Functional leaf anatomy of plants with crassulacean acid metabolism

2005 ◽  
Vol 32 (5) ◽  
pp. 409 ◽  
Author(s):  
Elizabeth A. Nelson ◽  
Tammy L. Sage ◽  
Rowan F. Sage

Crassulacean acid metabolism (CAM) has evolved independently on dozens of occasions and is now found in over 7% of plant species. In this study, the leaf structure of a phylogenetically diverse assemblage of 18 CAM plants was compared with six C3 plants and four C4 plants to assess whether consistent anatomical patterns that may reflect functional constraints are present. CAM plants exhibited increased cell size and increased leaf and mesophyll thickness relative to C3 and C4 species. CAM species also exhibited reduced intercellular air space (IAS) and reduced length of mesophyll surface exposed to IAS per unit area (Lmes / area). The low volume of IAS and low exposure of mesophyll surface to IAS likely increases internal resistance to CO2 in CAM tissues. While this diffusional barrier may limit uptake of CO2 during Phases II and IV, carbon economy could be enhanced through the reduced loss of internal CO2 during all four phases of CAM.


1979 ◽  
Vol 6 (4) ◽  
pp. 557 ◽  
Author(s):  
MH Spalding ◽  
DK Stumpf ◽  
MSB Ku ◽  
RH Burris ◽  
GE Edwards

Internal CO2 and O2 concentrations in Sedum praealtum DC. were determined by gas chromatography of 200-�l gas samples. Day-night monitoring showed that internal CO2 varied from a high of approximately 4000 �l/l during periods of daytime stomatal closure to a low of 270-280 �l/l during the dark period (stomata open). Internal O2 concentrations varied from a high of approximately 26 % at midday to a low of 20.8 % during the dark period. The calculated internal O2/CO2 ratio varied about 12-15-fold from 50-60 near midday to approximately 750 during the dark period (ratio in normal air is roughly 600). Day-night patterns of CO2 exchange and malic acid concentration were typical for a plant with crassulacean acid metabolism (CAM). Influx of CO2 during the late light period was inhibited by O2, but dark CO2 influx was O2-insensitive. Gas samples taken near midday from several CAM plants all showed elevated internal CO2 and O2 concentrations. Ratios of O2/CO2 in these plants ranged from 81 in Sedum praealtum to 285 in Hoya carnosa. The highest internal O2 concentration observed was 41.5% in Kalanchoe gastonis-bonnieri. The high CO2 concentration in leaves of CAM plants during daytime stomatal closure should provide a near- saturating level of this substrate for photosynthesis. In comparison to C3 plants, the relatively low O2/CO2 ratio in the CAM leaf during malic acid decarboxylation should be favourable for photosynthesis and unfavourable for O2 inhibition of photosynthesis.



2019 ◽  
Vol 20 (18) ◽  
pp. 4363 ◽  
Author(s):  
Paula Natália Pereira ◽  
John C. Cushman

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.



2002 ◽  
Vol 29 (6) ◽  
pp. 775 ◽  
Author(s):  
Rowan F. Sage

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. Despite sharing a similar metabolism, crassulacean acid metabolism (CAM) and C4 photosynthesis are not known to occur in identical species, with the exception of Portulaca spp. In Portulaca, C4 and weak CAM photosynthesis occur in distinct regions of the leaf, rather than in the same cells. This is in marked contrast to the situation in most CAM species where C3 and CAM photosynthesis are active in the same cell over the course of a day and growing season. The lack of CAM and C4 photosynthesis in identical cells of a plant indicates these photosynthetic pathways are incompatible. Incompatibilities between CAM and C4 photosynthesis could have a number of biochemical, anatomical and evolutionary explanations. Biochemical incompatibilities could result from the requirement for spatial separation of C3 and C4 phases in C4 plants versus temporal separation in CAM plants. In C4 plants, regulatory systems coordinate mesophyll and bundle sheath metabolism, with light intensity being the major environmental signal. In CAM plants, a circadian oscillator coordinates day and night phases of CAM. The requirement for rapid intercellular transport in C4 plants may be incompatible with the intracellular transport and storage needs of CAM. For example, the large vacuole required for malate storage in CAM could impede metabolite diffusion between mesophyll and bundle sheath cells in C4 plants. Anatomical barriers could also exist because both CAM and the C4 pathway require distinct leaf anatomies for efficient function. Efficient function of the C4 pathway generally requires an outer layer of cells specialized for phosphoenolpyruvate (PEP) carboxylation and regeneration and an inner layer for CO2 accumulation and refixation, while CAM species require enlarged vacuoles and tight cell packing. In evolutionary terms, barriers preventing CAM and C4 photosynthesis in the same species may be the initial steps in the respective evolutionary pathways from C3 ancestors. The first steps in C4 photosynthesis are related to scavenging photorespiratory CO2 via localization of glycine decarboxylase in the bundle sheath cells. The initial steps in CAM evolution are associated with the scavenging of respiratory CO2 at night by PEP carboxylation. In each, simplified versions of the specialized anatomy may need to be present for the evolutionary sequence to begin. For C4 evolution, enhanced bundle sheath size may be required in C3 ancestors; for CAM evolution, succulence may be required. Thus, before CAM or C4 photosynthesis began to evolve, the outcome of the evolutionary experiment may have been predetermined.



2005 ◽  
Vol 60 (3-4) ◽  
pp. 279-284 ◽  
Author(s):  
Misa Takahashi ◽  
Daisuke Konaka ◽  
Atsushi Sakamoto ◽  
Hiromichi Morikawa

Abstract In order to investigate nocturnal uptake and assimilation of NO2 by C3 and crassulacean acid metabolism (CAM) plants, they were fumigated with 4 μl I-115N-Iabeled nitrogen diox­ide (NO2) for 8 h. The amound of NO2 and assimilation of NO2by plants were determined by mass spectrometry and Kjeldahl-nitrogen based mass spectrometry, respectively. C3 plants such as kenaf (Hibiscus cannabinus), tobacco (Nicotiana tabacum) and ground cherry (Phy- salis alkekengi) showed a high uptake and assimilation during daytime as high as 1100 to 2700 ng N mg-1 dry weight. While tobacco and ground cherry strongly reduced uptake and assimilation of NO2 during nighttime, kenaf kept high nocturnal uptake and assimilation of NO2 as high as about 1500 ng N mg-1 dry weight. Stomatal conductance measurements indicated that there were no significant differences to account for the differences in the uptake of NO2 by tobacco and kenaf during nighttime. CAM plants such as Sedum sp., Kalanchoe blossfeldiana (kalanchoe) and Aloe arborescens exhibited nocturnal uptake and assimilation of NO2. However, the values of uptake and assimilation of NO2 both during daytime and nighttime was very low (at most about 500 ng N mg-1 dry weight) as compared with those of above mentioned C3 plants. The present findings indicate that kenaf is an efficient phytoremediator of NO2 both during daytime and nighttime.



1981 ◽  
Vol 8 (1) ◽  
pp. 31 ◽  
Author(s):  
JAM Holtum ◽  
CB Osmond

Pyruvate, PI dikinase (EC 2.7.9.1) was present in crassulacean acid metabolism (CAM) plants that lack phosphoenolpyruvate (PEP) carboxykinase (EC 4.1.1.32) but was not detected in plants that contain PEP carboxykinase or in C3 plants. It is suggested that, during deacidification in CAM plants that contain NAD and NADP malic enzymes (EC 1.1.1.38 and EC 1.1.1.40) but not PEP carboxykinase, pyruvate, P*i dikinase reverses the glycolytic reaction catalysed by pyruvate kinase (EC 2.7.1.40) and converts pyruvate to PEP as the first step in the gluconeogenic conservation of pyruvate as storage carbohydrate. The enzyme is not required by CAM plants that contain PEP carboxykinase and produce mainly PEP during decarboxylation. Leaf slices from Kalanchoe daigremontiana and CAM Mesembryanthemum crystallinum, two species that possess pyruvate, PI dikinase, transfer label from exogenous [3-14C]pyruvate to carbohydrates more rapidly than either Stapelia gigantea, a PEP carboxykinase CAM plant, or C3 Mesembryanthemum crystallinum, which lack the dikinase. Label from [2-14C]- and [3-14C]pyruvate is converted to carbohydrate at the same rate in K. daigremontiana while in S. gigantea label from [2-14C]pyruvate accumulates in carbohydrates twice as rapidly as label from [3-14C]pyruvate. The patterns observed for K. daigremontiana and for CAM M. crystallinum are consistent with the gluconeogenic anabolism of pyruvate whereas the patterns observed for S. gigantea and for C.3 M. crystallinum suggest pyruvate is oxidized possibly via the tricarboxylic acid cycle in these species. Deacidification in Aloe arborescens, a PEP carboxykinase CAM plant that also possesses NAD and NADP malic enzyme activity, was inhibited 80% by 0.1 mM 3-mercaptopicolinic acid (3-MPA), an inhibitor of PEP carboxykinase. It is thus likely that, in this species and probably also in other CAM plants with high PEP carboxykinase activities, a small proportion of the malic acid may be decarboxylated by malic enzymes. However, as 0.5 mM 3-MPA inhibited deacidification in K. daigremontiana by 40%, the inhibitor is probably only specific at low concentrations. 14CO2 fixation in the light by mesophyll cells isolated from K. daigremontiana was stimulated by 20-50% in the presence of 10 mM pyruvate, but there was no increase in 14CO2 fixation by mesophyll cells isolated from S. gigantea.



2003 ◽  
Vol 31 (3) ◽  
pp. 728-730 ◽  
Author(s):  
H.G. Nimmo

Crassulacean acid metabolism (CAM) plants exhibit persistent circadian rhythms of CO2 metabolism. These rhythms are driven by changes in the flux through phosphoenolpyruvate carboxylase, which is regulated by reversible phosphorylation in response to a circadian oscillator. This article reviews progress in our understanding of the circadian expression of phosphoenolpyruvate carboxylase kinase.



2019 ◽  
Vol 70 (22) ◽  
pp. 6611-6619
Author(s):  
Ming-He Li ◽  
Ding-Kun Liu ◽  
Guo-Qiang Zhang ◽  
Hua Deng ◽  
Xiong-De Tu ◽  
...  

Abstract Members of the Orchidaceae, one of the largest families of flowering plants, evolved the crassulacean acid metabolism (CAM) photosynthesis strategy. It is thought that CAM triggers adaptive radiation into new niche spaces, yet very little is known about its origin and diversification on different continents. Here, we assess the prevalence of CAM in Dendrobium, which is one of the largest genera of flowering plants and found in a wide range of environments, from the high altitudes of the Himalayas to relatively arid habitats in Australia. Based on phylogenetic time trees, we estimated that CAM, as determined by δ 13C values less negative than –20.0‰, evolved independently at least eight times in Dendrobium. The oldest lineage appeared in the Asian clade during the middle Miocene, indicating the origin of CAM was associated with a pronounced climatic cooling that followed a period of aridity. Divergence of the four CAM lineages in the Asian clade appeared to be earlier than divergence of those in the Australasian clade. However, CAM species in the Asian clade are much less diverse (25.6%) than those in the Australasian clade (57.9%). These findings shed new light on CAM evolutionary history and the aridity levels of the paleoclimate on different continents.



GigaScience ◽  
2020 ◽  
Vol 9 (3) ◽  
Author(s):  
Jin Zhang ◽  
Rongbin Hu ◽  
Avinash Sreedasyam ◽  
Travis M Garcia ◽  
Anna Lipzen ◽  
...  

Abstract Background Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. Results Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m–2 s–1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m−2 s−1) of white light to a high light treatment (1,000 μmol m–2 s–1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. Conclusions This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.



2020 ◽  
Vol 127 (1) ◽  
pp. 135-141
Author(s):  
Jacob S Suissa ◽  
Walton A Green

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.



Planta ◽  
1980 ◽  
Vol 147 (5) ◽  
pp. 477-484 ◽  
Author(s):  
C. Schnarrenberger ◽  
D. Gro� ◽  
Ch. Burkhard ◽  
M. Herbert


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