scholarly journals Metabolic Modeling of the C3-CAM Continuum Revealed the Establishment of a Starch/Sugar-Malate Cycle in CAM Evolution

2021 ◽  
Vol 11 ◽  
Author(s):  
Ignacius Y. Y. Tay ◽  
Kristoforus Bryant Odang ◽  
C. Y. Maurice Cheung
Keyword(s):  
Crassulacean Acid Metabolism ◽  
Large Scale ◽  
Acid Metabolism ◽  
Metabolic Modeling ◽  
Light Period ◽  
Mitochondrial Electron Transport Chain ◽  
Metabolic Fluxes ◽  
Transport Chain ◽  
Use Efficiency ◽  
Constraint Based Modeling

The evolution of Crassulacean acid metabolism (CAM) is thought to be along a C3-CAM continuum including multiple variations of CAM such as CAM cycling and CAM idling. Here, we applied large-scale constraint-based modeling to investigate the metabolism and energetics of plants operating in C3, CAM, CAM cycling, and CAM idling. Our modeling results suggested that CAM cycling and CAM idling could be potential evolutionary intermediates in CAM evolution by establishing a starch/sugar-malate cycle. Our model analysis showed that by varying CO2 exchange during the light period, as a proxy of stomatal conductance, there exists a C3-CAM continuum with gradual metabolic changes, supporting the notion that evolution of CAM from C3 could occur solely through incremental changes in metabolic fluxes. Along the C3-CAM continuum, our model predicted changes in metabolic fluxes not only through the starch/sugar-malate cycle that is involved in CAM photosynthetic CO2 fixation but also other metabolic processes including the mitochondrial electron transport chain and the tricarboxylate acid cycle at night. These predictions could guide engineering efforts in introducing CAM into C3 crops for improved water use efficiency.

scholarly journals Metabolic modelling of the C3-CAM continuum revealed the establishment of a starch/sugar-malate cycle in CAM evolution

2019 ◽  
Author(s):  
Ignacius Y. Y. Tay ◽  
Kristoforus Bryant Odang ◽  
C. Y. Maurice Cheung
Keyword(s):  
Crassulacean Acid Metabolism ◽  
Electron Transport Chain ◽  
Large Scale ◽  
Acid Metabolism ◽  
Light Period ◽  
Mitochondrial Electron Transport Chain ◽  
Metabolic Modelling ◽  
Metabolic Fluxes ◽  
Transport Chain ◽  
Use Efficiency

AbstractThe evolution of Crassulacean acid metabolism (CAM) is thought to be along a C3-CAM continuum including multiple variations of CAM such as CAM cycling and CAM idling. Here, we applied large-scale constraint-based modelling to investigate the metabolism and energetics of plants operating in C3, CAM, CAM cycling and CAM idling. Our modelling results suggested that CAM cycling and CAM idling could be potential evolutionary intermediates in CAM evolution by establishing a starch/sugar-malate cycle. Our model analysis showed that by varying CO2 exchange during the light period, as a proxy of stomatal conductance, there exists a C3-CAM continuum with gradual metabolic changes, supporting the notion that evolution of CAM from C3 could occur solely through incremental changes in metabolic fluxes. Along the C3-CAM continuum, our model predicted changes in metabolic fluxes not only through the starch/sugar-malate cycle that is involved in CAM photosynthetic CO2 fixation but also other metabolic processes including the mitochondrial electron transport chain and the tricarboxylate acid cycle at night. These predictions could guide engineering efforts in introducing CAM into C3 crops for improved water use efficiency.

Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns

1999 ◽  
Vol 26 (8) ◽  
pp. 749 ◽  
Author(s):  
Joseph A.M. Holtum ◽  
Klaus Winter
Keyword(s):  
Carbon Isotope ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Dark Period ◽  
Titratable Acidity ◽  
Isotope Ratios ◽  
Light Period ◽  
Co2 Uptake ◽  
Carbon Isotope Ratios ◽  
Net Co2 Uptake

Crassulacean acid metabolism (CAM) was observed in three species of tropical ferns, the epiphytes Microsorium punctatum and Polypodium crassifolium and the lithophyte Platycerium veitchii. Polypodium crassifolium and P. veitchii exhibited characteristics of weak CAM. Although no net nocturnal CO2 uptake was observed, the presence of CAM was inferred from nocturnal increases in titratable acidity of 4.7 and 4.1 µequiv (g fr wt)–1 respectively, a reduction in the rates of net CO2 evolution during the first half of the dark period, and the presence of a CAM-like decrease in net CO2 uptake during the early light period. In M. punctatum net CO2 uptake during the first half of the dark period was accompanied by an increase in titratable acidity of 39.2 µequiv (g fr wt)–1 and a pronounced reduction in net CO2 uptake during the early light period. When water was withheld from P. crassifolium and M. punctatum, net CO2 uptake during the light was reduced markedly but there was no change in the extent or patterns of CO2 exhange in the dark. As a consequence, the proportion of carbon gained due to CO2 fixation in the dark increased from 2.8 and 10% to 63.5 and 49.3%, respectively (100% being net CO2 uptake during the light plus the estimated CO2 uptake during the dark). After 9 days without added water, dark CO2 uptake was responsible for the maintenance of a net 24 h carbon gain in P. crassifolium. Platycerium veitchii, P. crassifolium and M. punctatum exhibited carbon isotope ratios of between –25.9 and –22.6‰ indicating that carbon isotope ratios may not, by themselves, be sufficient for the identification of weak CAM. We suggest that CAM may be more prevalent in tropical epiphytic and lithophytic ferns than currently envisaged.

scholarly journals CO2 starvation experiments provide support for the carbon-limited hypothesis on the evolution of CAM-like behaviour in Isoëtes

2020 ◽  
Vol 127 (1) ◽  
pp. 135-141
Author(s):  
Jacob S Suissa ◽  
Walton A Green
Keyword(s):  
Aquatic Ecosystems ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Selective Pressure ◽  
Atmospheric Co2 ◽  
Terrestrial Plants ◽  
Cam Plants ◽  
Acid Accumulation ◽  
Use Efficiency ◽  
Nocturnal Acid Accumulation

Abstract Background and Aims Crassulacean acid metabolism (CAM) is an adaptation to increase water use efficiency in dry environments. Similar biochemical patterns occur in the aquatic lycophyte genus Isoëtes. It has long been assumed and accepted that CAM-like behaviour in these aquatic plants is an adaptation to low daytime carbon levels in aquatic ecosystems, but this has never been directly tested. Methods To test this hypothesis, populations of Isoëtes engelmannii and I. tuckermanii were grown in climate-controlled chambers and starved of atmospheric CO2 during the day while pH was measured for 24 h. Key Results We demonstrate that terrestrial plants exposed to low atmospheric CO2 display diel acidity cycles similar to those in both xerophytic CAM plants and submerged Isoëtes. Conclusions Daytime CO2 starvation induces CAM-like nocturnal acid accumulation in terrestrial Isoëtes, substantiating the hypothesis that carbon starvation is a selective pressure for this physiological behaviour.

Regulation of Rubisco activity in crassulacean acid metabolism plants: better late than never

2002 ◽  
Vol 29 (6) ◽  
pp. 689 ◽  
Author(s):  
Kate Maxwell ◽  
Howard Griffiths ◽  
Brent Helliker ◽  
Andrew Roberts ◽  
Richard P. Haslam ◽  
...  
Keyword(s):  
Electron Transport ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Rubisco Activase ◽  
Light Period ◽  
Phase Iii ◽  
Co2 Uptake ◽  
Rubisco Activity ◽  
Free Atmosphere ◽  
Phase Iv

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. The diurnal regulation of Rubisco was compared for a range of crassulacean acid metabolism (CAM) species in the context of high carboxylation and electron transport capacities, which may be an order of magnitude greater than rates of net CO2 uptake. Early in the light period, Rubisco activity and electron transport were limited when phosphoenolpyruvate carboxylase (PEPC) may have been operating, and maximal extractable activities and activation state for Rubisco were achieved at the end of Phase III, prior to the direct atmospheric uptake of CO2 during Phase IV. The delayed activation was associated with levels of Rubisco activase protein, which reached a maximum at midday, and may account for this pattern of Rubisco activation. This regulation may be modified by environmental conditions - processes that tend to restrict PEPC activity, such as drought stress or incubation of leaves overnight in an oxygen-free atmosphere, release Rubisco from inhibition early in the light period. The quantum yield of light use also tracks Rubisco carboxylation, being particularly low at dawn when PEPC is active. The plasticity in expression of the CAM cycle is therefore matched by the regulation of key carboxylases, with extractable Rubisco activity maximal when drawdown of atmospheric CO2 to cells in succulent CAM tissues is most likely to limit photon utilization shortly after midday, during Phase IV.

Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism

2005 ◽  
Vol 32 (5) ◽  
pp. 381 ◽  
Author(s):  
Klaus Winter ◽  
Jorge Aranda ◽  
Joseph A. M. Holtum
Keyword(s):  
Water Use Efficiency ◽  
Water Use ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Aloe Vera ◽  
Dry Mass ◽  
Tropical Conditions ◽  
Δ13c Value ◽  
Use Efficiency ◽  
Cam Species

The relationship between water-use efficiency, measured as the transpiration ratio (g H2O transpired g–1 above- plus below-ground dry mass accumulated), and 13C / 12C ratio (expressed as δ13C value) of bulk biomass carbon was compared in 15 plant species growing under tropical conditions at two field sites in the Republic of Panama. The species included five constitutive crassulacean acid metabolism (CAM) species [Aloe vera (L.) Webb & Berth., Ananas comosus (L.) Merr., Euphorbia tirucalli L., Kalanchoë daigremontiana Hamet et Perr., Kalanchoë pinnata (Lam.) Pers.], two species of tropical C3 trees (Tectona grandis Linn. f. and Swietenia macrophylla King), one C4 species (Zea mays L.), and seven arborescent species of the neotropical genus Clusia, of which two exhibited pronounced CAM. The transpiration ratios of the C3 and CAM species, which ranged between 496 g H2O g–1 dry mass in the C3–CAM species Clusia pratensis Seeman to 54 g H2O g–1 dry mass in the constitutive CAM species Aloe vera, correlated strongly with δ13C values and nocturnal CO2 gain suggesting that δ13C value can be used to estimate both water-use efficiency and the proportion of CO2 gained by CAM species during the light and the dark integrated over the lifetime of the tissues.

scholarly journals Engineering crassulacean acid metabolism to improve water-use efficiency

2014 ◽  
Vol 19 (5) ◽  
pp. 327-338 ◽  
Author(s):  
Anne M. Borland ◽  
James Hartwell ◽  
David J. Weston ◽  
Karen A. Schlauch ◽  
Timothy J. Tschaplinski ◽  
...  
Keyword(s):  
Water Use Efficiency ◽  
Water Use ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Use Efficiency

scholarly journals Transcript and metabolite changes during the early phase of abscisic acid-mediated induction of crassulacean acid metabolism in Talinum triangulare

2019 ◽  
Vol 70 (22) ◽  
pp. 6581-6596 ◽  
Author(s):  
Eva Maleckova ◽  
Dominik Brilhaus ◽  
Thomas J Wrobel ◽  
Andreas P M Weber
Keyword(s):  
Abscisic Acid ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Enrichment Analysis ◽  
Titratable Acidity ◽  
Abscisic Acid Metabolism ◽  
Use Efficiency ◽  
Cam Regulation ◽  
Cam Species ◽  
Talinum Triangulare

Abstract Crassulacean acid metabolism (CAM) has evolved as a water-saving strategy, and its engineering into crops offers an opportunity to improve their water use efficiency. This requires a comprehensive understanding of the regulation of the CAM pathway. Here, we use the facultative CAM species Talinum triangulare as a model in which CAM can be induced rapidly by exogenous abscisic acid. RNA sequencing and metabolite measurements were employed to analyse the changes underlying CAM induction and identify potential CAM regulators. Non-negative matrix factorization followed by k-means clustering identified an early CAM-specific cluster and a late one, which was specific for the early light phase. Enrichment analysis revealed abscisic acid metabolism, WRKY-regulated transcription, sugar and nutrient transport, and protein degradation in these clusters. Activation of the CAM pathway was supported by up-regulation of phosphoenolpyruvate carboxylase, cytosolic and chloroplastic malic enzymes, and several transport proteins, as well as by increased end-of-night titratable acidity and malate accumulation. The transcription factors HSFA2, NF-YA9, and JMJ27 were identified as candidate regulators of CAM induction. With this study we promote the model species T. triangulare, in which CAM can be induced in a controlled way, enabling further deciphering of CAM regulation.

scholarly journals Exploring the Relationship between Crassulacean Acid Metabolism (CAM) and Mineral Nutrition with a Special Focus on Nitrogen

2019 ◽  
Vol 20 (18) ◽  
pp. 4363 ◽  
Author(s):  
Paula Natália Pereira ◽  
John C. Cushman
Keyword(s):  
Water Use Efficiency ◽  
Water Use ◽  
Nutrient Availability ◽  
Crassulacean Acid Metabolism ◽  
Acid Metabolism ◽  
Special Focus ◽  
Cam Plants ◽  
Use Efficiency ◽  
Cam Species ◽  
The Relationship

Crassulacean acid metabolism (CAM) is characterized by nocturnal CO2 uptake and concentration, reduced photorespiration, and increased water-use efficiency (WUE) when compared to C3 and C4 plants. Plants can perform different types of CAM and the magnitude and duration of CAM expression can change based upon several abiotic conditions, including nutrient availability. Here, we summarize the abiotic factors that are associated with an increase in CAM expression with an emphasis on the relationship between CAM photosynthesis and nutrient availability, with particular focus on nitrogen, phosphorus, potassium, and calcium. Additionally, we examine nitrogen uptake and assimilation as this macronutrient has received the greatest amount of attention in studies using CAM species. We also discuss the preference of CAM species for different organic and inorganic sources of nitrogen, including nitrate, ammonium, glutamine, and urea. Lastly, we make recommendations for future research areas to better understand the relationship between macronutrients and CAM and how their interaction might improve nutrient and water-use efficiency in order to increase the growth and yield of CAM plants, especially CAM crops that may become increasingly important as global climate change continues.

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