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Official websites use. Share sensitive information only on official, secure websites. Correspondence: luisa. The chemical profile of the female inflorescence extracts from seven Cannabis sativa L. The NMR metabolite profile sugars, organic acids, amino acids, and minor compounds subjected to principal components analysis PCA showed a strong variability according to the harvesting stages: samples harvested in stage I were characterized by a high content of sucrose and myo-inositol, whereas the ones harvested in stage II showed high levels of succinic acid, alanine, valine, isoleucine, phenylalanine, and threonine. Samples harvested in stage III were characterized by high levels of glucose, fructose, choline, trigonelline, malic acid, formic acid, and some amino acids. The ratio between chlorophylls and carotenoids content indicated that all plants grew up exposed to the sun, the Eletta Campana cultivar having the highest pigment amount. Tiborszallasi cultivar showed the highest polyphenol content. The highest antioxidant activity was generally observed in stage II. All these results suggested that the Cannabis sativa L. This information could be useful for producers and industries to harvest inflorescences in the appropriate stage to obtain samples with a peculiar chemical profile suitable for proper applications. Keywords: industrial hemp, dioecious cultivars, inflorescences, phenological growth stages, cannabinoids, metabolite profile, antioxidant activity, multimethodological analysis. Cannabis sativa L. From a taxonomic point of view, different classifications of Cannabis sativa L. Industrial hemp is a fiber-type Cannabis sativa L. In Italy, the second greatest hemp producer in the world after Russia \[ 3 \], hemp cultivation almost disappeared due to legislative restrictions and the economic crisis. These cultivars are listed in an official European database \[ 5 \], and their THC content is constantly monitored. Following the European guidelines, Italy has started a process for the valorization of hemp cultivation and applications, and in , the Lazio Region Central Italy approved a new regulation to enhance the reintroduction and the growth of C. In this scenario, the necessity of a better characterization and development of local Cannabis sativa L. Cannabis inflorescences have been traditionally considered as a waste product in the industrial field but, in the last years, the interest for this part of the plant increased exponentially, mainly for the extraction of cannabinoids and essential oils \[ 6 , 7 , 8 \]. The chemical composition of hemp inflorescences can be affected by several factors such as genotype, pedoclimatic conditions, agronomical practices, and harvesting time \[ 9 , 10 , 11 , 12 \]. Cannabis is naturally a dioecious cultivar; namely, the male and female flowers are presented on different plants: pollination occurs with the wind. Monoecious Cannabis cultivars are also obtained through breeding selection. The dioecious ones are mainly used for fiber production, whereas the monoecious ones for seed production \[ 13 , 14 \]. In a previous paper \[ 12 \], the chemical composition of the inflorescences from four Cannabis sativa L. In this paper, the proposed protocol was extended to dioecious female inflorescences of seven Cannabis sativa L. Targeted methodologies, namely ultra-high-performance liquid chromatography UHPLC and spectrophotometry, were applied to analyze and to monitor cannabinoids, natural pigments, and total phenolics, as well as to evaluate the antioxidant activity of the inflorescences extracts. The seasonal time trend of sugars, amino acids, organic acids, and minor compounds was monitored using untargeted NMR spectroscopy, a very powerful tool to investigate the metabolite profile of vegetable matrices \[ 17 , 18 \]. Targeted and untargeted methodologies were used to determine the chemical profile of the inflorescences extracts at three harvesting stages 4 September, 14 September, and 30 September. Analyses were carried out in triplicate. The chloroform extracts of Cannabis sativa L. Carmagnola; b vs. Fibranova; c vs. Kompolti; d vs. Tisza; e vs. Antal; f vs. Tiborszallasi; g vs. These untargeted assays were easy to perform, rapid, low-cost, and useful for achieving an overview of the antioxidant activity of the samples \[ 23 \]. Small molecules had better access to the radical site showing higher apparent antioxidant activity \[ 24 \]. Hemp inflorescences exhibited high variability in antioxidant activity and total phenolic content. The NMR profile of hydroalcoholic Bligh—Dyer inflorescences extracts was obtained by using literature data \[ 12 \]. Six sugars, six organic acids, thirteen amino acids, choline, and trigonelline were quantified at the three harvesting stages, and used for multivariate PCA, see Figure 1. In Table 4 , the quantified metabolites in hydroalcoholic Bligh—Dyer extracts are listed, together with the chemical shift ppm of the signals used for quantification. The first two PCs accounted for PCs score plots showed a sample groping according to the harvesting stages. The contribution of the variables to this grouping given by the variable loadings reported in Figure 1 B was discussed in detail in the Discussion paragraph. Trends of metabolite profiles during the three harvesting stages were discussed separately for each cultivar. Finally, a comparison among cultivars was also reported. CBD, the main cannabinoid, showed a gradual increase over the three different harvesting stages, reaching its maximum in stage III. Free amino acids. Asparagine was found to be the main amino acid in hemp inflorescences. Valine, glutamic acid, and proline showed an opposite trend. Glutamine content was quite constant in the first two harvesting stages and then slightly increased, whereas phenylalanine and isoleucine slightly decreased in stage III. Alanine and tryptophan concentrations were always constant. Free amino acids content in hydroalcoholic extracts of Cannabis sativa L. Sucrose, glucose, and fructose were the main sugars in hemp inflorescences. Glucose and fructose remained quite constant. Myo-inositol content was constant in the first two stages and then doubled. Sugars A , organic acids B , and miscellaneous compounds C content in hydroalcoholic extracts of Cannabis sativa L. Organic acids. Malic acid increased over time, whereas succinic acid increased until stage II and then drastically decreased Figure 3 B. Formic acid was constant in the first two stages and then slightly increased. Miscellaneous compounds. Trigonelline and choline increased over time Figure 3 C. Chlorophyll a, chlorophyll b, and total carotenoid contents decreased over time Table 2. Total phenolics and antioxidant activity. THCA was never detected in all stages considered. Asparagine, glutamine, proline, and glutamic acid contents increased over time Figure 2. All the other amino acids analyzed reached their highest content in stage II. Sucrose and myo-inositol decreased during the time, whereas glucose showed an opposite trend. Fructose content was constant over time Figure 3 A. The highest content of malic acid was measured in stage II, whereas succinic acid decreased over time. Formic acid slightly increased in stage II and then remained constant Figure 3 B. Choline and trigonelline concentrations increased from stage I to stage II and then remained constant Figure 3 C. Chlorophyll a, chlorophyll b, and total carotenoids content reached their highest value in stage II. Asparagine, GABA, valine, isoleucine, threonine, phenylalanine, and tryptophan reached their highest concentrations in stage II. Conversely, in this stage, the lowest value of proline was measured. Glutamine, glutamic acid, and aspartic acid increased in stage II and remained constant Figure 2. Sucrose drastically decreased over time Figure 3 A. Glucose and fructose slightly decreased in stage II and then increased. Myo-inositol decreased in stage II and then remained quite constant. Malic acid slightly increased from stage I to stage II and then drastically decreased. Succinic and formic acids reached their highest content in stage II. Figure 3 B. Both choline and trigonelline reached their highest amount in stage II. Figure 3 C. Total phenolics and antioxidant activi ty. Asparagine, valine, threonine, phenylalanine, and tryptophan reached their highest contents in stage II, whereas proline, glutamic acid, and isoleucine slightly decreased over time Figure 2. Glutamine and aspartic acid amounts were quite constant until stage II and then slightly increased. GABA increased in stage II and then remained constant, whereas the alanine amount was constant until stage II and then slightly decreased. Sucrose content drastically decreased over time, whereas glucose had an opposite trend Figure 3 A. Fructose content was constant until stage II and then increased, whereas myo-inositol content decreased in stage II and then increased. Malic acid and formic acid contents were constant until stage II, then decreased and increased, respectively. Succinic acid amount was the highest in stage II Figure 3 B. Trigonelline content increased in stage II and then remained constant, whereas choline increased over time. However, both ratios were typical of sun-exposed plants. Asparagine, GABA, glutamic acid, and aspartic acid slightly increased over time, whereas alanine had an opposite trend. Glutamine, proline, and tryptophan slightly decreased in stage II and then increased, whereas valine, isoleucine, and phenylalanine reached their highest content in stage II Figure 2. Threonine remained constant until stage II and then decreased. Sucrose content drastically decreased over time, whereas glucose slightly increased Figure 3 A. Fructose and myo-inositol remained constant until stage II and then increased and decreased, respectively. Malic and succinic acids decreased over time, whereas formic acid slightly decreased in stage II and then increased Figure 3 B. Trigonelline content was quite constant over time, whereas choline slightly increased. Chlorophyll a and total carotenoids content decreased over time, whereas chlorophyll b remained constant in the first two stages and then decreased. Asparagine, glutamine, aspartic acid, and tryptophan increased over time, whereas threonine had an opposite trend Figure 2. Proline and glutamic acid reached their lowest content in stage II. Conversely, in this stage, the highest concentrations of GABA, alanine, valine, isoleucine, and phenylalanine were found. Sucrose, glucose, and myo-inositol concentrations decreased over time, whereas fructose had an opposite trend Figure 3 A. Malic and formic acids increased over time, whereas succinic acid had an opposite trend Figure 3 B. Trigonelline increased in stage II and then remained constant. Choline slightly increased over time Figure 3 C. Asparagine and glutamine increased over the stages, whereas alanine and threonine showed an opposite trend Figure 2. Proline, glutamic acid, valine, isoleucine, and tryptophan contents decreased in stage II and then increased. GABA, aspartic acid, and phenylalanine amounts remained quite constant over time. Sucrose and myo-inositol decreased over time, whereas glucose increased until stage II and then remained constant Figure 3 A. Fructose content had its highest concentration in stage II. Malic acid content slightly decreased in stage II and then increased, whereas succinic acid remained quite constant during the three stages Figure 3 B. Formic acid concentration remained constant until stage II and then increased. Trigonelline and choline increased over time. Chlorophyll a, chlorophyll b, and total carotenoids decreased over time Table 3. However, the ratio values in all the stages were indicators of the light exposition of the plant. The cannabinoids content of the seven investigated cultivars Carmagnola, Fibranova, Kompolti, Tisza, Antal, Tiborszallasi, and Eletta Campana revealed common features but also important differences. In all the analyzed cultivars, the THC content was always under the legal limit, including Carmagnola, Fibranova, and Antal cultivars that, in , were excluded from the European Plant Database because of the variable THC content. As expected for the fiber-type chemotype, CBD was found to be the most abundant cannabinoid, with the highest concentration measured in Kompolti cultivar in stage II 5. In another study, the THC and CBD contents in hexane extracts of Kompolti air-dried inflorescences grown in Austria \[ 28 \] were reported being at least two times lower than those observed in the same cultivar in the present study. However, no indication regarding the harvesting stage was reported, making it difficult for comparison. The spectrophotometric analysis of chlorophylls and total carotenoids showed that chlorophyll a was always more abundant with respect to chlorophyll b, underlining the major involvement of chlorophyll a in the photosynthetic process. The maximum content of chlorophyll a, chlorophyll b, and total carotenoids was observed in stage I or stage II, depending on the cultivar. Conversely, regardless the cultivar, the lowest concentrations of the analyzed pigments were always found in stage III. Among the cultivars, Eletta Campana cultivar was characterized by the highest values of all the analyzed pigments in all the harvesting stages, whereas Tiborszallasi cultivar showed the opposite trend. It was noteworthy that the quantitative trend of chlorophylls and carotenoids during the considered stages was strictly correlated. In particular, an increase in chlorophylls generally coincided with an increment of carotenoids, too, although with different rates. This correlation could be explained since chlorophylls and carotenoids synthesis were characterized by common pathways \[ 29 , 30 \]. Regarding the total phenolic content, the lowest TPC value was measured in Fibranova in stage I, whereas the highest one was detected in Tiborszallasi in stage II. The TPC results suggested a different behavior of the investigated cultivars. Carmagnola and Kompolti, indeed, had a decrement in the last harvesting stage. Antal cultivar showed a unique trend, with a decrease in TPC values during the three harvesting stages. Kompolti presented a different trend for the antioxidant activity tests; in the DPPH assay, its trend was the same as the Antal cultivars, whereas, in the ABTS assay, the trend was that of the other cultivars. However, since the sample treatment, the extraction procedure, and the expression of the results were different from those of the present work, and it was not possible to make a comparison. Among the analyzed classes of compounds, polyphenols were, of course, involved in the antioxidant activity of hydroalcoholic hemp extracts since this activity was well recognized for these compounds \[ 32 , 33 \]. In particular, hemp inflorescences showed to be characterized by phenolic acids and flavonoids as the main polyphenolic compounds \[ 31 , 34 \]. Since the chemical profile of hemp inflorescences was very complex, it could be not easy to correlate the antioxidant activity trend of hemp extracts with that of specific chemical compounds, which was also shown by literature data \[ 37 \]. In fact, the Pearson correlation coefficient Table S1 not always showed a strong correlation between TPC and antioxidant activity assays. However, it could be supposed that polyphenols and cannabinoids were strongly involved in the antioxidant activity of hemp inflorescences, which was supported by the obtained results. In particular, for the analyzed cultivars, the highest antioxidant activity was generally observed in stage II, as well as the content of cannabinoids and total polyphenols. Moreover, Antal cultivar, whose antioxidant activity was higher in stage I, was also characterized by the highest contents of polyphenols and cannabinoids, particularly CBD, in this period. As for the metabolite profile of hemp inflorescences, it was possible to observe analogies and differences among cultivars and harvesting stages. Malic acid was the main organic acid, with the highest concentration measured in Kompolti cultivar in stage III. These metabolites can affect the sensorial properties of hemp infusions and beverages that can be used for food or pharmacological purposes \[ 38 \]. The PCA analysis of NMR data showed that in general, regardless of the cultivar, metabolite profiles could be differentiated owing to the harvesting stage. In particular, samples harvested in stage I were characterized by high contents of sucrose and myo-inositol, whereas the ones harvested in stage II showed higher levels of succinic acid, alanine, and essential amino acids. Samples harvested in stage III were distinguished by high levels of monosaccharides, choline, trigonelline, malic acid, formic acid, and some amino acids. In a previous work \[ 12 \], the NMR metabolite profile of four monoecious hemp cultivars was determined by using the same analytical protocol of the present work. Comparing the quantitative results obtained for both monoecious and dioecious cultivars in September considering the 14 September data for the present work , it was possible to observe that the two groups presented peculiar metabolites Figure S1. In particular, higher levels of fructose, formic acid, malic acid, choline, and trigonelline were observed in monoecious cultivars, whereas dioecious cultivars were characterized by higher amounts of glucose and some amino acids: valine, threonine, alanine, and asparagine. For instance, mid-September harvesting stage II was the most effective to obtain high concentrations of CBD and polyphenols; suggesting this harvesting stage as the main effective to obtain inflorescences with high pharmaceutical and nutraceutical properties. However, for Antal cultivar, the proper period to obtain inflorescences rich in bioactive compounds was early September stage I. Moreover, secondary metabolites, such as sugars and organic acids, could affect the sensorial properties of hemp-based products, such as infuses. In this context, the Tisza cultivar was characterized by high levels of sugars in stage I and stage III harvesting periods, whereas Kompolti was particularly rich in malic acid in stage III. Gradient grade water, acetonitrile, chloroform, methanol, and formic acid were purchased from Merck Life Science Milano, Italy. Deuterated water D 2 O Fresh inflorescences of seven dioecious female Cannabis sativa L. They were grown in experimental fields located in the North Lazio area Italy, Rome during the cultivation year. The same agronomical practices, previously described in \[ 12 \], were used for plant cultivation. The inflorescences sampling was carried out by applying the following systematic pattern: for each cultivar, 25 plants were collected in the central part of the cultivation area by cutting the upper part 30 cm of the stem. Analyzes were carried out within ten days of storage. After drying, mg of inflorescences were extracted with 4 mL of methanol \[ 39 , 40 \] in an ultrasonic bath for 30 min. The residual pellet was re-extracted again two times. Each extract was then filtered under vacuum conditions, diluted to 5 mL with methanol, filtered with a 0. Analyses were carried out by using an Ultimate ultra-high-performance liquid chromatography UHPLC; Thermo Fisher Scientific Rodano, Italy , with a binary gradient system, an automatic injector, a thermostatic column compartment, and a diode array detector. The flow rate was 0. The PDA detector was set to nm wavelength. Regression lines were calculated using the least squares method, and linearity was expressed by the determination coefficient R 2. For each calibration curve, the R 2 value was always greater than 0. Three replications were made for each sample. For the untargeted analysis, the fresh plant material was extracted by using the Bligh—Dyer protocol \[ 41 \] already described in detail \[ 12 \]. The dried hydroalcoholic extracts were solubilized in 0. Spectra were processed using TopSpin software version 4. For quantitative analysis, the integrals of the corresponding selected resonances in 1 H NMR spectra Table 2 were measured with respect to the internal standard TSP, allowing the molar concentration and the corresponding weight to be calculated. The amount of each metabolite was expressed as weight percentage with respect to the total weight of all quantified metabolites. Each sample was extracted and analyzed three times. Before the analysis, the selected variables were processed using autoscaling and then mean centered. The organic phase, which contained chlorophylls and carotenoids, was separated from the hydroalcoholic one and then analyzed. The absorbance values measured at , , and were considered. The extraction of phenolic compounds was carried out following a protocol previously described \[ 45 \], with some modifications. In particular, 0. After centrifugation, the supernatant was separated from the residual pellet that was extracted again using the same conditions described above. Supernatants obtained in both extractions were united, obtaining a final volume of 5 mL. Total phenolics content TPC was determined using the Folin—Ciocalteu method \[ 45 \], optimizing the protocol for hemp inflorescences: 1 mL of hydroalcoholic extract was added to 0. Each sample was stored in the dark for 45 min at room temperature, and the spectrophotometric analysis Lenway UV-Vis spectrophotometer Milan, Italy was performed at nm. For the DPPH assay, 1. After 30 min, the absorbance of the solution was recorded. For the ABTS assay, 3. After 15 min the absorbance of the solution was recorded. The reduction of radical concentration was evaluated by measuring the absorbance at nm for DPPH assay and nm for ABTS assay , as previously reported \[ 45 \]. Pearson correlation coefficients were also evaluated and reported in Table S1. The present study showed that the Cannabis sativa L. The following are available online. Figure S1. PCA maps obtained comparing September inflorescences samples of monoecious and dioecious Cannabis sativa L. Table S1. Pearson correlation coefficient r between total polyphenolic compounds and antioxidant activity. Conceptualization, M. Silvia Cammarone , S. Salvatore Ciano , G. Salvatore Ciano , A. All authors have read and agreed to the published version of the manuscript. This work was realized with funds received from the following agencies: the Italian Ministry of Education, Universities, and Research—Dipartimenti di Eccellenza—L. This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. A Multimethodological Characterization of Cannabis sativa L. Find articles by Mattia Spano. Find articles by Giacomo Di Matteo. Find articles by Cinzia Ingallina. Find articles by Bruno Botta. Find articles by Deborah Quaglio. Find articles by Francesca Ghirga. Find articles by Silvia Balducci. Find articles by Silvia Cammarone. Find articles by Enio Campiglia. Find articles by Anna Maria Giusti. Find articles by Giuliana Vinci. Find articles by Mattia Rapa. Find articles by Salvatore Ciano. Find articles by Luisa Mannina. Find articles by Anatoly P Sobolev. Severina Pacifico : Academic Editor. Open in a new tab. Compound ppm Compound ppm Isoleucine 1. Click here for additional data file. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Eletta Campana.

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