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Title: 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 (WUE) via an inverse (compared to C 3 and C 4 photosynthesis-performing species) day/night pattern of stomatal closure/opening to shift CO 2 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 behavior that underpins CAM. 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 C 3 model plant, Arabidopsis thaliana. A mechanistic finding that emerged is that CAM operates with a diel redox poise that is shifted relative to that in Arabidopsis thaliana. Moreover, we identified 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 how this molecular timekeeping regulates CAM physiology remains unclear. In this paper, we provide new insights into complex post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets together provide a resource to inform efforts tomore » engineer more water-use efficient CAM pathway traits into economically valuable C 3 crops.« less

Authors:
 [1]; ORCiD logo [1];  [2]; ORCiD logo [3];  [4]; ORCiD logo [1];  [1];  [3];  [1];  [1];  [1]; ORCiD logo [1];  [3];  [4];  [1];  [1]; ORCiD logo [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Newcastle, Newcastle upon Tyne (United KIngdom)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States). The Bredesen Center for Interdisciplinary Research and Graduate Education
  4. Univ. of Nevada, Reno, NV (United States). Dept. of Biochemistry and Molecular Biology
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1343502
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Plants
Additional Journal Information:
Journal Volume: 2; Journal Issue: 12; Journal ID: ISSN 2055-0278
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Photosynthesis; Plant molecular biology

Citation Formats

Abraham, Paul E., Yin, Hengfu, Borland, Anne M., Weighill, Deborah, Lim, Sung Don, De Paoli, Henrique Cestari, Engle, Nancy, Jones, Piet C., Agh, Ryan, Weston, David J., Wullschleger, Stan D., Tschaplinski, Timothy, Jacobson, Daniel, Cushman, John C., Hettich, Robert L., Tuskan, Gerald A., and Yang, Xiaohan. Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. United States: N. p., 2016. Web. doi:10.1038/nplants.2016.178.
Abraham, Paul E., Yin, Hengfu, Borland, Anne M., Weighill, Deborah, Lim, Sung Don, De Paoli, Henrique Cestari, Engle, Nancy, Jones, Piet C., Agh, Ryan, Weston, David J., Wullschleger, Stan D., Tschaplinski, Timothy, Jacobson, Daniel, Cushman, John C., Hettich, Robert L., Tuskan, Gerald A., & Yang, Xiaohan. Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. United States. doi:10.1038/nplants.2016.178.
Abraham, Paul E., Yin, Hengfu, Borland, Anne M., Weighill, Deborah, Lim, Sung Don, De Paoli, Henrique Cestari, Engle, Nancy, Jones, Piet C., Agh, Ryan, Weston, David J., Wullschleger, Stan D., Tschaplinski, Timothy, Jacobson, Daniel, Cushman, John C., Hettich, Robert L., Tuskan, Gerald A., and Yang, Xiaohan. Mon . "Transcript, protein and metabolite temporal dynamics in the CAM plant Agave". United States. doi:10.1038/nplants.2016.178. https://www.osti.gov/servlets/purl/1343502.
@article{osti_1343502,
title = {Transcript, protein and metabolite temporal dynamics in the CAM plant Agave},
author = {Abraham, Paul E. and Yin, Hengfu and Borland, Anne M. and Weighill, Deborah and Lim, Sung Don and De Paoli, Henrique Cestari and Engle, Nancy and Jones, Piet C. and Agh, Ryan and Weston, David J. and Wullschleger, Stan D. and Tschaplinski, Timothy and Jacobson, Daniel and Cushman, John C. and Hettich, Robert L. and Tuskan, Gerald A. and Yang, Xiaohan},
abstractNote = {Already a proven mechanism for drought resilience, 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 night, when evapotranspiration rates are low. A systems-level understanding of temporal molecular and metabolic controls is needed to define the cellular behavior that underpins CAM. 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 diel redox poise that is shifted relative to that in Arabidopsis thaliana. Moreover, we identified 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 how this molecular timekeeping regulates CAM physiology remains unclear. In this paper, we provide new insights into complex post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets together provide a resource to inform efforts to engineer more water-use efficient CAM pathway traits into economically valuable C3 crops.},
doi = {10.1038/nplants.2016.178},
journal = {Nature Plants},
number = 12,
volume = 2,
place = {United States},
year = {Mon Nov 21 00:00:00 EST 2016},
month = {Mon Nov 21 00:00:00 EST 2016}
}

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Works referenced in this record:

Synthetic biology as it relates to CAM photosynthesis: challenges and opportunities
journal, February 2014

  • DePaoli, Henrique C.; Borland, Anne M.; Tuskan, Gerald A.
  • Journal of Experimental Botany, Vol. 65, Issue 13, p. 3381-3393
  • DOI: 10.1093/jxb/eru038