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Article

Alkaloid and Nitrogenated Compounds from Different Sections of Coryphantha macromeris Plants and Callus Cultures

by
Valeria Viera-Escareño
1,
Eugenio Perez-Molphe Balch
2,
Yenny Adriana Gómez-Aguirre
2,3,
Oscar Javier Ramos-Herrera
1,
Gholamreza Abdi
4,
Francisco Cruz-Sosa
5,* and
Emmanuel Cabañas-García
6,*
1
Unidad Profesional Interdisciplinaria de Ingeniería Campus Zacatecas, Instituto Politécnico Nacional, Blvd. del Bote 202 Cerro del Gato, Ejido La Escondida, Col. Ciudad Administrativa, Zacatecas 98160, Mexico
2
Departamento de Química, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Av. Universidad 940, Aguascalientes 20100, Mexico
3
CONACyT Research Fellow—Departamento de Química, Centro de Ciencias Básicas, Universidad Autónoma de Aguascalientes, Av. Universidad 940, Aguascalientes 20100, Mexico
4
Department of Biotechnology, Persian Gulf Research Institute, Persian Gulf University, Bushehr 75169, Iran
5
Departamento de Biotecnología, Universidad Autónoma Metropolitana, Campus Iztapalapa, Ferrocarril de San Rafael Atlixco 186, Mexico City 09310, Mexico
6
Centro de Estudios Científicos y Tecnológicos No. 18, Instituto Politécnico Nacional, Blvd. del Bote 202, Zacatecas 98160, Mexico
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2023, 13(17), 9947; https://doi.org/10.3390/app13179947
Submission received: 28 June 2023 / Revised: 22 August 2023 / Accepted: 24 August 2023 / Published: 2 September 2023
(This article belongs to the Special Issue Advances in Biological Activities of Natural Products)
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Abstract

:
One of the distinctive characteristics of cacti species is the presence of alkaloids. Alkaloids are nitrogenated molecules with hallucinogenic and pharmacological properties in humans and other animals. Plant cell, tissue, and organ culture have emerged as an effective tool for investigating the biosynthesis of a variety of functional metabolites and for studying the preservation of endangered plant species. In this study, we examined the alkaloid and nitrogenated compound profiles of the aerial and radicular sections of Coryphantha macromeris plants that were cultivated in both greenhouse and in vitro conditions. Additionally, we analyzed the callus cultures generated from stem discs. To perform these analyses, Ultra-High-Performance Liquid Chromatography coupled with High-Resolution Mass Spectrometry (UHPLC-PDA-HESI-Orbitrap-MS/MS) was utilized. Under the working parameters, 78 compounds were detected, and 61 of them were identified. Among the identified compounds, the in vitro plants presented 24 compounds, greenhouse plants a total of 21 compounds, and callus tissue 16 compounds. On the other hand, 7 compounds (laurydiethanolamine, toluic acids, and their derivatives) were detected in all systems, suggesting that these metabolites may serve as markers to help find the authenticity of C. macromeris preparations, and that, plant and cell-tissue cultures with this plant species are suitable for the biosynthesis of the selected compounds. In addition, our research suggests that no alkaloids with reported psychotropic properties are present in C. macromeris.

1. Introduction

Secondary plant metabolites are compounds synthesized as a passive chemical defense mechanism induced by the ecological interactions between the plant and its environment. Among the secondary metabolites, phenolic compounds, terpenes, flavonoids, coumarins, and alkaloids contribute to plant adaptation and survival [1]. Plant species are traditionally employed for healing different diseases, and they represent a source for investigating culture technologies and the studying of bioactive metabolites [2,3,4,5,6,7,8]. Among bioactive metabolites, phenolics and alkaloids are two classes of secondary metabolites with recognized pharmacological properties; hence, plant species that contain alkaloids impact human health, including cacti species [9]. In this regard, the research on cacti species has increased in the last few years since these are plants that can easily adapt to harsh environments and have demonstrated functional properties [10,11,12,13,14,15,16,17].
Alkaloids are nitrogenated molecules with hallucinogenic, addictive, stimulant, and pharmacological properties in humans and animals. Therefore, cacti species that contain them are commonly used as therapeutic agents and diagnostic means in shamanic practices and traditional medicine, as is the case of Lophophora diffusa (Peyote) [18] and Echinopsis spp. (cactus de San Pedro) [19], which contains mescaline. In this regard, it has been proposed that mescaline is one of the main active compounds in Echinopsis spp., and that the highest concentration is mainly found in the chlorenchymatic layer [19,20]. Furthermore, it has been proposed that the mescaline content in different Echinopsis species varies from 0.053 to 4.7% of dry-weight biomass [19], directly correlating with the most used plants in traditional medicine and their alkaloid content. In this regard, El-Seedi et al. [21] detected the presence of mescaline (~2%) in the archaeological samples of Lophophora williamsii (peyote) located in Rio Grande, Texas by finding, through radiocarbon dating studies, that the samples correspond to the years 3780–3660 BC, which suggests that the native inhabitants could have used them, recognizing their psychotropic properties.
Recent studies dealing with the identification of alkaloids or nitrogenated compounds in cacti species are scarce; for instance, Brown et al. [22] evaluated the presence of alkaloids in 16 species of cacti belonging to different genera collected in different regions and at different seasons of the year of the southern United States (Dallas and Texas). They found that the species belonging to the genera Carnegiea, Lemaireocereus, Trichocereus, Selenicereus, Echinocereus, Echinomastus, Echinocactus, Ferrocactus, Neomammiliaria, and Coryphantha contained alkaloids, suggesting that different cacti species contain complex nitrogenated molecules. Similarly, in a series of papers, Starha [23], Starha et al. [24], and Starha et al. [25] evaluated the presence and content of alkaloids in Gymnocalycium and Turbinicarpus species, thereby finding that the concentration of nitrogenated compounds varies according to the plant species and that hordenine is present in higher concentrations in most of the analyzed species, followed by tyramine, thus suggesting that this may correspond to one of the main alkaloids in Gymnocalycium and Turbinicarpus species. These findings are similar to those reported by Follas et al. [26], who analyzed six species from the Lobivia genus (L. allegriana, L. aurea, L. backebergii, L. binghamiana, L. huashua, and L. pentlandii) and one species of the genus Pseudolobivia, which obtained from different sources in California and Arizona, USA. There, they found that hordenine was in higher concentrations for the species of the Lobivia genus, and that 3,4-dimethoxy-β-phenylethylamine and tyramine was higher for P. kermesina. This information also suggests that each species has a different genetic capacity through which to biosynthesize and accumulate alkaloids, and that the region (through variety in altitude, latitude, and rainfall) could affect the accumulation pattern of metabolites.
One strategy for the propagation of plants without environmental constraints is in vitro culture technology. In vitro technology includes different methodologies such as plant cell, tissue, and organ culture. Under in vitro conditions, plants are propagated in sterile and homogeneous conditions that contribute to the conservation of endangered species [27,28,29]. For in vitro derived plants and cells, it has been demonstrated that the obtained biomass has the biosynthetic capacity for producing most of the bioactive metabolites present in mother plants [30], and that the accumulation of compounds can be enhanced by using elicitor or precursor feeding treatments [3,31].
For Coryphantha species, reports dealing with the alkaloid profiles are scarce. In traditional practices, it has been proposed that different Coryphantha species has hallucinogenic properties; nevertheless, reports existing in the literature dealing with this topic are scarce. In previous reports, we have demonstrated the presence of phenolic compounds in the plant and cell cultures of Coryphantha macromeris [32,33,34], thereby finding that cells can produce a variety of phenolic compounds; in that series of papers, the alkaloid hirtioerectine C was identified; nevertheless, the generated information supports the use of the plant for medicinal purposes. Nevertheless, it has also been proposed that this plant species is collected due to its hallucinogenic properties. In this study, we aimed to deepen the knowledge of C. macromeris; thus, we performed experiments to analyze the presence of alkaloids and nitrogenated compounds in the aerial and radicular sections of C. macromeris plants obtained from different conditions, namely in vitro plants and greenhouse plants. Additionally, the callus tissue was also analyzed after 9 weeks of culture (which is when the biomass production reaches its maximum yield, as reported previously for C. macromeris callus cultures [34]).

2. Materials and Methods

2.1. In Vitro Germination, Greenhouse Culture, and Callus Induction of C. macromeris

The cultivation of the C. macromeris plants in either greenhouse or in vitro conditions followed our previously described methods [32,33]. Briefly, for establishing the in vitro cultures, seeds were collected from the wild and were then disinfected. This involved sequential immersion in 70% ethanol (1 min), a 1.8% sodium hypochlorite aqueous solution (25 min), and sterile distilled water (4 times). The disinfected seeds were then germinated and maintained under in vitro conditions using culture vessels containing a Murashige and Skoog (MS) medium [35], which was supplemented with 30 g L−1 of sucrose and 10 g L−1 of agar (Sigma-Aldrich, St. Louis, MO, USA). The culture vessels were incubated at 25 °C, under a 16/8 (light/dark) photoperiod (40 μmol m2 s−1). The pH of all the culture media was adjusted to 5.7, and the media were then sterilized by autoclaving at 121 °C for 15 min. The generated shoots were periodically sub-cultured each three months for one year within the in vitro conditions. Subsequently, they were acclimatized to greenhouse conditions for further growth, and then used for untargeted metabolomics analysis. The acclimated plants were maintained in the greenhouse for one year before being collected for analysis.

2.2. Media Preparation and Callus Culture Conditions

The callus cultures of C. macromeris were propagated following our previously reported method [34]. The cultures were grown on a MS basal medium (Sigma-Aldrich, St. Louis, MO, USA) that contained 3% sucrose, 8 g L−1 of agar, and adjusted to a pH of 5.7. The medium was supplemented with 6-benzylaminopurine (BAP) at a concentration of 2.2 μM, and 4-Amino-3,5,6-trichloropicolinic acid (picloram) at a concentration of 4.14 μM (Sigma-Aldrich, St. Louis, MO, USA). The cultures were kept at a consistent temperature of 25 °C and a light regime at a 16/8 (light/dark) photoperiod with a photon-flux density of 40 mmol m2S−1. After a period of nine weeks, samples were gathered during the stage of peak biomass production and underwent preparation for extraction and subsequent analysis.

2.3. Sample Preparation for Untargeted Metabolomics Analysis

As previously described [34], the samples from greenhouse and in vitro cultures were dried in an oven at 40 °C (Gallenkamp, London, UK) under dark conditions. Samples were dried before being ground up in a mortar, and the resulting powder was then extracted three times in an ultrasonic bath for 30 min each time using methanol (1:3 p/v). Rotary evaporation (Heidolph Instruments, Schwabach, Germany) was used to filter and concentrate the resultant extract while operating at decreased pressure, at a temperature of 40 °C, and then freeze-dried (FreeZone 4.5; Labconco Corporation, Kansas City, MO, USA). For untargeted metabolomic analysis, the freeze-dried samples were resuspended (2.5 mg mL−1) in HPLC-Mass Spectrometry methanol.

2.4. Untargeted Metabolomics Analysis Using UHPLC-PDA-HESI-Orbitrap-MS/MS

For the untargeted metabolomic analysis, a Dionex™ UltiMate™ 3000 UHPLC system (Thermo Fisher Scientific®, based in Waltham, MA, USA) was employed. The system comprised a C18 column with dimensions of 150 × 4.6 mm, and a particle size of 5 μm (Restek Corporation, Bellefonte, PA, USA).
The system was equipped with a quaternary Series RS pump and a Dionex™ UltiMate™ 3000 Series TCC-3000RS column compartment. Furthermore, the system incorporated an UltiMate™ 3000 Series WPS-3000RS autosampler manufactured by Thermo Fisher Scientific® and a high-speed Photodiode Array Detector (PDA) for rapid separations. The PDA was configured to record detection wavelengths at 254, 280, 320, and 440 nm; for peak characterization, the PDA recorded data in the wavelength range of 200 to 800 nm. To separate the compounds, a gradient elution method was employed involving 1% formic aqueous solution (A) and acetonitrile (B). The flow rate was 1.0 mL min−1, and the injection volume was set at 10 μL. The gradient program represented as [time (min), %B] was as follows: (0.00, 5), (5.00, 5), (10.00, 30), (15.00, 30), (20.00, 70), (25.00, 70), and (35.00, 5). Before each injection, a column equilibration period of 12 min was employed.
System control was accomplished using Thermo Scientific™ Chromeleon™ 7.2 Chromatography Data System (CDS) software. This software, developed by Thermo Fisher Scientific® in collaboration with Dionex Softron GmbH (a division of Thermo Fisher Scientific®, Olching-Geiselbullach, Germany) facilitated the system control.
The UHPLC system was connected to a Thermo ScientificTM Q ExactiveTM Focus Hybrid Quadrupole-OrbitrapTM mass spectrometer, which used the Heated Electrospray Ionization Source II (HESI II) from Thermo Fisher Scientific®. Nitrogen gas, with a purity exceeding 99.999%, was used as both the collision and damping gas, and it was generated by a Genius NM32LA nitrogen generator manufactured by Peak Scientific®. The Orbitrap mass spectrometer underwent weekly mass calibrations in both positive and negative ion modes. Caffeine and N-butylamine from Sigma-Aldrich® were employed as calibration standards for positive ions, while buspirone hydrochloride, sodium dodecyl sulfate, and taurocholic acid sodium salt were utilized for calibrating the mass spectrometer. The calibration compounds were dissolved in a mixture of acetic acid, acetonitrile, water, and methanol from Merck Darmstadt, Hesse, Germany, which were infused using a Chemyx Fusion 100 syringe pump (Chemyx Inc, Stafford, TX, USA). The UHPLC system was controlled, and data processing was performed using Xcalibur™ 2.3 and TraceFinder™ 3.2 software, which were both provided by Thermo Fisher Scientific®. The mass spectrometer, Q Exactive™ 2.0 SP2, was also operated using software developed by Thermo Fisher Scientific®.

2.4.1. MS Parameters

The HESI (Heated Electrospray Ionization) system was fine-tuned with the following parameters: an S-Lens RF level of 30, an auxiliary gas unit flow rate of 20, a spray voltage of 2500 V for ESI- (Electrospray Ionization negative mode), a capillary temperature of 400 °C, a sheath gas flow rate of 75 units, and an auxiliary gas heater temperature of 500 °C. For the positive-mode data acquisition, a full scan was performed at a selected resolution (70,000 full width half maximum (FWHM)) at m/z 200. The scan range for the target compounds was set to m/z 100–1000, with both the injection time and automatic gain control (AGC) set at 200 milliseconds (ms). A scan rate of two scans per second was selected. Before each set of samples, an external calibration procedure was conducted using a calibration solution in both positive and negative ion modes. In order to verify the outcomes achieved through the complete scan acquisition approach, a focused MS/MS analysis was executed. This involved utilizing a mass inclusion list and the anticipated retention times of the desired substances. The analysis was conducted within a time frame of 30 s, employing the Thermo Scientific™ Orbitrap™ mass analyzer operating in positive mode, with a resolution of 17,500 FWHM (m/z 200). The automatic gain control (AGC) target was configured to 2 × 105, and the maximum injection time was limited to 20 ms. The precursor ions underwent filtering by the quadrupole utilizing an isolation window of m/z 2. The vacuum conditions were maintained around 2 mbar for the fore vacuum, high vacuum, and ultrahigh vacuum, thus covering a range from 105 to below 1010 mbar, respectively. The collision energy within the HCD (Higher-Energy Collisional Dissociation) cell was adjusted to 30 eV.

2.4.2. Metabolite Identification Using Fragmentation Pattern Analysis

For the metabolite identity assignment, an analysis of the existing spectrometric evidences in the literature and the fragmentation pattern analysis of molecules were carried out. The compound structure search was performed using databases such as METLIN, isoMETLIN, The Human Metabolome Database (HMDB), Scopus, ScienceDirect, NCBI, ChemSpider, MassBank, and PubChem. Meanwhile, the chemical structure drawing was performed using ChemDraw professional 15.0 software. The resulting data were then compared with the obtained experimental spectrometric information. The identification of metabolites relied on their elemental composition and precise mass calculation, utilizing a defined mass tolerance window below 6 ppm.

3. Results and Discussion

In this work, we analyzed the alkaloid and nitrogenated compounds profile of C. macromeris plants and cell cultures. In previous reports, we presented the phenolic profile of this plant species, thereby finding that the in vitro cultures had the potential for a biosynthesis of the selected compounds [32,33,34,36]. Regarding the alkaloid and nitrogenated compound profiles analyzed in this work, the chromatographic profile (Figure 1) indicated the presence of 78 compounds. Among the detected compounds, 61 of them were identified. Within the identified compounds, the in vitro plants presented 24 metabolites, the greenhouse plants a total of 21, and the callus tissue 16 compounds. On the other hand, since the spectrometric evidence existent in the literature did not match with the generated spectrometric information, 17 compounds were not identified.
It has been proposed that this C. macromeris is traditionally employed for healing stomach disorders and for hallucinogenic purposes; nevertheless, for this last activity, few reports exist in the literature. In this work, we were not able to find psychotropic metabolites that may support the hallucinogenic functionality; nevertheless, some of the identified compounds are structurally related to alkaloids with recognized pharmacological properties.
Compounds 6, 11, and 14 were assigned as N-methyltyramine and their derivatives (compounds 2, 3, 7, 9, 10, and 12). The parental ion for this metabolite corresponded to m/z: 152.1072 and the generated fragments at m/z: 121.0651 ([M + H-CH4N]+) and 103.0546 ([M + H-CH4N-OH]+) are characteristic of methyltyramine [37,38]. These compounds were mainly detected in the radicular sections of the plants; however, the callus tissue also included two of their derivatives (compounds 3 and 9; see Table 1). This compound is a phenethylamine that has been previously reported in other natural sources, such as Citrus aurantium [39], and its activities against gastrointestinal disorders have been proposed [40]. Similarly, compounds 4, 13, 15, 17, 18, 19, 21, 26, and 42 were detected in both the aerial and radicular sections of the in vitro and greenhouse plants, and it was identified as salsoline. For this metabolite, the pseudomolecular ion at m/z: 194.1175 generated fragments at m/z: 148.0759, 121.0651, 118.0654, and 104.0497 (see Figure 2a). This metabolite is structurally related to anhalamine and heliamine, two tyrosine-derived alkaloids. In addition, it is structurally related to macromerine and normacromerine, two alkaloids previously reported in C. macromeris [41]. Other cacti species such as Echinocereus merkeri have reported the presence of this metabolite [42], and its activities as an antihypertensive agent have been proposed [43]. This compound was not detected in the callus tissue (or may be present but in concentrations below the detection limits).
Compounds 5 and 16 were assigned as benzocaine isomers. The fragmentation pattern analysis of these compounds indicated that the pseudomolecular ion at m/z: 166.0868 generated one fragment at m/z: 123.0446, which was produced by the loss of amino and one methyl group. Another fragment at m/z: 107.0495 was also generated by the cleavage of the amino group and C2H6O tail. This metabolite occurred exclusively in the callus tissue, and its potential applications as an antibacterial, antifungal, and anticancer agent have been proposed [44]. Compound 8 was assigned as N-methylphenylalanine and two of its derivatives (compounds 20 and 34). The pseudomolecular ion at m/z: 180.1025 of N-methylphenylalanine generated fragments at m/z: 148.07611, 120.08121, and 107.04962 (see Figure 2b). Similarly, compounds 22, 23, 29, and 33 were assigned as 3-amino-2-naphthoic acid isomers since the pseudomolecular ion at m/z: 188.0713 generated fragments at m/z: 143.0734, 118.0655, and 107.04945 (see Figure 2c); this nitrogenated phenolic acid occurred exclusively in radicular sections of plants. On the other hand, compounds 24 and 28 were identified as 1,2-ethanediol, 1-(3-ethenylphenyl) since pseudomolecular ion at m/z: 165.0916 yielded fragments at m/z: 135.0444, 121.0651, 107.0495, and 103.0546 (see Figure 2d). This compound was detected in the aerial and radicular sections of greenhouse plants; nevertheless, for in vitro plants, it was only detected in the aerial sections.
Peak 31 was assigned as hordenine, as reported by Zou, et al. [38]. For this metabolite, pseudomolecular ion at m/z: 166.1231 generated fragments at m/z: 121.0655 and 105.0702. Starha [23], Starha, Urbánková and Kuchyňa [24], Starha, and Chybidziurová and Lance [25] evaluated the presence and content of the alkaloids in different cacti species, such as Gymnocalycium and Turbinicarpus, thereby finding that hordenine, followed by tyramine, is found in higher concentrations in most of the analyzed species. This is similar to that reported by Follas, Cassady, and McLaughlin [26], who analyzed six species from the Lobivia genus (L. allegriana, L. aurea, L. backebergii, L. binghamiana, L. huashua, and L. pentlandii) and one species of the genus Pseudolobivia obtained from different sources in California and Arizona, USA. The authors of this paper found that hordenine was in higher concentrations for the species of the Lobivia genus, and 3,4-dimethoxy-β-phenylethylamine and tyramine was in higher concentrations for P. kermesina. The results obtained in the present study suggest that hordenine is present in different cacti species. This metabolite is a class of phenethylamine, which produces activity that increases the blood pressure and contraction force in dogs and rabbits when applied by injection; however, the oral consumption of this metabolite does not produce this activity [43].
Peak 32 occurred exclusively in the callus tissue, and it was assigned as 3,4,5-triethoxyphenethylamine since pseudomolecular ion at m/z: 254.1764 yielded one main fragment at m/z: 138.0918 ([M+H-2C2H6O-C2H6]+). This metabolite is commonly known as trisescaline, and it is structurally related to mescaline (an alkaloid that is present in cacti species such as peyote and San Pedro cactus, two species with recognized pharmacological and hallucinogenic properties [45,46]). On the other hand, peak 36 was assigned as maclurin since the pseudomolecular ion at m/z: 263.0542 produced fragments at m/z: 121.0647 and 107.0491. The signal at m/z: 121.0647 was generated by the fragmentation of the phenyl group and the elimination of two molecules of water; meanwhile, the fragment at m/z: 107.0491 was generated by the subsequent elimination of one methyl group from the aromatic moiety of the fragment at m/z: 121.0647. This compound was only detected in the aerial section of the in vitro plants, and it belongs to a class of metabolites known as benzophenones, a class of metabolites with applications in the cosmetic industry.
Compound 37 was only detected in the greenhouse plants. This compound was assigned as 3,4-dihydro-8-hydroxy-6,7-dimethoxy-1-methylisoquinoline since the pseudomolecular ion at m/z: 222.1124 yielded fragments at m/z: 162.0917 and 148.0761. The fragment at m/z: 162.0917 was generated by the loss of two methoxy groups, and the fragment at m/z: 148.0761 was generated by the subsequent elimination of one methyl group. Similarly, compounds 38, 41, 47, 49, 50, 51, and 53 were also detected in the callus tissue, as was the case in the aerial section of the in vitro plants. In addition, this metabolite was detected in the whole plant that grew under greenhouse conditions. These metabolites were assigned as 3,4-didehydrochromen-2-one derivatives since their signals revealed that they contained the basic structure of 3,4-didehydrochromen-2-one, but at a higher molecular mass.
Toluic acid (peaks 54, 55, and 57) and its derivatives (peaks 45, 59, 61, 64, 65, and 66) were predominantly detected in the in vitro cultures (as indicated in Table 1). The parental ion at m/z: 137.0601 for the toluic acid generated fragments at m/z: 107.0495 and 109.0652 resulting from the loss of one methyl group and the subsequent elimination of one hydroxyl group, respectively. Additionally, another fragment at m/z: 121.0652 was observed due to the loss of oxygen. The characteristic fragment ions of toluic acid were also detected for its derivatives in the mass spectrum. Additionally, two picein isomers (peaks 56 and 58) were detected in all systems. The pseudomolecular ion at m/z: 299.1123 of the picein generated fragments at m/z: 137.0601, 121.0652, and 107.0496. The fragments at m/z: 137.0601 and 121.0652 were generated due to the loss of the glycosidic moiety from the basic phenolic structure and the subsequent elimination of one water molecule, respectively. On the other hand, the fragment at m/z: 121.0652 was produced by the loss of hexose along with water and one methyl group.
Lauryldiethanolamine isomers, compounds 60 and 63, were identified based on their respective parental ion at a m/z: 274.2755, which generated fragment ions at m/z: 256.2643 and 230.2486. These fragments were observed due to the loss of water and the subsequent elimination of one ethyl group, respectively. Another fragment at m/z: 102.0916 was produced by the loss of a C6H24 radical. Similarly, compound 62, identified as 4-amino-2-dodecyltetrahydro-3-furanol, exhibited a fragment at m/z: 254.2491, which was generated by the loss of water. Four alibendol isomers (compounds 68, 69, 70, and 72) were detected in all the analyzed tissues. For this metabolite, the pseudomolecular ion at m/z: 252.1243 generated fragments at m/z: 196.0610, which was produced by losing one methyl and C3H6 radical. Similarly, fragments at m/z: 122.0600 ([M+H-C2H7O-H2O-CH4O-C3H6]+)and 178.0504 ([M+H-OH-CH3-C3H6]+) were also observed. Finally, compound 77, identified as 2-[dodecyl(methyl)amino] acetic acid, was exclusively detected in the callus tissue, with a fragment at m/z: 240.2334 generated due to the loss of water.
According to our analyses, no alkaloids with strong psychotropic properties reported in the literature were found in the C. macromeris plant extracts. On the other hand, in the callus tissue, we observed molecules that were structurally related to alkaloids with recognized psychotropic properties such as 3,4,5-triethoxyphenethylamine, which is corelated with the mescaline present in Lophophora williamsii [45]. Kikuchi, Uchiyama, Ogata, Kikura-Hanajiri, and Goda [41] evaluated the presence of alkaloids in one herbal product that was sold as incense in Japan, and they identified, using chromatographic and spectrometric approaches, two hallucinogenic phenethylamines (normacromerine and macromerine); additionally, by means of DNA sequence analyses, they found that the psychotropic product may include C. macromeris as one of its constituents. Similarly, in a series of papers, Keller and McLaughlin [47], Keller et al. [48], and Keller [49] reported the presence of alkaloids such as macromerine and normacromerine in C. macromeris sp. Runyonii, suggesting that—in past decades—this plant species was promoted as a natural and legal psychedelic agent; nevertheless, we did not find the reported molecules, suggesting that among the varieties there may exist phytochemical differences. In this regard, although no coincidences were found when compared with the literature, in vivo studies are required to evaluate the possible psychotropic effects of C. macromeris extracts and preparations.
On the other hand, it has been demonstrated that, for people without adequate botanical training, there is a difficulty in distinguishing species that share common physical characteristics, since within plant varieties there can only be slight morphological differences. In this regard, although C. macromeris is listed as a “least concern” type in the IUCN Red List of Threatened Species and in México, the local normativity does not include it under any protection category; this is an endemic species whose natural populations are being reduced due to the overexploitation of its habitats and the subtraction of specimens from its natural environment, and this occurs due to the desire to sample its psychotropic effects, as well as for ornamental purposes.

4. Conclusions

The procedures used allowed the detection of 78 metabolites of the C. macromeris extracts, 61 of them were detected as per the following: (1) in vitro plants (24 compounds), (2) greenhouse plants (21 compounds), and (3) callus tissue (16 compounds). In addition, 7 compounds that are common in the three types of plant culture systems were detected; thus, these secondary metabolites can serve as taxonomic markers to verify the authenticity of the C. macromeris species, and the plant tissue culture of this cactus species can also serve as an alternative source for the biosynthesis of selected compounds. In addition, based on our results, the generated information may help environmental public policy decision making by providing information through which to generate strategies to reduce the overcollection of this plant species since, under the working conditions, no recognized hallucinogenic alkaloids were identified in the plants or cell tissues; furthermore, the biotechnological information presented here can help to develop and implement strategies for their propagation, conservation, and reincorporation of this plant species into their natural habitats.

Author Contributions

E.C.-G.: conceptualization and information formal analysis, wrote the manuscript, and performed the identification of bioactive metabolites. V.V.-E.: analyzed information and helped to organize the data. E.P.-M.B. and F.C.-S.: conceptualization. G.A.: formal analysis, methodology and reviewing. O.J.R.-H.: reviewing. Y.A.G.-A.: conceptualization. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Council for Science and Technology (CONACYT), grant number 366290, Proyecto SIP: 20221180, and 20230403 from the National Polytechnic Institute, and resources were supplied by the Autonomous University of Aguascalientes.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the manuscript.

Acknowledgments

We thank Ruben Muñoz and Jorge Bórquez Ramírez from the University of Antofagasta, Chile, and Carlos Areche from the University of Chile, Chile for technical support.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 13 09947 g001aApplsci 13 09947 g001b
Figure 1. UHPLC profiles of the alkaloid and nitrogenated compounds present in C. macromeris. The separation profile was obtained using extracts prepared with aerial (a) and radicular (b) sections of the plants cultivated under in vitro conditions for 12 weeks. The aerial (c) and radicular (d) sections of plants growing under greenhouse conditions for one year were also analyzed and compared with the callus tissue (e) collected after nine weeks of culture.
Figure 1. UHPLC profiles of the alkaloid and nitrogenated compounds present in C. macromeris. The separation profile was obtained using extracts prepared with aerial (a) and radicular (b) sections of the plants cultivated under in vitro conditions for 12 weeks. The aerial (c) and radicular (d) sections of plants growing under greenhouse conditions for one year were also analyzed and compared with the callus tissue (e) collected after nine weeks of culture.
Applsci 13 09947 g001aApplsci 13 09947 g001b
Applsci 13 09947 g002
Figure 2. Proposed fragmentation pattern and MS2 scan of (a) salsoline (compounds 4, 13, 15, 17, 18, 19, 21, 26, and 42), (b) N-methylphenylalanine (compound 8), (c) 3-Amino-2-naphthoic acid (compounds 22, 23, 29, and 33), and (d) 1,2-Ethanediol, 1-(3-ethenylphenyl) (compounds 24 and 28).
Figure 2. Proposed fragmentation pattern and MS2 scan of (a) salsoline (compounds 4, 13, 15, 17, 18, 19, 21, 26, and 42), (b) N-methylphenylalanine (compound 8), (c) 3-Amino-2-naphthoic acid (compounds 22, 23, 29, and 33), and (d) 1,2-Ethanediol, 1-(3-ethenylphenyl) (compounds 24 and 28).
Applsci 13 09947 g002
Table 1. The alkaloid and nitrogenated compounds identified in the C. macromeris plants and in vitro cultures.
Table 1. The alkaloid and nitrogenated compounds identified in the C. macromeris plants and in vitro cultures.
PeakRetention Time (min)UV MaxTentative IdentificationElemental Composition [M + H]+Theoretical Mass (m/z)Measured Mass (m/z)Accuracy (ppm)MSn IonsTissue
11.35196, 210UnknownC20H15NO7+381.0848381.08392.36203.1038, 112.8961, 104.1078c
21.51221, 274N-methyltiramine derivativeC9H12NO+-150.0917-121.0651, 103.0546ri, rg
31.52210(3-ethenylphenol) N-methyltiramine derivativeC8H9O+121.0647121.06534.21103.0545c
41.67225, 277Salsoline isomer IC11H16NO2+194.1175194.11792148.0759, 121.0651, 118.0654, 104.0497ag
51.83204Benzocaine isomer IC9H12NO2+166.0862166.08683.61107.0495, 123.0446c
61.87220, 276N-methyltiramineC9H14NO+152.1069152.10721.90121.0652, 103.0546ai
71.88225, 274N-methyltiramine derivativeC9H12NO+-150.0918-121.0651, 103.0545rg
81.97220, 277N-methylphenylalanineC10H14NO2+180.1019180.10253.33148.0761, 120.0812, 107.0496ai, ag
92.05215(3-ethenylphenol) N-methyltiramine derivative isomerC8H9O+121.0647121.06523.38103.0545c
102.10220N-methyltiramine derivative isomerC9H12NO+-150.0918-121.0651, 103.0547,ri
112.31220N-methyltiramine isomerC9H14NO+152.1069152.10742.69103.0545c, rg
122.32220, 280(3-ethenylphenol) N-methyltiramine derivative isomerC8H9O+121.0647121.06523.38103.0546ri
132.45220, 276Salsoline isomer IIC11H16NO2+194.1175194.11781.59148.0760, 121.0650, 118.0657ai, ag
142.60223, 275N-methyltiramine isomerC9H14NO+152.1069152.10732.62121.0652, 103.0546ai, ri
153.16226, 276Salsoline isomer IIIC11H16NO2+194.1175194.11823.34148.0761, 121.0651, 118.0866ag, rg
163.35210Benzocaine isomer IIC9H12NO2+166.0862166.08683.61107.0495, 123.0446c
173.73220, 276Salsoline isomer IVC11H16NO2+194.1175194.11813.24148.0760, 121.0652, 118.0655ai, ri, ag, rg
184.41205, 228, 278Salsoline isomer VC11H16NO2+194.1175194.11813.09148.0761, 121.0651, 118.0867ai, ri
195.34220, 277Salsoline isomer VIC11H16NO2+194.1175194.11823.50148.0761, 121.0652, 118.0655ag
205.62225N-methylphenylalanine derivativeC10H14NO+-164.1075-148.0759, 120.0810, 107.0495ri
216.16226, 278Salsoline isomer VIIC11H16NO2+194.1175194.11813.19148.0761, 121.0651, 118.0867ai
227.76225, 2793-amino-2-naphthoic acidC11H10NO2+188.0706188.0713-143.0734, 118.0655, 107.0494rg
238.39218, 2853-amino-2-naphthoic acidC11H10NO2+188.0706188.07123.34143.0734, 118.0655, 107.0494ri
248.50230, 2791,2-ethanediol, 1-(3-ethenylphenyl)C10H13O2+165.0910165.09163.63135.0444, 121.0651, 107.0495, 103.0546ag, rg
258.69224, 280UnknownC13H25NO3+-243.1841-149.0238, 123.0445, 107.0495, 102.0918c
268.90220, 275Salsoline isomer VIIIC11H16NO2+194.1175194.11813.24148.0761, 121.0650, 118.0654ag, rg
279.04230, 282Unknown isomerC13H25NO3+-243.1841-149.0238, 107.0494, 102.0917c
289.14222, 2751,2-ethanediol, 1-(3-ethenylphenyl)C10H13O2+165.0910165.09153.02135.0444, 121.0651, 107.0495, 103.0546ai
299.35221, 2793-amino-2-naphthoic acidC11H10NO2+188.0706188.07133.82143.0734, 118.0655, 107.0496rg
309.35226, 280UnknownC13H24NO3+-243.1841-166.1232, 135.0809, 103.0546, 102.0917ri
319.59224, 276HordenineC10H15NO+166.1226166.12312.88121.0655, 105.0702ai
329.62236, 2853,4,5-triethoxyphenethylamineC14H24NO3+254.1751254.17645.11138.0918c
339.73222, 2843-amino-2-naphthoic acidC11H10NO2+188.0706188.07123.5143.0734, 118.0655, 107.0495ri
3410.10223, 280N-methylphenylalanine derivativeC10H10N+144.0807144.08123.05120.0811, 107.0496ri
3510.19240, 285UnknownC21H32N2O12+-504.1962-177.0551, 145.0288, 117.0339c
3610.38223, 275MaclurinC13H11O6+263.0550263.05422.85121.0647, 107.0491ai
3710.52234, 2773,4-dihydro-8-hydroxy-6,7- dimethoxy-1-methylisoquinolineC12H15NO3+222.1124222.11344.05162.0917, 148.0761ag, rg
3810.55238, 2823,4-didehydrochromen-2-one derivativeC22H18N2O2+-342.1367-145.0280, 117.0339c
3910.67236, 326UnknownC12H9N2O2+-213.0667-167.0608, 145.0287, 140.0498, 115.0546, 105.0339rg
4010.77235, 327UnknownC21H17NO7+-395.1000-194.1180, 167.0705, 145.0284, 105.0339ag
4110.83233, 298, 3203,4-didehydrochromen-2-one derivativeC23H32N2O13+-544.1908-342.1368, 145.0280, 117.0339c
4210.91225, 277SalsolineC11H16NO2+194.1175194.11792148.0759, 121.0651, 118.0654ag
4311.01236, 285UnknownC14H17O4+-249.1133-177.0551, 145.0287, 128.0624, 115.0545c
4411.26237, 327UnknownC10H9O3+-177.0553-145.0288, 117.0339, 103.0546, ai
4511.37238, 285Toluic acid derivativeC16H30N2O4+-314.2168-137.0601c
4611.38228, 283UnknownC29H36N2O9+-556.2421-256.1010, 144.0813, 130.0556, 115.0547rg
4711.54236, 285, 3193,4-didehydrochromen-2-one derivativeC21H16N2O+-312.12551.06145.0288, 117.0339c
4811.72227, 282UnknownC12H26N2O10+-358.1588-172.0762, 144.0881, 130.0655rg
4911.92238, 2823,4-didehydrochromen-2-one derivativeC22H18N2O2+-342.1368-145.0280, 117.0339c
5012.00234, 2773,4-didehydrochromen-2-one derivativeC22H18N2O2+-342.1368-145.0280, 117.0339ri, ag, rg
5112.15238, 3243,4-didehydrochromen-2-one derivativeC21H16N2O+-312.12551.12145.0288, 117.0339ai
5212.85259UnknownC16H15NO2+-253.1083-145.0288, 133.0651, 118.0416, 103.0547 ag, rg
5313.802853,4-didehydrochromen-2-one derivative --314.1412-145.0287, 117.0339, 109.1015ai, ri
5414.75230, 290Toluic acidC8H9O2+137.0597137.06012.84107.0495, 121.0652, 109.0651ri
5514.74221, 283Toluic acidC8H9O2+137.0597137.06012.84107.0495, 121.0651, 109.0651c, ai, ri, ag, rg
5616.36283PiceinC14H19O7+299.1125299.11230.63137.0601, 121.0652, 107.0495c, ag, rg
5717.08221, 286Toluic acidC8H9O2+137.0597137.06013.21107.0496, 121.0651, 109.0651ai
5815.27285Picein isomerC14H19O7+299.1125299.11230.53137.0601, 121.0653, 107.0491ai, ri
5918.70290Toluic acid derivative--353.2334-137.0601, 121.0654ri
6019.50283LauryldiethanolamineC16H36NO2+274.2740274.27555.5256.2643, 230.2486, 102.0916c, ai, ri, ag, rg
6119.70282Toluic acid derivative--230.2487-137.0601, 121.0649c, ai, ri, ag, rg
6219.902764-amino-2-dodecyltetrahydro-3-furanolC16H34NO2+272.2584272.26005.98254.2491ai, ri
6320.25282Lauryldiethanolamine isomerC16H36NO2+274.2740274.27555.5256.2640, 230.2489c, ri
6420.39243, 291M-toluic acid derivative--289.0990-137.0600, 121.0651rg
6520.56283M-toluic acid derivative--387.1849-137.0600, 121.0651c, ai, ag
6620.60284Toluic acid derivative--289.0992-137.0600, 121.0651,ri, ag
6720.862831-oxo-2-phenyl-phenalen-3-yl benzoateC26H17O3+377.1172377.11781.53123.0407ag
6820.90282AlibendolC13H18NO4+252.1230252.12445.43196.0610, 178.0504, 122.0600c, rg
6921.03266AlibendolC13H18NO4+252.1230252.12435.39196.0610, 178.0504, 122.0600ag
7021.33290AlibendolC13H18NO4+252.1230252.12435.31196.0610, 178.0504, 122.0600ri
7121.50284UnknownC17H35O11+-415.2175-149.0236, 119.0859, 105.0702c, ai, ag, rg
7221.48284AlibendolC13H18NO4+252.1230252.12435.15196.0610, 178.0504, 122.0600ai
7321.70295UnknownC16H36NO+-258.2804-119.0859ri
7421.92285UnknownC10H23NO11+-333.1264-167.0609, 140.0499, 113.0390ag, rg
7522.54284UnknownC21H45NO11+-487.2968-133.1016, 119.0848, 105.0703ag
7623.11282UnknownC27H60N5O6+-550.4589-256.2649, 165.0073, 135.0444, 105.0703, 102.0918c, ri, rg
7723.942832-[dodecyl(methyl)amino] acetic acidC15H32NO2+258.2427258.24425.8240.2334c
7824.45284UnknownC28H33NO+-399.2558-149.0236, 129.0700, 108.9046, 105.0702c, ai, ri, ag, rg
c = callus culture, ai = aerial part in vitro plants, ri = radicular part in vitro plants, ag = aerial part greenhouse plants, and rg = radicular part greenhouse plants.
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MDPI and ACS Style

Viera-Escareño, V.; Perez-Molphe Balch, E.; Gómez-Aguirre, Y.A.; Ramos-Herrera, O.J.; Abdi, G.; Cruz-Sosa, F.; Cabañas-García, E. Alkaloid and Nitrogenated Compounds from Different Sections of Coryphantha macromeris Plants and Callus Cultures. Appl. Sci. 2023, 13, 9947. https://doi.org/10.3390/app13179947

AMA Style

Viera-Escareño V, Perez-Molphe Balch E, Gómez-Aguirre YA, Ramos-Herrera OJ, Abdi G, Cruz-Sosa F, Cabañas-García E. Alkaloid and Nitrogenated Compounds from Different Sections of Coryphantha macromeris Plants and Callus Cultures. Applied Sciences. 2023; 13(17):9947. https://doi.org/10.3390/app13179947

Chicago/Turabian Style

Viera-Escareño, Valeria, Eugenio Perez-Molphe Balch, Yenny Adriana Gómez-Aguirre, Oscar Javier Ramos-Herrera, Gholamreza Abdi, Francisco Cruz-Sosa, and Emmanuel Cabañas-García. 2023. "Alkaloid and Nitrogenated Compounds from Different Sections of Coryphantha macromeris Plants and Callus Cultures" Applied Sciences 13, no. 17: 9947. https://doi.org/10.3390/app13179947

APA Style

Viera-Escareño, V., Perez-Molphe Balch, E., Gómez-Aguirre, Y. A., Ramos-Herrera, O. J., Abdi, G., Cruz-Sosa, F., & Cabañas-García, E. (2023). Alkaloid and Nitrogenated Compounds from Different Sections of Coryphantha macromeris Plants and Callus Cultures. Applied Sciences, 13(17), 9947. https://doi.org/10.3390/app13179947

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