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

Abstract

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

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Figure 1: CAM exhibits rescheduled central metabolism and redox homeostasis relative to C3.
Figure 2: Temporal changes in Agave gene expression across the diel cycle.
Figure 3: Diel gene expression and the rescheduling of stomatal movement-related genes in Agave compared with Arabidopsis.
Figure 4: Temporal changes in protein abundances in Agave across the diel cycle.

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Acknowledgements

This material is based on work supported by the Department of Energy Office of Science Genomic Science Program under award number DE-SC0008834. The authors would like to thank R. Giannone and M.A. Cushman for critical review and clarifying comments on the manuscript. This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility (OLCF) at the Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the US Department of Energy (under contract number DE-AC05-00OR22725).

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X.Y., G.A.T., P.E.A. and R.L.H. contributed to conception and design of the experiment; P.A., H.Y., A.M.B., S.D.L., H.C.D.P., N.E., R.A. and T.T. contributed to the acquisition of data; and P.A., H.Y., A.B., D.J.W., P.C.J., D.J., T.T. and J.C.C. contributed to data analysis and interpretation; P.A., X.Y., G.T. and A.B. drafted the manuscript and all authors critically revised and approved the final version of the manuscript for publication.

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Correspondence to Xiaohan Yang.

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The authors declare no competing financial interests.

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Supplementary Figures 1–8, Supplementary Table Legends 1–17, Supplementary Notes, Supplementary References. (PDF 1380 kb)

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Abraham, P., Yin, H., Borland, A. et al. Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nature Plants 2, 16178 (2016). https://doi.org/10.1038/nplants.2016.178

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