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

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

doi:10.1038/nplants.2016.178

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

Journal Article · Mon Nov 21 00:00:00 EST 2016 · Nature Plants (Online)

DOI:https://doi.org/10.1038/nplants.2016.178· OSTI ID:1343502

Abraham, Paul E. ^[1];

^[1]; Borland, Anne M. ^[2];

^[3]; Lim, Sung Don ^[4];

^[1]; Engle, Nancy ^[1]; Jones, Piet C. ^[3]; Agh, Ryan ^[1]; Weston, David J. ^[1]; Wullschleger, Stan D. ^[1];

^[1]; Jacobson, Daniel ^[3]; Cushman, John C. ^[4]; Hettich, Robert L. ^[1]; Tuskan, Gerald A. ^[1];

^[1]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Newcastle, Newcastle upon Tyne (United KIngdom)
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
Univ. of Nevada, Reno, NV (United States). Dept. of Biochemistry and Molecular Biology

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1343502

Journal Information:: Nature Plants (Online), Vol. 2, Issue 12; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 102 works

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References (55)

High light-induced switch from C3-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light Grams, T. E. E. Journal of Experimental Botany, Vol. 53, Issue 373 https://doi.org/10.1093/jexbot/53.373.1475	journal	June 2002
Phloem Transport of Fructans in the Crassulacean Acid Metabolism Species Agave deserti Wang, Ning; Nobel, Park S. Plant Physiology, Vol. 116, Issue 2 https://doi.org/10.1104/pp.116.2.709	journal	February 1998
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands Borland, A. M.; Griffiths, H.; Hartwell, J. Journal of Experimental Botany, Vol. 60, Issue 10 https://doi.org/10.1093/jxb/erp118	journal	April 2009
Regulation of malic-acid metabolism in Crassulacean-acid-metabolism plants in the dark and light: In-vivo evidence from 13C-labeling patterns after 13CO2 fixation Osmond, C. B.; Holtum, J. A. M.; O'Leary, M. H. Planta, Vol. 175, Issue 2 https://doi.org/10.1007/BF00392426	journal	August 1988
CYCLIN H;1 Regulates Drought Stress Responses and Blue Light-Induced Stomatal Opening by Inhibiting Reactive Oxygen Species Accumulation in Arabidopsis Zhou, Xiao Feng; Jin, Yin Hua; Yoo, Chan Yul Plant Physiology, Vol. 162, Issue 2 https://doi.org/10.1104/pp.113.215798	journal	May 2013
PYR/PYL/RCAR Abscisic Acid Receptors Regulate K+ and Cl- Channels through Reactive Oxygen Species-Mediated Activation of Ca2+ Channels at the Plasma Membrane of Intact Arabidopsis Guard Cells Wang, Y.; Chen, Z. -H.; Zhang, B. PLANT PHYSIOLOGY, Vol. 163, Issue 2 https://doi.org/10.1104/pp.113.219758	journal	July 2013
The Arabidopsis rcn1-1 Mutation Impairs Dephosphorylation of Phot2, Resulting in Enhanced Blue Light Responses Tseng, Tong-Seung; Briggs, Winslow R. The Plant Cell, Vol. 22, Issue 2 https://doi.org/10.1105/tpc.109.066423	journal	February 2010
CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses Lai, A. G.; Doherty, C. J.; Mueller-Roeber, B. Proceedings of the National Academy of Sciences, Vol. 109, Issue 42 https://doi.org/10.1073/pnas.1209148109	journal	October 2012
Basic Local Alignment Search Tool Altschul, S. Journal of Molecular Biology, Vol. 215, Issue 3 https://doi.org/10.1006/jmbi.1990.9999	journal	October 1990
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis Umezawa, T.; Sugiyama, N.; Mizoguchi, M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 41 https://doi.org/10.1073/pnas.0907095106	journal	September 2009
Water-Soluble Carbohydrates and Fructan Structure Patterns from Agave and Dasylirion Species Mancilla-Margalli, N. Alejandra; López, Mercedes G. Journal of Agricultural and Food Chemistry, Vol. 54, Issue 20 https://doi.org/10.1021/jf060354v	journal	October 2006
Label-free Quantitative Proteomics for the Extremely Thermophilic Bacterium Caldicellulosiruptor obsidiansis Reveal Distinct Abundance Patterns upon Growth on Cellobiose, Crystalline Cellulose, and Switchgrass Lochner, Adriane; Giannone, Richard J.; Keller, Martin Journal of Proteome Research, Vol. 10, Issue 12 https://doi.org/10.1021/pr200536j	journal	December 2011
Elevated CO 2 -Induced Responses in Stomata Require ABA and ABA Signaling Chater, Caspar; Peng, Kai; Movahedi, Mahsa Current Biology, Vol. 25, Issue 20 https://doi.org/10.1016/j.cub.2015.09.013	journal	October 2015
Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves Bartoli, C. G. Journal of Experimental Botany, Vol. 57, Issue 8 https://doi.org/10.1093/jxb/erl005	journal	May 2006
Overexpression of SOS (Salt Overly Sensitive) Genes Increases Salt Tolerance in Transgenic Arabidopsis Yang, Qing; Chen, Zhi-Zhong; Zhou, Xiao-Feng Molecular Plant, Vol. 2, Issue 1 https://doi.org/10.1093/mp/ssn058	journal	January 2009
CAP3: A DNA Sequence Assembly Program Huang, X. Genome Research, Vol. 9, Issue 9 https://doi.org/10.1101/gr.9.9.868	journal	September 1999
A Diel Flux Balance Model Captures Interactions between Light and Dark Metabolism during Day-Night Cycles in C ₃ and Crassulacean Acid Metabolism Leaves Cheung, C. Y. Maurice; Poolman, Mark G.; Fell, David. A. Plant Physiology, Vol. 165, Issue 2 https://doi.org/10.1104/pp.113.234468	journal	March 2014
Engineering crassulacean acid metabolism to improve water-use efficiency Borland, Anne M.; Hartwell, James; Weston, David J. Trends in Plant Science, Vol. 19, Issue 5 https://doi.org/10.1016/j.tplants.2014.01.006	journal	May 2014
Comparison of the water-soluble carbohydrate composition and fructan structures of Agave tequilana plants of different ages Arrizon, Javier; Morel, Sandrine; Gschaedler, Anne Food Chemistry, Vol. 122, Issue 1 https://doi.org/10.1016/j.foodchem.2010.02.028	journal	September 2010
Ascorbate function and associated transport systems in plants Horemans, Nele; H. Foyer, Christine; Potters, Geert Plant Physiology and Biochemistry, Vol. 38, Issue 7-8 https://doi.org/10.1016/S0981-9428(00)00782-8	journal	July 2000
D IVERSITY AND R EGULATION OF P LANT Ca ²⁺ P UMPS : Insights from Expression in Yeast Sze, Heven; Liang, Feng; Hwang, Ildoo Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 51, Issue 1 https://doi.org/10.1146/annurev.arplant.51.1.433	journal	June 2000
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
Photosynthesis, Reorganized West-Eberhard, M. J.; Smith, J. A. C.; Winter, K. Science, Vol. 332, Issue 6027 https://doi.org/10.1126/science.1205336	journal	April 2011
RPT2 Is a Signal Transducer Involved in Phototropic Response and Stomatal Opening by Association with Phototropin 1 in Arabidopsis thaliana Inada, Sayaka; Ohgishi, Maki; Mayama, Tomoko The Plant Cell, Vol. 16, Issue 4 https://doi.org/10.1105/tpc.019901	journal	March 2004
Alteration of Organic Acid Metabolism in Arabidopsis Overexpressing the Maize C ₄ NADP-Malic Enzyme Causes Accelerated Senescence during Extended Darkness Fahnenstich, Holger; Saigo, Mariana; Niessen, Michaela Plant Physiology, Vol. 145, Issue 3 https://doi.org/10.1104/pp.107.104455	journal	September 2007
Gas exchange and metabolite fluctuations in green and yellow bands of variegated leaves of the monocotyledonous CAM species Agave americana Raveh, Eran; Wang, Ning; Nobel, Park S. Physiologia Plantarum, Vol. 103, Issue 1 https://doi.org/10.1034/j.1399-3054.1998.1030112.x	journal	May 1998
Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis Winter, K.; Holtum, J. A. M. Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru063	journal	March 2014
Light quality modulates metabolic synchronization over the diel phases of crassulacean acid metabolism Ceusters, J.; Borland, A. M.; Taybi, T. Journal of Experimental Botany, Vol. 65, Issue 13 https://doi.org/10.1093/jxb/eru185	journal	May 2014
Quantitative shotgun proteomics using a protease with broad specificity and normalized spectral abundance factors Zybailov, Boris L.; Florens, Laurence; Washburn, Michael P. Molecular BioSystems, Vol. 3, Issue 5 https://doi.org/10.1039/b701483j	journal	January 2007
The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance: AtCLCc in chloride homeostasis Jossier, Mathieu; Kroniewicz, Laëtitia; Dalmas, Fabien The Plant Journal, Vol. 64, Issue 4 https://doi.org/10.1111/j.1365-313X.2010.04352.x	journal	October 2010
Guard cell photosynthesis is critical for stomatal turgor production, yet does not directly mediate CO ₂ - and ABA-induced stomatal closing Azoulay-Shemer, Tamar; Palomares, Axxell; Bagheri, Andisheh The Plant Journal, Vol. 83, Issue 4 https://doi.org/10.1111/tpj.12916	journal	July 2015
Informing the improvement and biodesign of crassulacean acid metabolism via system dynamics modelling Borland, Anne M.; Yang, Xiaohan New Phytologist, Vol. 200, Issue 4 https://doi.org/10.1111/nph.12529	journal	November 2013
Reconstruction of protein networks from an atlas of maize seed proteotypes Walley, J. W.; Shen, Z.; Sartor, R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 49 https://doi.org/10.1073/pnas.1319113110	journal	November 2013
Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification Christopher, J. T.; Holtum, Jam. Plant Physiology, Vol. 112, Issue 1 https://doi.org/10.1104/pp.112.1.393	journal	September 1996
Plant blue-light receptors Banerjee, Roopa; Batschauer, Alfred Planta, Vol. 220, Issue 3 https://doi.org/10.1007/s00425-004-1418-z	journal	November 2004
CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences Liu, Chang; Shi, Linchun; Zhu, Yingjie BMC Genomics, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2164-13-715	journal	January 2012
Arabidopsis HT1 kinase controls stomatal movements in response to CO2 Hashimoto, Mimi; Negi, Juntaro; Young, Jared Nature Cell Biology, Vol. 8, Issue 4 https://doi.org/10.1038/ncb1387	journal	March 2006
Ascorbate and Glutathione: The Heart of the Redox Hub Foyer, Christine H.; Noctor, Graham Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.167569	journal	January 2011
Evolution along the crassulacean acid metabolism continuum Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark Functional Plant Biology, Vol. 37, Issue 11 https://doi.org/10.1071/FP10084	journal	January 2010
Leaf Mitochondria Modulate Whole Cell Redox Homeostasis, Set Antioxidant Capacity, and Determine Stress Resistance through Altered Signaling and Diurnal Regulation Dutilleul, Christelle; Garmier, Marie; Noctor, Graham The Plant Cell, Vol. 15, Issue 5 https://doi.org/10.1105/tpc.009464	journal	March 2003
A molecular pathway for CO2 response in Arabidopsis guard cells Tian, Wang; Hou, Congcong; Ren, Zhijie Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7057	journal	January 2015
SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler Luo, Ruibang; Liu, Binghang; Xie, Yinlong GigaScience, Vol. 1, Issue 1 https://doi.org/10.1186/2047-217X-1-18	journal	December 2012
On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoe, and Opuntia Winter, K.; Garcia, M.; Holtum, J. A. M. Journal of Experimental Botany, Vol. 59, Issue 7 https://doi.org/10.1093/jxb/ern080	journal	June 2007
RNA-Seq analysis in MeV Howe, E. A.; Sinha, R.; Schlauch, D. Bioinformatics, Vol. 27, Issue 22 https://doi.org/10.1093/bioinformatics/btr490	journal	October 2011
Regulation of Circadian Clocks by Redox Homeostasis Stangherlin, Alessandra; Reddy, Akhilesh B. Journal of Biological Chemistry, Vol. 288, Issue 37 https://doi.org/10.1074/jbc.R113.457564	journal	July 2013
Synthetic biology as it relates to CAM photosynthesis: challenges and opportunities DePaoli, Henrique C.; Borland, Anne M.; Tuskan, Gerald A. Journal of Experimental Botany, Vol. 65, Issue 13, p. 3381-3393 https://doi.org/10.1093/jxb/eru038	journal	February 2014
Redox rhythm reinforces the circadian clock to gate immune response Zhou, Mian; Wang, Wei; Karapetyan, Sargis Nature, Vol. 523, Issue 7561 https://doi.org/10.1038/nature14449	journal	June 2015
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis Mockler, T. C.; Michael, T. P.; Priest, H. D. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 72, Issue 1 https://doi.org/10.1101/sqb.2007.72.006	journal	January 2007
Molecular Mechanism for Inhibition of a Critical Component in the Arabidopsis thaliana Abscisic Acid Signal Transduction Pathways, SnRK2.6, by Protein Phosphatase ABI1 Xie, Tian; Ren, Ruobing; Zhang, Yuan-yuan Journal of Biological Chemistry, Vol. 287, Issue 1 https://doi.org/10.1074/jbc.M111.313106	journal	November 2011
Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plant species Chia, David W.; Yoder, Tennessee J.; Reiter, Wolf-Dieter Planta, Vol. 211, Issue 5 https://doi.org/10.1007/s004250000345	journal	October 2000
TM4: A Free, Open-Source System for Microarray Data Management and Analysis Saeed, A. I.; Sharov, V.; White, J. BioTechniques, Vol. 34, Issue 2 https://doi.org/10.2144/03342mt01	journal	February 2003
Basic local alignment search tool Altschul, Stephen F.; Gish, Warren; Miller, Webb Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410 https://doi.org/10.1016/S0022-2836(05)80360-2	journal	October 1990
Mesobacillus aurantius sp. nov., isolated from an orange-colored pond near a solar saltern Rai, Anusha; Smita, N.; Shabbir, A. Archives of Microbiology, Vol. 203, Issue 4 https://doi.org/10.1007/s00203-020-02146-w	journal	January 2021
Characterization and functional analysis of phytoene synthase gene family in tobacco Wang, Zhaojun; Zhang, Lin; Dong, Chen BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-020-02816-3	journal	January 2021

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59 BASIC BIOLOGICAL SCIENCES
Photosynthesis
Plant molecular biology

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

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