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Variations in Δ C Rates and Crassulacean Acid Metabolism of Six Coleus Species

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Variations in Δ C Rates and Crassulacean Acid Metabolism of Six Coleus Species British Journal of Applied Science & Technology 6(3): 295-303, 2015, Article no.BJAST.2015.088 ISSN: 2231-0843 SCIENCEDOMAIN international www.sciencedomain.org Variations in 13C Rates and Crassulacean Acid Metabolism of Six Coleus species G. V. Ramana1 and K. V. Chaitanya1* 1Department of Biotechnology, GITAM Institute of Technology, GITAM University, Visakhapatnam-530045, India. Authors’ contributions This work was carried out in collaboration between both authors. Both authors contributed equally for this study. Authors affirm that this work is in genuine. Both authors read and approved the final manuscript. Article Information DOI: 10.9734/BJAST/2015/14099 Editor(s): (1) Teresa De Pilli, Department of Science of Agriculture of Food of Environnement (SAFE), University of Foggia, Italy. (2) Harry E. Ruda, Centre for Advanced Nanotechnology, University of Toronto, Canada. Reviewers: (1) Chunsong Bao, Hangzhou Botanical Garden, Zhejiang Province, P. R. China. (2) Anonymous, Brazil. Complete Peer review History: http://www.sciencedomain.org/review-history.php?iid=766&id=5&aid=7347 Received 18th September 2014 Accepted 5th November 2014 Original Research Article th Published 16 December 2014 ABSTRACT Photosynthetic adaptations and biomass productivity of six Coleus species namely Coleus aromaticus, spicatus, blumei, zeylanicus, forskholii, and ambonicus were studied by determining their photosynthetic rates, Crassulacean acid metabolism (CAM) and carbohydrate levels. CAM metabolism was investigated by studying the activities of phosphoenol pyruvate carboxylase (PEPC), PEP carboxykinase and diurnal fluctuations of malate dehydrogenase along with levels of total organic acids, malic acid and citric acids. Carbohydrates such as sucrose, starch, glucose and fructose were assayed spectrophotometrically. Significant differences among the six Coleus species were observed in photosynthesis levels and CAM metabolic pathway enzymes whose activities were correlated with the aerial biomass. Our study indicates that Coleus is a CAM plant with nicotineamine Adenine Di nucleotide (Phosphate) (NAD (P)) as a preponderant malic enzyme and diurnal fluctuations in the levels of carbohydrates reveals that Coleus utilizes reservoir of starch for the synthesis of malic acid. Δ13C accumulation is more in Coleus aromaticus and ambonicus whose aerial biomass values are also high indicating the correlation between carbon fixation and biomass accumulation. _____________________________________________________________________________________________________ *Corresponding author: E-mail: [email protected]; Ramana and Chaitanya; BJAST, 6(3): 295-303, 2015; Article no.BJAST.2015.088 Keywords: Aerial biomass; CAM path way; carbohydrates; Coleus species; photosynthetic carbon fixation; organic acids. ABBREVIATIONS CAM: Crassulacean Acid Metabolism; PEPC: Phosphoenol Pyruvate Carboxylase; PEPCK: Phosphoenol Pyruvate Carboxykinase; MDH: Malate Dehydrogenase; NAD(P): Nicotineamine Adenine Dinucleotide (phosphate). 1. INTRODUCTION zeylanicus are aromatic perennial herbs that are native to Indonesia. C. aromaticus is used for Crassulacean Acid Metabolism (CAM) is one of chronic cough and asthma. It is considered to be the three forms of the photosynthetic carbon antispasmodic, stimulant and stomachic and is assimilation and is considered as one of the used for the treatment of headache, fever, important models for probing the evolution of epilepsy and dyspepsia. Coleus blumei is a complex traits in response to changing perennial native to Java, but now spread over environment [1]. CAM form of carbon many parts of tropical Africa, Europe and Asia, assimilation has been characterized in 16,000 popular as an ornamental plant. Coleus species of 328 genera in 33 families including forskohlii, an Indian herb, produces the labdane Crassulaceae, Lamiaceae, Polypodiaceae etc. diterpenoid forskolin in its tuberous roots, which [2]. The mechanism of CAM is typically has been shown to be a hypertensive agent with characterized by the acquisition of nocturnal CO2 spasmolytic, cardiotonic and platelet aggregation via protein kinase activated phosphoenol inhibitory activity, antiglaucomic in nature and a pyruvate carboxylase (PEPC), leading to the potent stimulator of the enzyme adenylate formation of organic acids mainly malic acid, cyclase, which increases the levels of cAMP which are stored in the large central cell sap affecting cardiac muscle contraction, blood and vacuoles. In the subsequent light period, organic intraocular pressure, cancer, eczema, acid is released from the vacuole, rheumatism and obesity [7]. The medicinal decarboxylated to release CO2 for assimilation in properties of this plant have been well studied the Calvin cycle behind closed stomata [3]. but the photosynthetic performance of this CAM Based on the differences in the decarboxylation plant was not studied. Previous studies have of malic acid, three subtypes of CAM plants are mentioned the role of environment on gas known, NAD-ME type, NAD(P)-ME type and exchange and CAM mechanisms of Plectranthus PEPCK type [4]. CAM plants perform nocturnal marrubioides, P. parviflorus and P. prostratus recycling of CO2 through malic acid for the (Lamiaceae) [8,9]. Here, we report the purpose of photosynthesis. photosynthesis and CAM mechanisms of six Coleus species, C. aromaticus, C. spicatus, C. CAM plants possess high efficiency in water blumei, C. zeylanicus, C. forskholii, and C. utilization by losing 50-100g of water per 1g of ambonicus and their aerial biomass levels. CO2 fixed in comparison to the 250-300g of water Characterizing the Coleus species depending on by the C4 and 400-500 gm of water by the C3 the mechanism of CAM photosynthesis, which plants respectively [5]. CAM plants contain utilizes either malate or PEPCK and identification scotoactive stomata, which opens during night of starch or sucrose carbohydrate reservoir pool facilitating the CO2 leading to reduce utilized for the carbon fixation, are few of the photorespiration. CAM plants are also provided important aspects of the present study. with various morphological, anatomical features such as thick cuticles, low surface-to-volume 2. MATERIALS AND METHODS ratios, large cells and vacuoles with enhanced water storage capacity (succulence), reduced 2.1 Plant Material and Growth Conditions stomatal size and frequency, which minimizes water loss [6]. Six Coleus species namely C. aromaticus, C. spicatus, C. blumei, C. zeylanicus, C. forskholii, Coleus (Lamiaceae) is an important plant used and C. ambonicus were propagated in the traditionally in folk medicine in India due to its GITAM University botanical garden, potential medicinal value as an expectorant, for Visakhapatnam, India in 30 cm pots under 12h the treatment of bronchitis, eczema and natural photoperiod [1600-1800 µ moles m-2 s-1] rheumatism. Coleus aromaticus and Coleus with day/night temperatures of 30C/23C and 296 Ramana and Chaitanya; BJAST, 6(3): 295-303, 2015; Article no.BJAST.2015.088 approximate relative air humidity of 60%. The oxaloacetic acid, 10 µM of MgCl2, 0.4 µM NADH plants were well watered with normal tap water. and 0.2 ml of enzyme extract. Five pots were used for each Coleus species and PEPCarboxykinase (EC 4.1.1.49) was assayed one plant is grown per pot. Third or fourth fully spectrophotometrically [13]. Carboxylation expanded leaf from the top of the 3-month-old activity was measured following the oxidation of plant was collected for all physiological NADH by malate dehydrogenase at 340 nm experiments and aerial biomass measurements using 100 mM HEPES (pH 7.0), 4% 2-mercapto made by measuring the mass of the above ethanol, 100 mM KCl, 90 mM KHCO3, 5 mM ground plant. PEP, 1 mM ADP, 10 m MnCl2,4 mM MgCl2, 0.14 mM NADH and 6 units of malate 2.2 Carbon Isotope Determination dehydrogenase. Samples were prepared by drying the Coleus NAD-ME (EC 1.1.1.38) was assayed leaves in a hot air oven at 80°C for 72h. spectrophotometrically at 340 nm [14] using 5mM Completely dried leaves were grinded into fine malate, 25mM HEPES- KOH of pH 7.2, 2 mM powder in a mortar with pestle. 2 mg dry powder NAD, 2.5 mM MnCl2, 5mM DTT and 500 µM of each Coleus species leaf was subjected in the fructose bis phosphate and 0.2 ml enzyme Flash Elemental Analyzer (NA 1112, Carlo Erba, extract in a volume of 1 ml assay mixture. NADP- Italy) interfaced to an Isotope Ratio Mass ME (EC 1.1.1.40) was assayed Spectrometer (IRMS; Delta-Plus, Thermo- spectrophotometrically at 340 nm [15]. Assay Finnigan, Bremen, Germany) via a continuous mixture contained 50 mM Tris-HCl (pH 7.3), 10 flow device (Conflo-III). The carbon isotopic mM MgCl2, 0.5 mM NADP and 10 mM l-malate 13 composition of plant samples ( Cp) was with 0.2 ml of enzyme extract. determined with an analytical precision of less than 0.1. Carbon isotope discrimination (Ä 2.4 Titratable Acidity, Malic Acid and 13C) was computed according to [10] assuming Citric Acid Contents the isotopic composition of atmospheric air 13 Day and night oscillations of titratable acidity ( Ca) to be –8. were measured using fully expanded Coleus 13 13 13 13 leaves collected during 8 A.M. and 8 P.M. [16]. C (‰) = [ Ca – Cp]/[1 + Cp/1000]. 1g of leaf tissue was cut into small pieces, boiled 2.3 Extraction and Assay of Enzymes in a beaker with 50 ml of distilled water for 30 minutes and the slurry was filtered. 2.5 ml of extract was neutralized with 5 ml of 1N NaOH for All extractions were performed at 4°C. The leaf 15 minutes and 1 drop of phenolphthalein was blades (10 g) were homogenized in a grinding added. The contents were titrated against 1N medium consisting of 100 mM Tris-HCl (pH 7.8), HCl till the solution becomes colour less [17]. 5 mM DTT, 10 mM MgCl2, 1 mM EDTA, 5 mM magnesium acetate and 1.5% PVP at 4C. The Content of malic acid was determined according homogenate was squeezed through four layers to [18]. 1 gram leaf sample was homogenized in of cheesecloth and then centrifuged at 10000 g a mortar and pestle with 0.6N perchloric acid. for 10min. The solution was filtered to remove The sample was centrifuged at 15000g for 5 the cellulose and washed thrice with the minutes.
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