustainability, crassulacean acid metabolism (CAM) is a specialized type of photosynthesis that maximizes water-use efficiency (WUE) via an inverse (compared to C3 and C4 photosynthesis-performing species) day/night pattern of stomatal closure/opening to shift CO2 uptake to the nighttime, when evapotranspiration rates are low. A systems-level understanding spanning temporal molecular and metabolic controls is needed to define the cellular behavior that confers advantages in water-limited conditions. Here, we report high-resolution temporal behaviors of transcript, protein, and metabolite abundances across a CAM diel cycle and, where applicable, compare those observations to the well-established C3 model plant, Arabidopsis thaliana. A mechanistic finding that emerged is that CAM operates with a shifted altered redox poise relative to Arabidopsis thaliana. Moreover, we identify widespread rescheduled expression for genes associated with signal transduction mechanisms that are presented in guard cells to regulate stomatal opening/closing. Controlled production and degradation of transcript and proteins is a timing mechanism by which to regulate cellular function, yet knowledge of how this molecular timekeeping regulates CAM physiology is unknown. Here, we provide new insight into complex, post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets together provide a resource that could inform efforts to engineer traits of the more efficient CAM plant into economically valuable C3 crops.