Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth
Abstract
Here, mitochondrial NAD-malic enzyme (ME) and/or cytosolic/plastidic NADP-ME combined with the cytosolic/plastidic pyruvate orthophosphate dikinase (PPDK) catalyze two key steps during light-period malate decarboxylation that underpin secondary CO2 fixation in some Crassulacean acid metabolism (CAM) species. We report the generation and phenotypic characterization of transgenic RNA interference lines of the obligate CAM species Kalanchoë fedtschenkoi with reduced activities of NAD-ME or PPDK. Transgenic line rNAD-ME1 had 8%, and rPPDK1 had 5% of the wild-type level of activity, and showed dramatic changes in the light/dark cycle of CAM CO2 fixation. In well-watered conditions, these lines fixed all of their CO2 in the light; they thus performed C3 photosynthesis. The alternative malate decarboxylase, NADP-ME, did not appear to compensate for the reduction in NAD-ME, suggesting that NAD-ME was the key decarboxylase for CAM. The activity of other CAM enzymes was reduced as a consequence of knocking out either NAD-ME or PPDK activity, particularly phosphoenolpyruvate carboxylase (PPC) and PPDK in rNAD-ME1. Furthermore, the circadian clock-controlled phosphorylation of PPC in the dark was reduced in both lines, especially in rNAD-ME1. This had the consequence that circadian rhythms of PPC phosphorylation, PPC kinase transcript levels and activity, and the classic circadian rhythm of CAM CO2more »
- Authors:
-
[1]
- Univ. of Liverpool, Liverpool (United Kingdom)
- Univ. of Liverpool, Liverpool (United Kingdom); Univ. of Cambridge, Cambridge (United Kingdom)
- Publication Date:
- Research Org.:
- Univ. of Nevada, Reno, NV (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1455174
- Grant/Contract Number:
- SC0008834
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Plant Physiology (Bethesda)
- Additional Journal Information:
- Journal Name: Plant Physiology (Bethesda); Journal Volume: 167; Journal Issue: 1; Journal ID: ISSN 0032-0889
- Publisher:
- American Society of Plant Biologists
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Dever, Louisa V., Boxall, Susanna F., Knerova, Jana, and Hartwell, James. Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth. United States: N. p., 2014.
Web. doi:10.1104/pp.114.251827.
Dever, Louisa V., Boxall, Susanna F., Knerova, Jana, & Hartwell, James. Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth. United States. https://doi.org/10.1104/pp.114.251827
Dever, Louisa V., Boxall, Susanna F., Knerova, Jana, and Hartwell, James. Wed .
"Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth". United States. https://doi.org/10.1104/pp.114.251827. https://www.osti.gov/servlets/purl/1455174.
@article{osti_1455174,
title = {Transgenic Perturbation of the Decarboxylation Phase of Crassulacean Acid Metabolism Alters Physiology and Metabolism But Has Only a Small Effect on Growth},
author = {Dever, Louisa V. and Boxall, Susanna F. and Knerova, Jana and Hartwell, James},
abstractNote = {Here, mitochondrial NAD-malic enzyme (ME) and/or cytosolic/plastidic NADP-ME combined with the cytosolic/plastidic pyruvate orthophosphate dikinase (PPDK) catalyze two key steps during light-period malate decarboxylation that underpin secondary CO2 fixation in some Crassulacean acid metabolism (CAM) species. We report the generation and phenotypic characterization of transgenic RNA interference lines of the obligate CAM species Kalanchoë fedtschenkoi with reduced activities of NAD-ME or PPDK. Transgenic line rNAD-ME1 had 8%, and rPPDK1 had 5% of the wild-type level of activity, and showed dramatic changes in the light/dark cycle of CAM CO2 fixation. In well-watered conditions, these lines fixed all of their CO2 in the light; they thus performed C3 photosynthesis. The alternative malate decarboxylase, NADP-ME, did not appear to compensate for the reduction in NAD-ME, suggesting that NAD-ME was the key decarboxylase for CAM. The activity of other CAM enzymes was reduced as a consequence of knocking out either NAD-ME or PPDK activity, particularly phosphoenolpyruvate carboxylase (PPC) and PPDK in rNAD-ME1. Furthermore, the circadian clock-controlled phosphorylation of PPC in the dark was reduced in both lines, especially in rNAD-ME1. This had the consequence that circadian rhythms of PPC phosphorylation, PPC kinase transcript levels and activity, and the classic circadian rhythm of CAM CO2 fixation were lost, or dampened toward arrhythmia, under constant light and temperature conditions. Surprisingly, oscillations in the transcript abundance of core circadian clock genes also became arrhythmic in the rNAD-ME1 line, suggesting that perturbing CAM in K. fedtschenkoi feeds back to perturb the central circadian clock.},
doi = {10.1104/pp.114.251827},
journal = {Plant Physiology (Bethesda)},
number = 1,
volume = 167,
place = {United States},
year = {Wed Nov 05 00:00:00 EST 2014},
month = {Wed Nov 05 00:00:00 EST 2014}
}
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Works referenced in this record:
Period and phase control by temperature in the circadian rhythm of carbon dioxide fixation in illuminated leaves of Bryophyllum fedtschenkoi
journal, April 1989
- Anderson, Clare M.; Wilkins, Malcolm B.
- Planta, Vol. 177, Issue 4
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
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
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
Engineering crassulacean acid metabolism to improve water-use efficiency
journal, May 2014
- Borland, Anne M.; Hartwell, James; Weston, David J.
- Trends in Plant Science, Vol. 19, Issue 5
Metabolite Control Overrides Circadian Regulation of Phospho enol pyruvate Carboxylase Kinase and CO 2 Fixation in Crassulacean Acid Metabolism
journal, November 1999
- Borland, Anne M.; Hartwell, James; Jenkins, Gareth I.
- Plant Physiology, Vol. 121, Issue 3
Conservation and Divergence of Circadian Clock Operation in a Stress-Inducible Crassulacean Acid Metabolism Species Reveals Clock Compensation against Stress
journal, February 2005
- Boxall, Susanna F.; Foster, Jonathan M.; Bohnert, Hans J.
- Plant Physiology, Vol. 137, Issue 3
C 4 acid decarboxylases required for C 4 photosynthesis are active in the mid-vein of the C 3 species Arabidopsis thaliana , and are important in sugar and amino acid metabolism
journal, January 2010
- Brown, Naomi J.; Palmer, Ben G.; Stanley, Susan
- The Plant Journal, Vol. 61, Issue 1
Cloning and expression of maize-leaf pyruvate, Pi dikinase regulatory protein gene
journal, June 2006
- Burnell, Jim N.; Chastain, Chris J.
- Biochemical and Biophysical Research Communications, Vol. 345, Issue 2
Circadian rhythms in the activity of a plant protein kinase.
journal, August 1991
- Carter, P. J.; Nimmo, H. G.; Fewson, C. A.
- The EMBO Journal, Vol. 10, Issue 8
Further Analysis of Maize C4 Pyruvate,Orthophosphate Dikinase Phosphorylation by Its Bifunctional Regulatory Protein Using Selective Substitutions of the Regulatory Thr-456 and Catalytic His-458 Residues
journal, March 2000
- Chastain, Chris J.; Botschner, Montgomery; Harrington, Grant E.
- Archives of Biochemistry and Biophysics, Vol. 375, Issue 1
Regulation of pyruvate, orthophosphate dikinase by ADP-/Pi-dependent reversible phosphorylation in C3 and C4 plants
journal, June 2003
- Chastain, Chris J.; Chollet, Raymond
- Plant Physiology and Biochemistry, Vol. 41, Issue 6-7
Pyruvate,Orthophosphate Dikinase in Leaves and Chloroplasts of C 3 Plants Undergoes Light-/Dark-Induced Reversible Phosphorylation
journal, February 2002
- Chastain, Chris J.; Fries, Jason P.; Vogel, Julie A.
- Plant Physiology, Vol. 128, Issue 4
Posttranslational Modification of Maize Chloroplast Pyruvate Orthophosphate Dikinase Reveals the Precise Regulatory Mechanism of Its Enzymatic Activity
journal, April 2014
- Chen, Yi-Bo; Lu, Tian-Cong; Wang, Hong-Xia
- Plant Physiology, Vol. 165, Issue 2
Shared origins of a key enzyme during the evolution of C4 and CAM metabolism
journal, March 2014
- Christin, Pascal-Antoine; Arakaki, Monica; Osborne, Colin P.
- Journal of Experimental Botany, Vol. 65, Issue 13
Protective Mechanism of the Mexican Bean Weevil against High Levels of [alpha]-Amylase Inhibitor in the Common Bean
journal, June 1996
- Ishimoto, M.; Chrispeels, M. J.
- Plant Physiology, Vol. 111, Issue 2
Cloning and Sequence of a cDNA Encoding Phenylalanine Ammonia-Lyase from the Tropical Forage Legume Stylosanthes humilis
journal, July 1995
- Manners, J. M.; McIntyre, C. L.; Nourse, J. P.
- Plant Physiology, Vol. 108, Issue 3
Isolation and Characterization of Mutants of Common Ice Plant Deficient in Crassulacean Acid Metabolism
journal, March 2008
- Cushman, John C.; Agarie, Sakae; Albion, Rebecca L.
- Plant Physiology, Vol. 147, Issue 1
CRASSULACEAN ACID METABOLISM: Molecular Genetics
journal, June 1999
- Cushman, John C.; Bohnert, Hans J.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1
Nicotinamide Adenine Dinucleotide-specific “Malic” Enzyme in Kalanchoë daigremontiana and Other Plants Exhibiting Crassulacean Acid Metabolism
journal, February 1976
- Dittrich, Peter
- Plant Physiology, Vol. 57, Issue 2
Regulation of Phospho enol pyruvate Carboxylase Phosphorylation by Metabolites and Abscisic Acid during the Development and Germination of Barley Seeds
journal, August 2008
- Feria, Ana-Belén; Alvarez, Rosario; Cochereau, Ludivine
- Plant Physiology, Vol. 148, Issue 2
Evolution of asexual reproduction in leaves of the genus Kalanchoe
journal, September 2007
- Garces, H. M. P.; Champagne, C. E. M.; Townsley, B. T.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 39
Isolation and characterisation of a wheat phosphoenolpyruvate carboxylase gene. Modelling of the encoded protein
journal, February 2002
- González, Marı́a-Cruz; Echevarrı́a, Cristina; Vidal, Jean
- Plant Science, Vol. 162, Issue 2
The co-ordination of central plant metabolism by the circadian clock
journal, October 2005
- Hartwell, J.
- Biochemical Society Transactions, Vol. 33, Issue 5
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression
journal, November 1999
- Hartwell, James; Gill, Aideen; Nimmo, Gillian A.
- The Plant Journal, Vol. 20, Issue 3
Higher plant phosphoenolpyruvate carboxylase kinase is regulated at the level of translatable mRNA in response to light or a circadian rhythm
journal, December 1996
- Hartwell, James; Smith, Lucy H.; Wilkins, Malcolm B.
- The Plant Journal, Vol. 10, Issue 6
Determination of NAD Malic Enzyme in Leaves of C 4 Plants: EFFECTS OF MALATE DEHYDROGENASE AND OTHER FACTORS
journal, February 1982
- Hatch, Marshall D.; Tsuzuki, Mikio; Edwards, Gerald E.
- Plant Physiology, Vol. 69, Issue 2
Photosynthetic entrainment of the Arabidopsis thaliana circadian clock
journal, October 2013
- Haydon, Michael J.; Mielczarek, Olga; Robertson, Fiona C.
- Nature, Vol. 502, Issue 7473
Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants
journal, January 2002
- Hibberd, Julian M.; Quick, W. Paul
- Nature, Vol. 415, Issue 6870
Storage of competent cells for Agrobacterium transformation
journal, January 1988
- Hofgen, Rainer; Willmitzer, Lothar
- Nucleic Acids Research, Vol. 16, Issue 20
Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism
journal, January 2005
- Holtum, Joseph A. M.; Smith, J. Andrew C.; Neuhaus, H. Ekkehard
- Functional Plant Biology, Vol. 32, Issue 5
GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002
- Karimi, Mansour; Inzé, Dirk; Depicker, Ann
- Trends in Plant Science, Vol. 7, Issue 5, p. 193-195
Species variation in the intracellular localization of pyruvate, Pi dikinase in leaves of crassulacean-acid-metabolism plants: an immunogold electron-microscope study
journal, March 2000
- Kondo, Ayumu; Nose, Akihiro; Yuasa, Hiroshi
- Planta, Vol. 210, Issue 4
CO2-concentrating: consequences in crassulacean acid metabolism
journal, November 2002
- Luttge, U.
- Journal of Experimental Botany, Vol. 53, Issue 378
Genetic Interactions between Phytochrome A, Phytochrome B, and Cryptochrome 1 during Arabidopsis Development
journal, September 1998
- Neff, Michael M.; Chory, Joanne
- Plant Physiology, Vol. 118, Issue 1
Diurnal changes in the properties of phosphoenolpyruvate carboxylase in Bryophyllum leaves: a possible co valent modification
journal, December 1984
- Nimmo, G. A.; Nimmo, H. G.; Fewson, C. A.
- FEBS Letters, Vol. 178, Issue 2
Purification of the phosphorylated night form and dephosphorylated day form of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi
journal, October 1986
- Nimmo, G. A.; Nimmo, H. G.; Hamilton, I. D.
- Biochemical Journal, Vol. 239, Issue 1
Persistent circadian rhythms in the phosphorylation state of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi leaves and in its sensitivity to inhibition by malate
journal, March 1987
- Nimmo, G. A.; Wilkins, M. B.; Fewson, C. A.
- Planta, Vol. 170, Issue 3
The regulation of phosphoenolpyruvate carboxylase in CAM plants
journal, February 2000
- Nimmo, Hugh G.
- Trends in Plant Science, Vol. 5, Issue 2
Crassulacean Acid Metabolism: A Curiosity in Context
journal, June 1978
- Osmond, C. B.
- Annual Review of Plant Physiology, Vol. 29, Issue 1
Regulatory phosphorylation of C4 phosphoenolpyruvate carboxylase from Sorghum: An immunological study using specific anti-phosphorylation site-antibodies
journal, March 1995
- Pacquit, Val�rie; Giglioli, Nathalie; Cr�tin, Claude
- Photosynthesis Research, Vol. 43, Issue 3
The Arabidopsis PPDK gene is transcribed from two promoters to produce differentially expressed transcripts responsible for cytosolic and plastidic proteins
journal, August 2006
- Parsley, Kate; Hibberd, Julian M.
- Plant Molecular Biology, Vol. 62, Issue 3
Pyruvate Pi dikinase activity in different groups of crassulacean acid metabolism plants
journal, May 1982
- Ramachandra Reddy, A.; Das, V. S. R.
- Plant Science Letters, Vol. 25, Issue 2
Evolution along the crassulacean acid metabolism continuum
journal, January 2010
- Silvera, Katia; Neubig, Kurt M.; Whitten, W. Mark
- Functional Plant Biology, Vol. 37, Issue 11
Multiple isoforms of phosphoenolpyruvate carboxylase in the Orchidaceae (subtribe Oncidiinae): implications for the evolution of crassulacean acid metabolism
journal, June 2014
- Silvera, Katia; Winter, Klaus; Rodriguez, B. Leticia
- Journal of Experimental Botany, Vol. 65, Issue 13
Quantification of starch in plant tissues
journal, August 2006
- Smith, Alison M.; Zeeman, Samuel C.
- Nature Protocols, Vol. 1, Issue 3
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
Cloning of the Arabidopsis Clock Gene TOC1, an Autoregulatory Response Regulator Homolog
journal, August 2000
- Strayer, C.
- Science, Vol. 289, Issue 5480
Occurrence of Pyruvate Orthophosphate Dikinase in the Succulent Plant, Kalanchoë daigremontiana Hamet. et. Perr.
journal, November 1975
- Sugiyama, Tatsuo; Laetsch, Watson M.
- Plant Physiology, Vol. 56, Issue 5
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
Immunological analysis of the phosphorylation state of maize C 4 -form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide: Immunological detection of phosphorylated PEPC
journal, January 2000
- Ueno, Yoshihisa; Imanari, Eiji; Emura, Junji
- The Plant Journal, Vol. 21, Issue 1
Stomatal responses to CO 2 during a diel Crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata
journal, May 2009
- Von Caemmerer, Susanne; Griffiths, Howard
- Plant, Cell & Environment, Vol. 32, Issue 5
Partial Purification and Characterization of Phosphoenolpyruvate Carboxylase Protein-Serine Kinase from Illuminated Maize Leaves
journal, August 1993
- Wang, Y. H.; Chollet, R.
- Archives of Biochemistry and Biophysics, Vol. 304, Issue 2
An Endogenous Rhythm in the Rate of Carbon Dioxide Output of Bryophyllum: I. SOME PRELIMINARY EXPERIMENTS
journal, January 1959
- Wilkins, M. B.
- Journal of Experimental Botany, Vol. 10, Issue 3
Tansley Review No. 37 Circadian rhythms: their origin and control
journal, July 1992
- Wilkins, Malcolm B.
- New Phytologist, Vol. 121, Issue 3
On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoe, and Opuntia
journal, June 2007
- Winter, K.; Garcia, M.; Holtum, J. A. M.
- Journal of Experimental Botany, Vol. 59, Issue 7
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
Crassulacean Acid Metabolism: Current Status and Perspectives
book, January 1996
- Winter, K.; Smith, J. A. C.
- Crassulacean Acid Metabolism
Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the Crassulacean acid metabolism plant Kalancho� daigremontiana: testing the tonoplast-as-oscillator model
journal, May 2004
- Wyka, TomaszP.; Bohn, Andreas; Duarte, HeitorM.
- Planta, Vol. 219, Issue 4
Further Analysis of Maize C4 Pyruvate,Orthophosphate Dikinase Phosphorylation by Its Bifunctional Regulatory Protein Using Selective Substitutions of the Regulatory Thr-456 and Catalytic His-458 Residues
journal, March 2000
- Chastain, Chris J.; Botschner, Montgomery; Harrington, Grant E.
- Archives of Biochemistry and Biophysics, Vol. 375, Issue 1
Pyruvate Pi dikinase activity in different groups of crassulacean acid metabolism plants
journal, May 1982
- Ramachandra Reddy, A.; Das, V. S. R.
- Plant Science Letters, Vol. 25, Issue 2
Quantification of starch in plant tissues
journal, August 2006
- Smith, Alison M.; Zeeman, Samuel C.
- Nature Protocols, Vol. 1, Issue 3
Purification of the phosphorylated night form and dephosphorylated day form of phosphoenolpyruvate carboxylase from Bryophyllum fedtschenkoi
journal, October 1986
- Nimmo, G. A.; Nimmo, H. G.; Hamilton, I. D.
- Biochemical Journal, Vol. 239, Issue 1
Probing the circadian control of phosphoenolpyruvate carboxylase kinase expression in Kalanchoë fedtschenkoi
journal, January 2002
- Hartwell, James; Nimmo, Gillian A.; Wilkins, Malcolm B.
- Functional Plant Biology, Vol. 29, Issue 6
An Endogenous Rhythm in the Rate of Carbon Dioxide Output of Bryophyllum: I. SOME PRELIMINARY EXPERIMENTS
journal, January 1959
- Wilkins, M. B.
- Journal of Experimental Botany, Vol. 10, Issue 3
CO2-concentrating: consequences in crassulacean acid metabolism
journal, November 2002
- Luttge, U.
- Journal of Experimental Botany, Vol. 53, Issue 378
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
Multiple isoforms of phosphoenolpyruvate carboxylase in the Orchidaceae (subtribe Oncidiinae): implications for the evolution of crassulacean acid metabolism
journal, June 2014
- Silvera, Katia; Winter, Klaus; Rodriguez, B. Leticia
- Journal of Experimental Botany, Vol. 65, Issue 13
Storage of competent cells for Agrobacterium transformation
journal, January 1988
- Hofgen, Rainer; Willmitzer, Lothar
- Nucleic Acids Research, Vol. 16, Issue 20
Pyruvate,Orthophosphate Dikinase in Leaves and Chloroplasts of C 3 Plants Undergoes Light-/Dark-Induced Reversible Phosphorylation
journal, February 2002
- Chastain, Chris J.; Fries, Jason P.; Vogel, Julie A.
- Plant Physiology, Vol. 128, Issue 4
Conservation and Divergence of Circadian Clock Operation in a Stress-Inducible Crassulacean Acid Metabolism Species Reveals Clock Compensation against Stress
journal, February 2005
- Boxall, Susanna F.; Foster, Jonathan M.; Bohnert, Hans J.
- Plant Physiology, Vol. 137, Issue 3
Regulation of Phospho enol pyruvate Carboxylase Phosphorylation by Metabolites and Abscisic Acid during the Development and Germination of Barley Seeds
journal, August 2008
- Feria, Ana-Belén; Alvarez, Rosario; Cochereau, Ludivine
- Plant Physiology, Vol. 148, Issue 2
Decarboxylation of Malate in the Crassulacean Acid Metabolism Plant Bryophyllum (Kalanchoe) fedtschenkoi (Role of NAD-Malic Enzyme)
journal, December 1995
- Cook, R. M.; Lindsay, J. G.; Wilkins, M. B.
- Plant Physiology, Vol. 109, Issue 4
Patterns of Carbon Partitioning in Leaves of Crassulacean Acid Metabolism Species during Deacidification
journal, September 1996
- Christopher, J. T.; Holtum, Jam.
- Plant Physiology, Vol. 112, Issue 1
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
Occurrence of Pyruvate Orthophosphate Dikinase in the Succulent Plant, Kalanchoë daigremontiana Hamet. et. Perr.
journal, November 1975
- Sugiyama, Tatsuo; Laetsch, Watson M.
- Plant Physiology, Vol. 56, Issue 5
Nicotinamide Adenine Dinucleotide-specific “Malic” Enzyme in Kalanchoë daigremontiana and Other Plants Exhibiting Crassulacean Acid Metabolism
journal, February 1976
- Dittrich, Peter
- Plant Physiology, Vol. 57, Issue 2
Determination of NAD Malic Enzyme in Leaves of C 4 Plants: EFFECTS OF MALATE DEHYDROGENASE AND OTHER FACTORS
journal, February 1982
- Hatch, Marshall D.; Tsuzuki, Mikio; Edwards, Gerald E.
- Plant Physiology, Vol. 69, Issue 2
Stomatal responses to CO 2 during a diel Crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata
journal, May 2009
- Von Caemmerer, Susanne; Griffiths, Howard
- Plant, Cell & Environment, Vol. 32, Issue 5
Cloning of the Arabidopsis Clock Gene TOC1, an Autoregulatory Response Regulator Homolog
journal, August 2000
- Strayer, C.
- Science, Vol. 289, Issue 5480
CRASSULACEAN ACID METABOLISM: Molecular Genetics
journal, June 1999
- Cushman, John C.; Bohnert, Hans J.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1
Crassulacean Acid Metabolism: A Curiosity in Context
journal, June 1978
- Osmond, C. B.
- Annual Review of Plant Physiology, Vol. 29, Issue 1
Works referencing / citing this record:
The role of cis-elements in the evolution of crassulacean acid metabolism photosynthesis
journal, January 2020
- Chen, Li-Yu; Xin, Yinghui; Wai, Ching Man
- Horticulture Research, Vol. 7, Issue 1
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017
- Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu
- Nature Communications, Vol. 8, Issue 1
Ecophysiology of constitutive and facultative CAM photosynthesis
journal, February 2019
- Winter, Klaus
- Journal of Experimental Botany, Vol. 70, Issue 22
Hierarchical clustering reveals unique features in the diel dynamics of metabolites in the CAM orchid Phalaenopsis
journal, April 2019
- Ceusters, Nathalie; Luca, Stijn; Feil, Regina
- Journal of Experimental Botany, Vol. 70, Issue 12
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journal, June 2019
- Davis, Sarah C.; Simpson, June; Gil-Vega, Katia del Carmen
- Journal of Experimental Botany, Vol. 70, Issue 22
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journal, September 2019
- Yang, Xiaohan; Liu, Degao; Tschaplinski, Timothy J.
- Journal of Experimental Botany, Vol. 70, Issue 22
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journal, September 2019
- Liu, Degao; Chen, Mei; Mendoza, Brian
- Journal of Experimental Botany, Vol. 70, Issue 22
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
C 4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation
journal, November 2019
- Ferrari, Renata C.; Bittencourt, Priscila P.; Rodrigues, Maria A.
- New Phytologist, Vol. 225, Issue 4
Altered Gene Regulatory Networks Are Associated With the Transition From C3 to Crassulacean Acid Metabolism in Erycina (Oncidiinae: Orchidaceae)
journal, January 2019
- Heyduk, Karolina; Hwang, Michelle; Albert, Victor
- Frontiers in Plant Science, Vol. 9
Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses
journal, January 2009
- Wang, Xiyin; Gowik, Udo; Tang, Haibao
- Genome Biology, Vol. 10, Issue 6
Shared expression of crassulacean acid metabolism (CAM) genes pre-dates the origin of CAM in the genus Yucca
journal, April 2019
- Heyduk, Karolina; Ray, Jeremy N.; Ayyampalayam, Saaravanaraj
- Journal of Experimental Botany, Vol. 70, Issue 22
The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism
journal, December 2017
- Yang, Xiaohan; Hu, Rongbin; Yin, Hengfu
- Nature Communications, Vol. 8, Issue 1
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
Comparative genomics can provide new insights into the evolutionary mechanisms and gene function in CAM plants
journal, September 2019
- Yang, Xiaohan; Liu, Degao; Tschaplinski, Timothy J.
- Journal of Experimental Botany, Vol. 70, Issue 22
CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants
journal, September 2019
- Liu, Degao; Chen, Mei; Mendoza, Brian
- Journal of Experimental Botany, Vol. 70, Issue 22