skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis

Abstract

Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that exploits a temporal CO2 pump with nocturnal CO2 uptake and concentration to reduce photorespiration, improve water-use efficiency (WUE), and optimize the adaptability of plants to hotter and drier climates. Introducing the CAM photosynthetic machinery into C3 (or C4) photosynthesis plants (CAM Biodesign) represents a potentially breakthrough strategy for improving WUE while maintaining high productivity. To optimize the success of CAM Biodesign approaches, the functional analysis of individual C4 metabolism cycle genes is necessary to identify the essential genes for robust CAM pathway introduction. Here, we isolated and analyzed the subcellular localizations of 13 enzymes and regulatory proteins of the C4 metabolism cycle of CAM from the common ice plant in stably transformed Arabidopsis thaliana. Six components of the carboxylation module were analyzed including beta-carbonic anhydrase (McBCA2), phosphoenolpyruvate carboxylase (McPEPC1), phosphoenolpyruvate carboxylase kinase (McPPCK1), NAD-dependent malate dehydrogenase (McNAD-MDH1, McNAD-MDH2), and NADP-dependent malate dehydrogenase (McNADP-MDH1). In addition, seven components of the decarboxylation module were analyzed including NAD-dependent malic enzyme (McNAD-ME1, McNAD-ME2), NADP-dependent malic enzyme (McNADP-ME1, NADP-ME2), pyruvate, orthophosphate dikinase (McPPDK), pyruvate, orthophosphate dikinase-regulatory protein (McPPDK-RP), and phosphoenolpyruvate carboxykinase (McPEPCK). Ectopic overexpression of most C4-metabolism cycle components resulted in increased rosette diameter,more » leaf area, and leaf fresh weight of A. thaliana except for McNADP-MDH1, McPPDK-RP, and McPEPCK. Overexpression of most carboxylation module components resulted in increased stomatal conductance and dawn/dusk titratable acidity (TA) as an indirect measure of organic acid (mainly malate) accumulation in A. thaliana. In contrast, overexpression of the decarboxylating malic enzymes reduced stomatal conductance and TA. This comprehensive study provides fundamental insights into the relative functional contributions of each of the individual components of the core C4-metabolism cycle of CAM and represents a critical first step in laying the foundation for CAM Biodesign.« less

Authors:
; ; ; ;
Publication Date:
Research Org.:
Univ. of Nevada, Reno, NV (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1494212
Alternate Identifier(s):
OSTI ID: 1611161
Grant/Contract Number:  
SC0008834
Resource Type:
Published Article
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Name: Frontiers in Plant Science Journal Volume: 10; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Plant Sciences; crassulacean acid metabolism; CAM biodesign; water-use efficiency; C4 metabolism; ice plant; Mesembryanthemum crystallinum; Arabidopsis thaliana

Citation Formats

Lim, Sung Don, Lee, Sojeong, Choi, Won-Gyu, Yim, Won Cheol, and Cushman, John C. Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis. Switzerland: N. p., 2019. Web. https://doi.org/10.3389/fpls.2019.00101.
Lim, Sung Don, Lee, Sojeong, Choi, Won-Gyu, Yim, Won Cheol, & Cushman, John C. Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis. Switzerland. https://doi.org/10.3389/fpls.2019.00101
Lim, Sung Don, Lee, Sojeong, Choi, Won-Gyu, Yim, Won Cheol, and Cushman, John C. Mon . "Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis". Switzerland. https://doi.org/10.3389/fpls.2019.00101.
@article{osti_1494212,
title = {Laying the Foundation for Crassulacean Acid Metabolism (CAM) Biodesign: Expression of the C4 Metabolism Cycle Genes of CAM in Arabidopsis},
author = {Lim, Sung Don and Lee, Sojeong and Choi, Won-Gyu and Yim, Won Cheol and Cushman, John C.},
abstractNote = {Crassulacean acid metabolism (CAM) is a specialized mode of photosynthesis that exploits a temporal CO2 pump with nocturnal CO2 uptake and concentration to reduce photorespiration, improve water-use efficiency (WUE), and optimize the adaptability of plants to hotter and drier climates. Introducing the CAM photosynthetic machinery into C3 (or C4) photosynthesis plants (CAM Biodesign) represents a potentially breakthrough strategy for improving WUE while maintaining high productivity. To optimize the success of CAM Biodesign approaches, the functional analysis of individual C4 metabolism cycle genes is necessary to identify the essential genes for robust CAM pathway introduction. Here, we isolated and analyzed the subcellular localizations of 13 enzymes and regulatory proteins of the C4 metabolism cycle of CAM from the common ice plant in stably transformed Arabidopsis thaliana. Six components of the carboxylation module were analyzed including beta-carbonic anhydrase (McBCA2), phosphoenolpyruvate carboxylase (McPEPC1), phosphoenolpyruvate carboxylase kinase (McPPCK1), NAD-dependent malate dehydrogenase (McNAD-MDH1, McNAD-MDH2), and NADP-dependent malate dehydrogenase (McNADP-MDH1). In addition, seven components of the decarboxylation module were analyzed including NAD-dependent malic enzyme (McNAD-ME1, McNAD-ME2), NADP-dependent malic enzyme (McNADP-ME1, NADP-ME2), pyruvate, orthophosphate dikinase (McPPDK), pyruvate, orthophosphate dikinase-regulatory protein (McPPDK-RP), and phosphoenolpyruvate carboxykinase (McPEPCK). Ectopic overexpression of most C4-metabolism cycle components resulted in increased rosette diameter, leaf area, and leaf fresh weight of A. thaliana except for McNADP-MDH1, McPPDK-RP, and McPEPCK. Overexpression of most carboxylation module components resulted in increased stomatal conductance and dawn/dusk titratable acidity (TA) as an indirect measure of organic acid (mainly malate) accumulation in A. thaliana. In contrast, overexpression of the decarboxylating malic enzymes reduced stomatal conductance and TA. This comprehensive study provides fundamental insights into the relative functional contributions of each of the individual components of the core C4-metabolism cycle of CAM and represents a critical first step in laying the foundation for CAM Biodesign.},
doi = {10.3389/fpls.2019.00101},
journal = {Frontiers in Plant Science},
number = ,
volume = 10,
place = {Switzerland},
year = {2019},
month = {2}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.3389/fpls.2019.00101

Citation Metrics:
Cited by: 6 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Localization of carbonic anhydrase in crassulacean acid metabolism plants
journal, February 1982


Orchestration of carbohydrate processing for crassulacean acid metabolism
journal, June 2016


Engineering for drought avoidance: expression of maize NADP‐malic enzyme in tobacco results in altered stomatal function
journal, April 2002

  • Laporte, Marianne M.; Shen, Bo; Tarczynski, Mitchell C.
  • Journal of Experimental Botany, Vol. 53, Issue 369
  • DOI: 10.1093/jexbot/53.369.699

Changes in Photosynthetic Carbon Flow in Transgenic Rice Plants That Express C4-Type Phospho enol pyruvate Carboxykinase from Urochloa panicoides
journal, September 2000

  • Suzuki, Shoichi; Murai, Nobuhiko; Burnell, James N.
  • Plant Physiology, Vol. 124, Issue 1
  • DOI: 10.1104/pp.124.1.163

Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
journal, May 2010

  • Trapnell, Cole; Williams, Brian A.; Pertea, Geo
  • Nature Biotechnology, Vol. 28, Issue 5
  • DOI: 10.1038/nbt.1621

Enhanced tolerance to drought in transgenic rice plants overexpressing C4 photosynthesis enzymes
journal, December 2013


Engineered GFP as a vital reporter in plants
journal, March 1996


CO2-concentrating: consequences in crassulacean acid metabolism
journal, November 2002


Constitutive and dark-induced expression of Solanum tuberosum phosphoenolpyruvate carboxylase enhances stomatal opening and photosynthetic performance of Arabidopsis thaliana
journal, October 2011

  • Kebeish, Rashad; Niessen, Markus; Oksaksin, Mehtap
  • Biotechnology and Bioengineering, Vol. 109, Issue 2
  • DOI: 10.1002/bit.23344

Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum
journal, June 1993


Arabidopsis NAD-Malic Enzyme Functions As a Homodimer and Heterodimer and Has a Major Impact on Nocturnal Metabolism
journal, January 2008

  • Tronconi, Marcos A.; Fahnenstich, Holger; Gerrard Weehler, Mariel C.
  • Plant Physiology, Vol. 146, Issue 4
  • DOI: 10.1104/pp.107.114975

Reversibility of the Stress-Induced Development of CAM Photosynthesis in Plants
journal, March 2004


A Diel Flux Balance Model Captures Interactions between Light and Dark Metabolism during Day-Night Cycles in C 3 and Crassulacean Acid Metabolism Leaves
journal, March 2014

  • Cheung, C. Y. Maurice; Poolman, Mark G.; Fell, David. A.
  • Plant Physiology, Vol. 165, Issue 2
  • DOI: 10.1104/pp.113.234468

AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis
journal, April 2013

  • De Angeli, Alexis; Zhang, Jingbo; Meyer, Stefan
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2815

Characterization and expression analysis of genes encoding ? and ? carbonic anhydrases in Arabidopsis
journal, May 2007


Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014


Aberrant chloroplasts in transgenic rice plants expressing a high level of maize NADP-dependent malic enzyme
journal, July 2000


Climate-resilient agroforestry: physiological responses to climate change and engineering of crassulacean acid metabolism (CAM) as a mitigation strategy: CAM engineering in trees
journal, December 2014

  • Borland, Anne M.; Wullschleger, Stan D.; Weston, David J.
  • Plant, Cell & Environment, Vol. 38, Issue 9
  • DOI: 10.1111/pce.12479

A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010


Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis
journal, March 2014

  • Winter, K.; Holtum, J. A. M.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru063

Malate valves to balance cellular energy supply
journal, January 2004


Overexpression of C4‐cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3‐photosynthesis
journal, April 2002

  • Häusler, Rainer E.; Hirsch, Heinz‐Josef; Kreuzaler, Fritz
  • Journal of Experimental Botany, Vol. 53, Issue 369
  • DOI: 10.1093/jexbot/53.369.591

The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world: Tansley review
journal, June 2011


Emerging model systems for functional genomics analysis of Crassulacean acid metabolism
journal, June 2016

  • Hartwell, James; Dever, Louisa V.; Boxall, Susanna F.
  • Current Opinion in Plant Biology, Vol. 31
  • DOI: 10.1016/j.pbi.2016.03.019

Control of stomatal aperture: A renaissance of the old guard
journal, September 2011

  • Araújo, Wagner L.; Fernie, Alisdair R.; Nunes-Nesi, Adriano
  • Plant Signaling & Behavior, Vol. 6, Issue 9
  • DOI: 10.4161/psb.6.9.16425

Characterization of the Plastidic Phosphate Translocators in the Inducible Crassulacean Acid Metabolism Plant Mesembryanthemum crystallinum
journal, July 2013

  • Kore-Eda, Shin; Nozawa, Akira; Okada, Yusuke
  • Bioscience, Biotechnology, and Biochemistry, Vol. 77, Issue 7
  • DOI: 10.1271/bbb.130174

Intracellular Localization of Some Key Enzymes of Crassulacean Acid Metabolism in Sedum praealtum
journal, April 1979

  • Spalding, Martin H.; Schmitt, Mark R.; Ku, S. B.
  • Plant Physiology, Vol. 63, Issue 4
  • DOI: 10.1104/pp.63.4.738

Effects of altered phosphoenolpyruvate carboxylase activities on transgenic C3 plant Solanum tuberosum
journal, December 1996

  • Gehlen, Johanna; Panstruga, Ralph; Smets, Helga
  • Plant Molecular Biology, Vol. 32, Issue 5
  • DOI: 10.1007/BF00020481

Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth
journal, November 2014

  • Dever, Louisa V.; Boxall, Susanna F.; Kneřová, Jana
  • Plant Physiology, Vol. 167, Issue 1
  • DOI: 10.1104/pp.114.251827

Withdrawal from functional Crassulacean acid metabolism (CAM) is accompanied by changes in both gene expression and activity of antioxidative enzymes
journal, October 2018


Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation
journal, November 1993


RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity
journal, February 2015


CO 2 Sensing and CO 2 Regulation of Stomatal Conductance: Advances and Open Questions
journal, January 2016


Proteomic analysis of Mesembryanthemum crystallinum leaf microsomal fractions finds an imbalance in V-ATPase stoichiometry during the salt-induced transition from C3 to CAM
journal, February 2013

  • Cosentino, Cristian; Di Silvestre, Dario; Fischer-Schliebs, Elke
  • Biochemical Journal, Vol. 450, Issue 2
  • DOI: 10.1042/BJ20121087

Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco
journal, June 1994

  • Majeau, Nathalie; Arnoldo, MaryAnne; Coleman, John R.
  • Plant Molecular Biology, Vol. 25, Issue 3
  • DOI: 10.1007/BF00043867

Expression of Maize Phospho enol pyruvate Carboxylase in Transgenic Tobacco : Effects on Biochemistry and Physiology
journal, February 1992

  • Hudspeth, Richard L.; Grula, John W.; Dai, Ziyu
  • Plant Physiology, Vol. 98, Issue 2
  • DOI: 10.1104/pp.98.2.458

Crassulacean acid metabolism-cycling in Euphorbia milii
journal, January 2013


Engineering Cellular Metabolism
journal, March 2016


Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, August 2012

  • Barkla, Bronwyn J.; Vera-Estrella, Rosario; Pantoja, Omar
  • PROTEOMICS, Vol. 12, Issue 18
  • DOI: 10.1002/pmic.201200152

The Ice Plant Cometh: Lessons in Abiotic Stress Tolerance
journal, September 2000

  • Bohnert, Hans J.; Cushman, John C.
  • Journal of Plant Growth Regulation, Vol. 19, Issue 3
  • DOI: 10.1007/s003440000033

Impaired pH Homeostasis in Arabidopsis Lacking the Vacuolar Dicarboxylate Transporter and Analysis of Carboxylic Acid Transport across the Tonoplast
journal, February 2005

  • Hurth, Marco Alois; Suh, Su Jeoung; Kretzschmar, Tobias
  • Plant Physiology, Vol. 137, Issue 3
  • DOI: 10.1104/pp.104.058453

Transcriptional profiles of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum
journal, January 2005

  • Kore-eda, Shin; Noake, Chiyuki; Ohishi, Masahisa
  • Functional Plant Biology, Vol. 32, Issue 5
  • DOI: 10.1071/FP04188

Improved Gateway Binary Vectors: High-Performance Vectors for Creation of Fusion Constructs in Transgenic Analysis of Plants
journal, August 2007

  • Nakagawa, Tsuyoshi; Suzuki, Takamasa; Murata, Satoko
  • Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 8
  • DOI: 10.1271/bbb.70216

Open or Close the Gate – Stomata Action Under the Control of Phytohormones in Drought Stress Conditions
journal, January 2013


Analysis of a C4 maize pyruvate, orthophosphate dikinase expressed in C3 transgenic Arabidopsis plants
journal, October 1997


Analysis of Arabidopsis with Highly Reduced Levels of Malate and Fumarate Sheds Light on the Role of These Organic Acids as Storage Carbon Molecules
journal, January 2010

  • Zell, Martina B.; Fahnenstich, Holger; Maier, Alexandra
  • Plant Physiology, Vol. 152, Issue 3
  • DOI: 10.1104/pp.109.151795

Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands
journal, April 2009

  • Borland, A. M.; Griffiths, H.; Hartwell, J.
  • Journal of Experimental Botany, Vol. 60, Issue 10
  • DOI: 10.1093/jxb/erp118

De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis
journal, July 2013

  • Haas, Brian J.; Papanicolaou, Alexie; Yassour, Moran
  • Nature Protocols, Vol. 8, Issue 8
  • DOI: 10.1038/nprot.2013.084

High Level Expression of C4-Specific NADP-Malic Enzyme in Leaves and Impairment of Photoautotrophic Growth in a C3 Plant, Rice
journal, February 2001

  • Tsuchida, Hiroko; Tamai, Tesshu; Fukayama, Hiroshi
  • Plant and Cell Physiology, Vol. 42, Issue 2
  • DOI: 10.1093/pcp/pce013

The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier
journal, August 2003

  • Emmerlich, V.; Linka, N.; Reinhold, T.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 19
  • DOI: 10.1073/pnas.1832002100

Computational analysis of the productivity potential of CAM
journal, February 2018


Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method
journal, June 2006

  • Zhang, Xiuren; Henriques, Rossana; Lin, Shih-Shun
  • Nature Protocols, Vol. 1, Issue 2
  • DOI: 10.1038/nprot.2006.97

Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase
journal, December 2011

  • Hebbelmann, Inga; Selinski, Jennifer; Wehmeyer, Corinna
  • Journal of Experimental Botany, Vol. 63, Issue 3
  • DOI: 10.1093/jxb/err386

The Cytoplasmic Carbonic Anhydrases β CA2 and β CA4 Are Required for Optimal Plant Growth at Low CO 2
journal, March 2016

  • DiMario, Robert J.; Quebedeaux, Jennifer C.; Longstreth, David J.
  • Plant Physiology, Vol. 171, Issue 1
  • DOI: 10.1104/pp.15.01990

Cell organelles from crassulacean acid metabolism (CAM) plants: II. Compartmentation of enzymes of the crassulacean acid metabolism
journal, February 1980

  • Schnarrenberger, C.; Gro�, D.; Burkhard, Ch.
  • Planta, Vol. 147, Issue 5
  • DOI: 10.1007/BF00380191

An improved RNA isolation method for succulent plant species rich in polyphenols and polysaccharides
journal, December 2000

  • Gehrig, H. H.; Winter, K.; Cushman, J.
  • Plant Molecular Biology Reporter, Vol. 18, Issue 4
  • DOI: 10.1007/Bf02825065

Alteration of Organic Acid Metabolism in Arabidopsis Overexpressing the Maize C 4 NADP-Malic Enzyme Causes Accelerated Senescence during Extended Darkness
journal, September 2007

  • Fahnenstich, Holger; Saigo, Mariana; Niessen, Michaela
  • Plant Physiology, Vol. 145, Issue 3
  • DOI: 10.1104/pp.107.104455

A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world
journal, July 2015

  • Yang, Xiaohan; Cushman, John C.; Borland, Anne M.
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13393

Cloning and sequence analysis of cDNAs encoding plant cytosolic malate dehydrogenase
journal, October 1997


Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia
journal, February 2014

  • Barrera Zambrano, V. A.; Lawson, T.; Olmos, E.
  • Journal of Experimental Botany, Vol. 65, Issue 13
  • DOI: 10.1093/jxb/eru022

Enhanced Photosynthetic Performance and Growth as a Consequence of Decreasing Mitochondrial Malate Dehydrogenase Activity in Transgenic Tomato Plants
journal, January 2005

  • Nunes-Nesi, Adriano; Carrari, Fernando; Lytovchenko, Anna
  • Plant Physiology, Vol. 137, Issue 2
  • DOI: 10.1104/pp.104.055566

SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads
journal, February 2014


Age-dependent induction of pyruvate, orthophosphate dikinase in Mesembryanthemum crystallinum L.
journal, June 1995

  • Fi�lthaler, Beate; Meyer, Gabriele; Bohnert, HansJ.
  • Planta, Vol. 196, Issue 3
  • DOI: 10.1007/BF00203649

Impaired Malate and Fumarate Accumulation Due to the Mutation of the Tonoplast Dicarboxylate Transporter Has Little Effects on Stomatal Behavior
journal, September 2017

  • Medeiros, David B.; Barros, Kallyne A.; Barros, Jessica Aline S.
  • Plant Physiology, Vol. 175, Issue 3
  • DOI: 10.1104/pp.17.00971

Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification
journal, September 1996


Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum
journal, May 2015

  • Oh, Dong-Ha; Barkla, Bronwyn J.; Vera-Estrella, Rosario
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13414

The influence of plant pyruvate, orthophosphate dikinase on a C3 plant with respect to the intracellular location of the enzyme
journal, August 1998


A Vitis vinifera basic helix-loop-helix transcription factor enhances plant cell size, vegetative biomass and reproductive yield
journal, April 2018

  • Lim, Sung Don; Yim, Won Choel; Liu, Degao
  • Plant Biotechnology Journal, Vol. 16, Issue 9
  • DOI: 10.1111/pbi.12898

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

Transgenic approaches to manipulate the environmental responses of the C3 carbon fixation cycle
journal, March 2006


Leaf inner structure and immunogold localization of some key enzymes involved in carbon metabolism in CAM plants
journal, December 1998


Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM)
journal, March 2008

  • Cushman, John C.; Tillett, Richard L.; Wood, Joshua A.
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/ern008

The Arabidopsis vacuolar malate channel is a member of the ALMT family
journal, December 2007


Mitochondrial Malate Dehydrogenase Lowers Leaf Respiration and Alters Photorespiration and Plant Growth in Arabidopsis
journal, September 2010

  • Tomaz, Tiago; Bagard, Matthieu; Pracharoenwattana, Itsara
  • Plant Physiology, Vol. 154, Issue 3
  • DOI: 10.1104/pp.110.161612

Elevated pyruvate,orthophosphate dikinase (PPDK) activity alters carbon metabolism in C3 transgenic potatoes with a C4 maize PPDK gene
journal, July 1998


PEPCase Transcript Levels in Mesembryanthemum crystallinum Decline Rapidly upon Relief from Salt Stress
journal, April 1988

  • Vernon, Daniel M.; Ostrem, James A.; Schmitt, Juergen M.
  • Plant Physiology, Vol. 86, Issue 4
  • DOI: 10.1104/pp.86.4.1002

Induction of a Crassulacean Acid-like Metabolism in the C4 Succulent Plant, Portulaca oleracea L.: Study of Enzymes Involved in Carbon Fixation and Carbohydrate Metabolism
journal, May 2004

  • Lara, María V.; Drincovich, María F.; Andreo, Carlos S.
  • Plant and Cell Physiology, Vol. 45, Issue 5
  • DOI: 10.1093/pcp/pch073

An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants
journal, October 2002


    Works referencing / citing this record:

    Undervalued potential of crassulacean acid metabolism for current and future agricultural production
    journal, June 2019

    • Davis, Sarah C.; Simpson, June; Gil-Vega, Katia del Carmen
    • Journal of Experimental Botany, Vol. 70, Issue 22
    • DOI: 10.1093/jxb/erz223