Rethinking the potential productivity of crassulacean acid metabolism by integrating metabolic dynamics with shoot architecture, using the example of Agave tequilana.
3-D plant form
bioenergy
crassulacean acid metabolism
crassulacean acid metabolism (CAM) photosynthesis
drought
food security
metabolic model
photosynthesis
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
31
10
2022
accepted:
04
06
2023
medline:
18
8
2023
pubmed:
4
8
2023
entrez:
3
8
2023
Statut:
ppublish
Résumé
Terrestrial CAM plants typically occur in hot semiarid regions, yet can show high crop productivity under favorable conditions. To achieve a more mechanistic understanding of CAM plant productivity, a biochemical model of diel metabolism was developed and integrated with 3-D shoot morphology to predict the energetics of light interception and photosynthetic carbon assimilation. Using Agave tequilana as an example, this biochemical model faithfully simulated the four diel phases of CO
Substances chimiques
Carbon
7440-44-0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2180-2196Informations de copyright
© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.
Références
Abraham PE, Yin H, Borland AM, Weighill D, Lim SD, De Paoli HC, Engle N, Jones PC, Agh R, Weston DJ et al. 2016. Transcript, protein and metabolite temporal dynamics in the CAM plant Agave. Nature Plants 2: 16178.
Alduchov OA, Eskridge RE. 1996. Improved Magnus form approximation of saturation vapor pressure. Journal of Applied Meteorology 35: 601-609.
Arundale RA, Dohleman FG, Heaton EA, McGrath JM, Voigt TB, Long SP. 2014. Yields of Miscanthus × giganteus and Panicum virgatum decline with stand age in the Midwestern USA. Global Change Biology Bioenergy 6: 1-13.
Ball JT, Woodrow IE, Berry JA. 1987. A model predicting stomatal conductance and its contribution to the control of photosynthesis under different environmental conditions. In: Biggens J, ed. Progress in photosynthesis research, vol. IV. Dordrecht, the Netherlands: Martinus Nijhoff Publishers, 221-224.
Ball TJ, Berry JA. 1982. The Ci/Cs ratio: a basis for predicting stomatal control of photosynthesis. Carnegie Institution of Washington Year Book 81: 88-92.
Bartlett MS, Vico G, Porporato A. 2014. Coupled carbon and water fluxes in CAM photosynthesis: modeling quantification of water use efficiency and productivity. Plant and Soil 383: 111-138.
Beale CV, Long SP. 1995. Can perennial C4 grasses attain high efficiencies of radiant energy conversion in cool climates? Plant, Cell & Environment 18: 641-650.
Blasius B, Beck F, Lüttge U. 1997. A model for photosynthetic oscillations in crassulacean acid metabolism (CAM). Journal of Theoretical Biology 184: 345-351.
Blasius B, Beck F, Lüttge U. 1998. Oscillatory model of crassulacean acid metabolism: structural analysis and stability boundaries with a discrete hysteresis switch. Plant, Cell & Environment 21: 775-784.
Blasius B, Neif R, Beck F, Lüttge U. 1999. Oscillatory model of crassulacean acid metabolism with a dynamic hysteresis switch. Proceedings of the Royal Society of London B: Biological Sciences 266: 93-101.
Borland AM, Griffiths H. 1997. A comparative study on the regulation of C3 and C4 carboxylation processes in the constitutive crassulacean acid metabolism (CAM) plant Kalanchoë daigremontiana and the C3-CAM intermediate Clusia minor. Planta 201: 368-378.
Borland AM, Griffiths H, Hartwell J, Smith JAC. 2009. Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. Journal of Experimental Botany 60: 2879-2896.
Borland AM, Guo H-B, Yang X, Cushman JC. 2016. Orchestration of carbohydrate processing for crassulacean acid metabolism. Current Opinion in Plant Biology 31: 118-124.
Borland AM, Hartwell J, Weston DJ, Schlauch KA, Tschaplinski TJ, Tuskan GA, Yang X, Cushman JC. 2014. Engineering crassulacean acid metabolism to improve water-use efficiency. Trends in Plant Science 19: 327-338.
Boxall SF, Kadu N, Dever LV, Kneřová J, Waller JL, Gould PJD, Hartwell J. 2020. Kalanchoë PPC1 is essential for crassulacean acid metabolism and the regulation of core circadian clock and guard cell signaling genes. Plant Cell 32: 1136-1160.
Boyd RA, Gandin A, Cousins AB. 2015. Temperature responses of C4 photosynthesis: biochemical analysis of Rubisco, phosphoenolpyruvate carboxylase, and carbonic anhydrase in Setaria viridis. Plant Physiology 169: 1850-1861.
Brilhaus D, Bräutigam A, Mettler-Altmann T, Winter K, Weber APM. 2015. Reversible burst of transcriptional changes during induction of crassulacean acid metabolism (CAM) in Talinum triangulare. Plant Physiology 170: 102-122.
Burgos A, Miranda E, Vilaprinyo E, Meza-Canales ID, Alves R. 2022. CAM models: lessons and implications for CAM evolution. Frontiers in Plant Science 13: 893095.
von Caemmerer S. 2000. Biochemical models of leaf photosynthesis. Collingwood, Victoria, Australia: CSIRO Publishing.
Ceusters N, Borland AM, Ceusters J. 2021. How to resolve the enigma of diurnal malate remobilisation from the vacuole in plants with crassulacean acid metabolism? New Phytologist 229: 3116-3124.
Ceusters N, Luca S, Feil R, Claes JE, Lunn JE, Van den Ende W, Ceusters J. 2019. Hierarchical clustering reveals unique features in the diel dynamics of metabolites in the CAM orchid Phalaenopsis. Journal of Experimental Botany 70: 3269-3281.
Chaves CJN, Leal BSS, de Lemos-Filho JP. 2015. Temperature modulation of thermal tolerance of a CAM-tank bromeliad and the relationship with acid accumulation in different leaf regions. Physiologia Plantarum 154: 500-510.
Cheung CM, Poolman MG, Fell DA, Ratcliffe RG, Sweetlove LJ. 2014. A diel flux balance model captures interactions between light and dark metabolism during day-night cycles in C3 and crassulacean acid metabolism leaves. Plant Physiology 165: 917-929.
Chomthong M, Griffiths H. 2020. Model approaches to advance crassulacean acid metabolism system integration. The Plant Journal 101: 951-963.
Cockburn W, Ting IP, Sternberg LO. 1979. Relationships between stomatal behavior and internal carbon dioxide concentration in crassulacean acid metabolism plants. Plant Physiology 63: 1029-1032.
Collatz GJ, Ribas-Carbo M, Berry J. 1992. Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Functional Plant Biology 19: 519-538.
Comins H, Farquhar G. 1982. Stomatal regulation and water economy in Crassulacean acid metabolism plants: an optimization model. Journal of Theoretical Biology 99: 263-284.
Cushman JC, Davis SC, Yang X, Borland AM. 2015. Development and use of bioenergy feedstocks for semi-arid and arid lands. Journal of Experimental Botany 66: 4177-4193.
Davey PA, Hunt S, Hymus GJ, DeLucia EH, Drake BG, Karnosky DF, Long SP. 2004. Respiratory oxygen uptake is not decreased by an instantaneous elevation of [CO2], but is increased with long-term growth in the field at elevated [CO2]. Plant Physiology 134: 520-527.
Davis SC, Kuzmick ER, Niechayev N, Hunsaker DJ. 2017. Productivity and water use efficiency of Agave americana in the first field trial as bioenergy feedstock on arid lands. Global Change Biology Bioenergy 9: 314-325.
Davis SC, LeBauer DS, Long SP. 2014. Light to liquid fuel: theoretical and realized energyconversion efficiency of plants using crassulacean acid metabolism (CAM) in arid conditions. Journal of Experimental Botany 65: 3471-3478.
Davis SC, Simpson J, Gil-Vega KC, Niechayev NA, Ev T, Castano NH, Dever LV, Búrquez A. 2019. Undervalued potential of crassulacean acid metabolism for current and future agricultural production. Journal of Experimental Botany 70: 6521-6537.
De Pury DGG, Farquhar G. 1997. Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant, Cell & Environment 20: 537-557.
De Souza AP, Burguess SJ, Doran L, Hansen J, Manukyan L, Maryn N, Gotarkar D, Leonelli L, Niyogi KK, Long SP. 2022. Soybean photosynthesis and crop yield is improved by accelerating recovery from photoprotection. Science 377: 851-854.
Dever LV, Boxall SF, Kneřová J, Hartwell J. 2015. Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiology 167: 44-59.
Díaz-Torres JJ, Hernández-Mena L, Murillo-Tovar MA, León-Becerril E, López-López A, Suárez-Plascencia C, Aviña-Rodriguez E, Barradas-Gimate A, Ojeda-Castillo V. 2017. Assessment of the modulation effect of rainfall on solar radiation availability at the Earth's surface. Meteorological Applications 24: 180-190.
Dittrich P. 1976. Nicotinamide adenine dinucleotide-specific “malic” enzyme in Kalanchoë daigremontiana and other plants exhibiting crassulacean acid metabolism. Plant Physiology 57: 310-314.
Farquhar GD, von Caemmerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78-90.
Freschi L, Takahashi CA, Cambui CA, Semprebom TR, Cruz AB, Mioto PT, de Melo VL, Calvente A, Latansio-Aidar SR, Aidar MPM. 2010. Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage. Journal of Plant Physiology 167: 526-533.
Garcia-Moya E, Romero-Manzanares A, Nobel PS. 2011. Highlights for Agave productivity. Global Change Biology Bioenergy 3: 4-14.
Gentry HS. 1982. Agaves of continental North America. Tucson, AZ, USA: The University of Arizona Press.
Hartzell S, Bartlett MS, Inglese P, Consoli S, Yin J, Porporato A. 2021. Modelling nonlinear dynamics of Crassulacean acid metabolism productivity and water use for global predictions. Plant, Cell & Environment 44: 34-48.
Hartzell S, Bartlett MS, Porporato A. 2018. Unified representation of the C3, C4, and CAM photosynthetic pathways with the Photo3 model. Ecological Modelling 384: 173-187.
Holtum JAM, Winter K. 2014. Limited photosynthetic plasticity in the leaf-succulent CAM plant Agave angustifolia. Functional Plant Biology 41: 843-849.
Huang J, Yu H, Guan X, Wang G, Guo R. 2016. Accelerated dryland expansion under climate change. Nature Climate Change 6: 166-171.
IPCC. 2023. IPCC Sixth Assessment Report (AR6) “climate change 2023” synthesis report approved summary for policymakers. Geneva, Switzerland: IPCC/UNEP/WHO.
Kannan K, Wang Y, Lang M, Challa GS, Long SP, Marshall-Colon A. 2019. Combining gene network, metabolic and leaf-level models shows means to future-proof soybean photosynthesis under rising CO2. in silico Plants 1: diz008.
Kearns J, Teletzke G, Palmer J, Thomann H, Kheshgi H, Chen Y-HH, Paltsev S, Herzog H. 2017. Developing a consistent database for regional geologic CO2 storage capacity worldwide. Energy Procedia 114: 4697-4709.
Kluge M, Ting IP. 1978. Crassulacean acid metabolism: analysis of an ecological adaptation. Berlin, Germany: Springer-Verlag.
Köhler IH, Ruiz-Vera UM, VanLoocke A, Thomey ML, Clemente T, Long SP, Ort DR, Bernacchi CJ. 2017. Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions. Journal of Experimental Botany 68: 715-726.
Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP. 2016. Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354: 857-861.
Lim SD, Lee S, Choi W-G, Yim WC, Cushman JC. 2019. Laying the foundation for crassulacean acid metabolism (CAM) biodesign: expression of the C4 metabolism cycle genes of CAM in Arabidopsis. Frontiers in Plant Science 10: 101.
Liu D, Chen M, Mendoza B, Cheng H, Hu R, Li L, Trinh CT, Tuskan GA, Yang X. 2019. CRISPR/Cas9-mediated targeted mutagenesis for functional genomics research of crassulacean acid metabolism plants. Journal of Experimental Botany 70: 6621-6629.
Lüttge U. 2000. The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211: 761-769.
Lüttge U, Ball E. 1987. Dark respiration of CAM plants. Plant Physiology and Biochemistry 25: 3-10.
Lüttge U, Beck F. 1992. Endogenous rhythms and chaos in crassulacean acid metabolism. Planta 188: 28-38.
Lüttge U, Smith JAC. 1984. Mechanism of passive malic-acid efflux from vacuoles of the CAM plant Kalanchoë daigremontiana. Journal of Membrane Biology 81: 149-158.
Lüttge U, Smith JAC, Marigo OCB. 1981. Energetics of malate accumulation in the vacuoles of Kalanchoë tubiflora cells. FEBS Letters 126: 81-84.
Males J, Griffiths H. 2017. Stomatal biology of CAM plants. Plant Physiology 174: 550-560.
MATLAB. 2017. Mathworks Inc. [WWW document] URL www.mathworks.com [accessed 14 April 2023].
Maxwell K, Borland AM, Haslam RP, Helliker BR, Roberts A, Griffiths H. 1999. Modulation of Rubisco activity during the diurnal phases of the crassulacean acid metabolism plant Kalanchoë daigremontiana. Plant Physiology 121: 849-856.
Ming R, VanBuren R, Wai CM, Tang H, Schatz MC, Bowers JE, Lyons E, Wang M-L, Chen J, Biggers E et al. 2015. The pineapple genome and the evolution of CAM photosynthesis. Nature Genetics 47: 1435-1442.
Morgan JA, Rhodes D. 2002. Mathematical modeling of plant metabolic pathways. Metabolic Engineering 4: 80-89.
Morison JIL. 1987. Intercellular CO2 concentration and stomatal response to CO2. In: Zeiger E, Farquhar GD, Cowan IR, eds. Stomatal function. Stanford, CA, USA: Stanford University Press, 229-251.
Nabhan GP, Colunga-GarcíaMarín P, Zizumbo-Villarreal D. 2022. Comparing wild and cultivated food plant richness between the Arid American and the Mesoamerican centers of diversity, as means to advance indigenous food sovereignty in the face of climate change. Frontiers in Sustainable Food Systems 6: 840619.
Neales T. 1973. The effect of night temperature on CO2 assimilation, transpiration, and water use efficiency in Agave americana L. Australian Journal of Biological Sciences 26: 705-714.
Neff R, Blasius B, Beck F, Lüttge U. 1998. Thermodynamics and energetics of the tonoplast membrane operating as a hysteresis switch in an oscillatory model of crassulacean acid metabolism. Journal of Membrane Biology 165: 37-43.
Niechayev NA, Jones AM, Rosenthal DM, Davis SC. 2019a. A model of environmental limitations on production of Agave americana L. grown as a biofuel crop in semi-arid regions. Journal of Experimental Botany 70: 6549-6559.
Niechayev NA, Pereira PN, Cushman JC. 2019b. Understanding trait diversity associated with crassulacean acid metabolism (CAM). Current Opinion in Plant Biology 49: 74-85.
Nimmo HG. 2000. The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5: 75-80.
Nobel PS. 1984. Productivity of Agave deserti: measurement by dry weight and monthly prediction using physiological responses to environmental parameters. Oecologia 64: 1-7.
Nobel PS. 1985. PAR, water and temperature limitations on the productivity of cultivated Agave fourcroydes (henequen). Journal of Applied Ecology 22: 157-173.
Nobel PS. 1988. Environmental biology of agaves and cacti. Cambridge, UK: Cambridge University Press.
Nobel PS. 1991. Achievable productivities of certain CAM plants: basis for high values compared with C3 and C4 plants. New Phytologist 119: 183-205.
Nobel PS. 2000. Crop ecosystem responses to climatic change: crassulacean acid metabolism crops. In: Reddy KR, Hodges HF, eds. Climate change and global crop productivity. New York, NY, USA: CABI Publishing, 315-331.
Nobel PS, García de Cortázar V. 1987. Interception of photosynthetically active radiation and predicted productivity for Agave rosettes. Photosynthetica 21: 261-272.
Nobel PS, Valenzuela AG. 1987. Environmental responses and productivity of the CAM plant, Agave tequilana. Agricultural and Forest Meteorology 39: 319-334.
Nungesser D, Kluge M, Tolle H, Oppelt W. 1984. A dynamic computer model of the metabolic and regulatory processes in Crassulacean acid metabolism. Planta 162: 204-214.
Ogburn RM, Edwards EJ. 2010. The ecological water-use strategies of succulent plants. Advances in Botanical Research 55: 179-225.
Ögren E, Evans JR. 1993. Photosynthetic light-response curves. 1. The influence of CO2 partial pressure and leaf inversion. Planta 189: 182-190.
Osmond CB. 1978. Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29: 379-414.
Owen NA, Choncubhair ÓN, Males J, del Real Laborde JI, Rubio-Cortés R, Griffiths H, Lanigan G. 2016. Eddy covariance captures four-phase crassulacean acid metabolism (CAM) gas exchange signature in Agave. Plant, Cell & Environment 39: 295-309.
Owen NA, Griffiths H. 2013. A system dynamics model integrating physiology and biochemical regulation predicts extent of crassulacean acid metabolism (CAM) phases. New Phytologist 200: 1116-1131.
Owen NA, Griffiths H. 2014. Marginal land bioethanol yield potential of four crassulacean acid metabolism candidates (Agave fourcroydes, Agave salmiana, Agave tequilana and Opuntia ficus-indica) in Australia. Global Change Biology Bioenergy 6: 687-703.
Pérez-Pimienta JA, López-Ortega MG, Sanchez A. 2017. Recent developments in agave performance as a drought-tolerant biofuel feedstock: agronomics, characterization, and biorefining. Biofuels, Bioproducts and Biorefining 11: 732-748.
Popp M, Janett HP, Lüttge U, Medina E. 2003. Metabolite gradients and carbohydrate translocation in rosette leaves of CAM and C3 bromeliads. New Phytologist 157: 649-656.
Prăvălie R. 2016. Drylands extent and environmental issues. A global approach. Earth-Science Reviews 161: 259-278.
Purseglove J. 1972. Tropical crops. Monocotyledons 1. London, UK: Longman.
Renewable Fuels Association. 2021. [WWW document] URL https://ethanolrfa.org/markets-and-statistics/annual-ethanol-production [accessed 14 March 2023].
Saitou K, Agata W, Asakura M, Kubota F. 1992. Structural and kinetic properties of NADP-malic enzyme from the inducible Crassulacean Acid Metabolism plant Mesembryanthemum crystallinum L. Plant and Cell Physiology 33: 595-600.
Schiller K, Bräutigam A. 2021. Engineering of crassulacean acid metabolism. Annual Review of Plant Biology 72: 77-103.
Shameer S, Baghalian K, Cheung CYM, Ratcliffe RG, Sweetlove LJ. 2018. Computational analysis of the productivity potential of CAM. Nature Plants 4: 165-171.
Shameer S, Wang Y, Bota P, Ratcliffe RG, Long SP, Sweetlove LJ. 2022. A hybrid kinetic and constraint-based model of leaf metabolism allows predictions of metabolic fluxes in different environments. The Plant Journal 109: 295-313.
Slattery RA, Ort DR. 2015. Photosynthetic energy conversion efficiency: setting a baseline for gauging future improvements in important food and biofuel crops. Plant Physiology 168: 383-392.
Smith JAC, Ingram J, Tsiantis MS, Barkla BJ, Bartholomew DM, Bettey M, Pantoja O, Pennington AJ. 1996. Transport across the vacuolar membrane in CAM plants. In: Winter K, Smith JAC, eds. Crassulacean acd metabolism: biochemistry, ecophysiology and evolution. Berlin, Germany: Springer, 53-71.
Smith JAC, Nobel PS. 1986. Water movement and storage in a desert succulent: anatomy and rehydration kinetics for leaves of Agave deserti. Journal of Experimental Botany 37: 1044-1053.
Song Q, Zhang GL, Zhu X-G. 2013. Optimal crop canopy architecture to maximise canopy photosynthetic CO2 uptake under elevated CO2 - a theoretical study using a mechanistic model of canopy photosynthesis. Functional Plant Biology 40: 109-124.
Spalding MH, Stumpf DK, Ku MSB, Burris RH, Edwards GE. 1979. Crassulacean acid metabolism and diurnal variations of internal CO2 and O2 concentrations in Sedum praealtum DC. Australian Journal of Plant Physiology 6: 557-567.
Stewart JR. 2015. Agave as a model CAM crop system for a warming and drying world. Frontiers in Plant Science 6: 684.
Töpfer N, Braam T, Shameer S, Ratcliffe RG, Sweetlove LJ. 2020. Alternative crassulacean acid metabolism modes provide environment-specific water-saving benefits in a leaf metabolic model. Plant Cell 32: 3689-3705.
Van Velthuizen H. 2007. Mapping biophysical factors that influence agricultural production and rural vulnerability (no. 11). Rome, Italy: Food & Agriculture Organization.
Wai CM, VanBuren R, Zhang J, Huang L, Miao W, Edger PP, Yim WC, Priest HD, Meyers BC, Mockler T et al. 2017. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. The Plant Journal 92: 19-30.
Wang Y, Bräutigam A, Weber APM, Zhu X-G. 2014a. Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis. Journal of Experimental Botany 65: 3567-3578.
Wang Y, Chan KX, Long SP. 2021. Towards a dynamic photosynthesis model to guide yield improvement in C4 crops. The Plant Journal 107: 343-359.
Wang Y, Long SP, Zhu X-G. 2014b. Elements required for an efficient NADP-malic enzyme type C4 photosynthesis. Plant Physiology 164: 2231-2246.
Wang Y, Song Q, Jaiswal D, De Souza AP, Long SP, Zhu XG. 2017. Development of a three-dimensional ray-tracing model of sugarcane canopy photosynthesis and its application in assessing impacts of varied row spacing. Bioenergy Research 10: 626-634.
Winter K. 1985. Crassulacean acid metabolism. In: Barber J, Baker NR, eds. Photosynthetic mechanisms and the environment. Amsterdam, the Netherlands: Elsevier, 329-387.
Winter K, Garcia M, Holtum JAM. 2014. Nocturnal versus diurnal CO2 uptake: how flexible is Agave angustifolia? Journal of Experimental Botany 65: 3695-3703.
Winter K, Smith JAC. 1996. Crassulacean acid metabolism: current status and perspectives. In: Winter K, Smith JAC, eds. Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Berlin, Germany: Springer-Verlag, 389-426.
Winter K, Smith JAC. 2022. CAM photosynthesis: the acid test. New Phytologist 233: 599-609.
Woodhouse RM, Williams JG, Nobel PS. 1980. Leaf orientation, radiation interception, and nocturnal acidity increases by the CAM plant Agave deserti (Agavaceae). American Journal of Botany 67: 1179-1185.
Yan X, Corbin KR, Burton RA, Tan DK. 2020. Agave: a promising feedstock for biofuels in the water-energy-food-environment (WEFE) nexus. Journal of Cleaner Production 261: 121283.
Yan X, Tan DK, Inderwildi OR, Smith JAC, King DA. 2011. Life cycle energy and greenhouse gas analysis for Agave-derived bioethanol. Energy & Environmental Science 4: 3110-3121.
Yang X, Cushman JC, Borland AM, Edwards EJ, Wullschleger SD, Tuskan GA, Owen NA, Griffiths H, Smith JAC, De Paoli HC et al. 2015. A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytologist 207: 491-504.
Yang X, Hu R, Yin H, Jenkins J, Shu S, Tang H, Liu D, Weighill DA, Cheol Yim W, Ha J et al. 2017. The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nature Communications 8: 1899.
Zhu XG, de Sturler E, Long SP. 2007. Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiology 145: 513-526.
Zhu XG, Long SP, Ort DR. 2008. What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Current Opinion in Biotechnology 19: 153-159.
Zhu XG, Ort DR, Whitmarsh J, Long SP. 2004. The slow reversibility of photosystem II thermal energy dissipation on transfer from high to low light may cause large losses in carbon gain by crop canopies: a theoretical analysis. Journal of Experimental Botany 55: 1167-1175.