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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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).

Author information

Affiliations

  1. Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA

    • Paul E. Abraham
    •  & Robert L. Hettich
  2. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA

    • Hengfu Yin
    • , Anne M. Borland
    • , Deborah Weighill
    • , Henrique Cestari De Paoli
    • , Nancy Engle
    • , Piet C. Jones
    • , Ryan Agh
    • , David J. Weston
    • , Timothy Tschaplinski
    • , Daniel Jacobson
    • , Gerald A. Tuskan
    •  & Xiaohan Yang
  3. School of Biology, University of Newcastle, Newcastle upon Tyne NE1 7RU, UK

    • Anne M. Borland
  4. The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville, Tennessee 37996, USA

    • Deborah Weighill
    • , Piet C. Jones
    •  & Daniel Jacobson
  5. Department of Biochemistry and Molecular Biology, University of Nevada, MS330, Reno, Nevada 89557-0330, USA

    • Sung Don Lim
    •  & John C. Cushman
  6. Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, USA

    • Stan D. Wullschleger

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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Xiaohan Yang.

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