Chemical Composition of Plants of the Genus Zaluzania

Abstract

The chemical structure of compounds identified in species of the genus Zaluzania is reported herein, highlighting the contributions by Professor Pedro Joseph-Nathan to the chemistry of these plants. Although 36 names have been proposed for Zaluzania, only 14 species are currently accepted in the genus, and they are reported to be a rich source of sesquiterpene lactones and flavonoids. Their essential oils also contain several terpenoids, especially ent-kaurene-type diterpenes. In addition, we identified the guaianolides zaluzanin A and zaluzanin B, zaluzanin C, and zaluzanin D, and the eudesmanolides ivalin and ivalin acetate as the major constituents in infusions of aerial parts of Zaluzania augusta, Zaluzania parthenioides, and Zaluzania triloba, respectively. These sesquiterpene lactones were characterized by their physical and spectroscopic data, including ¹H and ¹³C nuclear magnetic resonance (NMR). Likewise, the structures of zaluzanins C and ivalin were confirmed by X-ray diffraction analysis. The presence of guaianolides in Z. parthenioides and eudesmanolides in Z. triloba could be used as a biomarker to differentiate these 2 species, which were previously considered synonymous.

Keywords

chemical composition sesquiterpene lactones flavonoids essential oil

Introduction

The genus Zaluzania includes a small number of shrubby plants native to Mexico, except for Zaluzania grayana, which has also been found in Arizona and New Mexico.¹ According to the International Plant Names Index, 36 names related to Zaluzania have been recorded, but only 14 species are accepted in the genus (Table 1).¹ Several of these plant species are considered synonyms and, in some cases, there is uncertainty about their taxonomic identification.

Table 1.

Plant Names Related to Zaluzania.¹

Name	Current taxonomic status
Zaluzania angusta Benth. & Hook.f.	Unplaced^a
Zaluzania anthemidifolia B.L.Rob. and Greenm.	Synonym of Hybridella anthemidifolia
Zaluzania asperrima Sch. Bip.	Synonym of Zaluzania montagnaefolia
Zaluzania asperrima var. montagnaefolia B.L.Rob. & Greenm.	Synonym of Zaluzania montagnaefolia
Zaluzania augusta (Lag.) Sch. Bip.	Accepted
Zaluzania augusta var. rzedowskii McVaugh	Accepted
Zaluzania cinerascens Sch. Bip.	Synonym of Zaluzania megacephala var. megacephala
Zaluzania coulteri Hemsl.	Synonym of Zaluzania megacephala var. megacephala
Zaluzania delgadoana B.L. Turner	Accepted
Zaluzania discoidea A. Gray	Accepted
Zaluzania durangensis B.L. Turner	Accepted
Zaluzania eminens F.T. Hubb.	Synonym of Podachaenium eminens
Zaluzania ensifolia Sch. Bip.	Synonym of Aldama ensifolia
Zaluzania globosa Sch. Bip	Synonym of Hybridella globosa var. globosa
Zaluzania globosa var. myriophylla (Sch. Bip.) W.M. Sharp	Synonym of Hybridella globosa var. myriophylla
Zaluzania grayana B.L. Rob. and Greenm.	Accepted
Zaluzania grayiana B.L. Rob. and Greenm.	Unplaced^a
Zaluzania indica Reinw. ex Blume	Unplaced^a
Zaluzania megacephala Sch. Bip.	Accepted
Zaluzania megacephala var. coahuilensis Olsen	Accepted
Zaluzania mollissima A. Gray	Accepted
Zaluzania montagnaefolia Sch. Bip.	Accepted
Zaluzania myriophylla Sch. Bip.	Synonym of Hybridella globosa var. myriophylla
Zaluzania nonensis Hieron.	Synonym of Kingianthus paniculatus
Zaluzania oppositifolia Sch. Bip.	Synonym of Alloispermum scabrifolium
Zaluzania parthenioides (DC.) Rzed.	Accepted
Zaluzania pinnatilobata Sch. Bip.	Synonym of Sidneya pinnatilobata
Zaluzania pringlei Greenm.	Accepted
Zaluzania quitensis Hieron.	Synonym of Kingianthus paniculatus
Zaluzania resinosa S. Watson	Synonym of Greenmaniella resinosa
Zaluzania robinsonii W.M. Sharp	Synonym of Zaluzania parthenioides
Zaluzania sodiroi Hieron.	Synonym of Kingianthus paniculatus
Zaluzania squarrosa Sch. Bip.	Synonym of Aldama squarrosa
Zaluzania subcordata W.M. Sharp	Accepted
Zaluzania triloba (Ortega) Pers.	Accepted
Zaluzania trilobata Hoffmanns.	Synonym of Zaluzania triloba

Names that cannot be accepted or synonymized.

Some Zaluzania species have been used in traditional medicine in Mexico because of their antidiabetic and abortifacient effects; in particular, Zaluzania augusta and Zaluzania triloba have been reported to have such properties.^2,3 Infusion of the roots of Z. augusta has been used to induce menstruation in some parts of the state of Hidalgo, while Z. triloba is used for stomach pain and wounds.⁴ The branches of Z. augusta are used to fumigate poultry houses infested with Dermanyssus gallinae (red mite), and the infusion of aerial parts of Z. triloba is used to wash wormy wounds in sheep and goats to eliminate fly larvae.⁵

Chemical studies on Zaluzania species have shown them to be valuable sources of sesquiterpene lactones, while flavonoids, essential oils, and lipophilic metabolites have also been identified. This work is aimed at describing the chemical structure of the compounds identified in Zaluzania species, highlighting the contribution of Professor Pedro Joseph-Nathan in the chemistry of this plant genus.

Results and Discussion

Sesquiterpene Lactones

The chemical composition of a Zaluzania species was first reported by Romo et al.⁶ They studied the EtOH extract of the aerial part of Z augusta, which was partitioned with CHCl₃ and the residue chromatographed on alumina. This procedure allowed the isolation of sesquiterpene lactones of the guaine series, zaluzanin A (1) and zaluzanin B (2) (Figure 1). Subsequently, following the same procedure described above, Romo-de Vivar et al⁷ reported 2 other guaianolides, zaluzanin C (3) and zaluzanin D (4), as well as the eudesmanoline ivalin (6) (Figure 1). Compound 3 was isolated from Z. augusta, while 4 and 6 were found in Z. triloba. In 1971, Romo de Vivar and González⁸ reported another guaianolide, dehydrocostus lactone (5) from the roots of Z triloba.⁹ This lactone was obtained as crystalline product by alumina column purification of the EtOH extract. In addition, Jolad et al¹⁰ reported the isolation of 3 as an antileukemic principle from the EtOH extract of Z. robinsonii (now Z. parthenioides). Sequential partitioning with CHCl₃ and EtOAc of the extract, followed by silica gel column chromatography of the EtOAc part, led to 3. Also, Domínguez et al¹¹ informed the isolation of 3 from the petroleum ether extract of the aerial part of Z. parthenioides.

Figure 1.

Chemical structure of sesquiterpene lactones isolated from Zaluzania spp.

Yabuta et al¹² reported the presence of sesquiterpene lactones in Z. augusta, Z. montagnaefolia (named by then as Z. montagnifolia), Z. parthenioides, Z. pringlei, and Z. triloba. The aerial part of each of the species was extracted with CHCl₃ and direct crystallization or chromatography on silica gel or alumina of the extract led to obtaining 1-4 and 6 along with the germacranolides costunolide (8) and epi-tulipenolide (9), as well as the eudesmanolide α-cyclocostunolide (11) (Figure 1). Thus, the presence of 1 and 2 had already been confirmed in Z. augusta, although both compounds were also found in Z. montagnaefolia. Similarly, 2 and 3 were found in Z. parthenioides and Z. tribloba, while 8 and 11 were identified in Z. montagnaefolia, and 9 in Z. pringlei. At that time, Z. parthenioides and Z. triloba were considered synonymous, but differences in chemical composition between them had already been noted. It wasn’t until 2012 that Billie L. Turner considered these 2 species to be different.¹³ After, Spring et al (1995) studied Z. grayana and were able to isolate 3, the germacranolide 10 (considered as a 15-hydroxy derivative of 8), and the modified guaianolide zaluzanin E (12) (Figure 1).¹⁴ In this study, the leaves of the species were extracted with CH₂Cl₂ and the extract was subjected to on-line high-performance liquid chromatography (HPLC)/RMN experiments, which led to the identification of the compounds.

Some sesquiterpene lactones from Zaluzania spp. possess relevant biological activity. Thus, for example, zaluzanin A (1) induced relaxation in KCl-induced contraction in rat uterine smooth muscle and reduced human sperm motility in vitro¹⁵; zaluzanins 3 and 4 exhibited antileukemic and anticancer properties^10,16,17; and 4 was also reported as an antifungal agent.¹⁸ Ivalin (6) showed significant cytotoxic activity against several murine and human tumor cell lines, comparable to that of cisplatin.¹⁹

Flavonoids

In an interesting study on flavonoids in Zaluzania spp.,²⁰ Olsen and Mabry (1980) found that various species in this genus produce about 20 compounds, 13 of which were characterized as methyl ethers and/or glycosides of quercetin (13-20), kaempferol (21, 22), and patuletin (23, 24). Jaceidin (25) was also identified (Figure 2). All other compounds could only be detectable in trace amounts. This analysis was carried out utilizing leaf material extracted with aq. MeOH. Thus, 14, 18, 19, and 20 were identified in Z. augusta; 15, 17, 23, and 24 in Z. augusta var. rzedowskii; 15, 17, and 23 in Z. megacephala var. coahuilensis, while 15, 17, 23, 24, and traces of 18 were identified in Z. megacephala. Also, 14, 16, 20, 22, and traces of jaceidin (25) were documented in Z. mollissima; 16, 18, and 22 in Z. montagnaefolia (Z. montagnifolia); and 14 and 20 in Z. pringlei. In addition, 13, 21, 22, and 25 were identified in Z. triloba.

Figure 2.

Chemical structure of flavonoids identified in Zaluzania spp.

Lipophilic Constituents and Essential Oils

Lipophilic constituents of Zaluzania spp. have been chemically characterized in Z. parthenioides,¹¹ Z. augusta,²¹ and Z. montagnaefolia (Z. montagnifolia).^22,23 On silica gel column chromatography of the petroleum ether extract from the aerial part of Z. parthenioides, octacosane, β-sitosterol (26) and stigmasterol (27) were isolated (Figure 3),¹¹ whereas (−)-kaur-9(11),16-dien-19-oic acid (grandiflorenic acid) (28), and 16α-hydroxy-(−)-kauran-19-oic acid (29) (Figure 3) were obtained by tonsil chromatography of the CHCl₃ extract form the aerial part of Z. augusta.²¹ Likewise, Villa-Ruano et al²² reported 56 compounds from the hexane extract of the flowers, leaves, and roots of Z. montagnaefolia. Years later, the same research team reported (2018) the composition of essential oils, obtained by hydrodistillation and recovery with hexane, from flowers and leaves of this species, identifying 32 metabolites.²³ Compounds from Z. montagnaefolia were characterized by GS-MS and comparison of the mass fragmentation pattern with those described in the NIST, Wiley, Pherobase, and Flavornet mass spectral databases, as well as by co-injection with available authentic standards; as a result, 18 monoterpenes were identified: β-myrcene (33), ocimene (34), linalool (35), linalyl isobutyrate (36), linalool oxide (37), limonene (38), α-terpinene (39), terpinolene (40), α-thujene (41), sabinene (42), α-terpineol (43), α-pinene (44), β-pinene (45), borneol (46), camphor (47), camphene (48), tricyclene (49), and methyl epi-jasmonate (50) (Figure 4). The presence of 39 sesquiterpenes was also established: α-humulene (51), humulene epoxide II (52), 14-hydroxy-α-humulene (53), β-cariophyllene (54), iso-cariophyllene (55), nerolidol (56), β-bisabolene (57), α-bisabolol (58), bisabolone (59), β-curcumene (60), α-cadinene (61), δ-cadinene (62), τ-cadinol (63), α-muurolene (64), α-muurolol (65), 1-epicubenol (66), trans-calamenen-10-ol (67), E-β-farnesene (68), germacrene D (69), germacrene D-4-ol (70), bicyclogermacrene (71), α-selinene (72), β-selinene (73), δ-selinene (74), γ-eudesmol (75), β-eudesmol (76), elemol (77), neo-intermedeol (78), guaia-1(10)-11-dien-9-one (79), gurjunene (80), spathulenol (81), globulol (82), alloaromadendrene epoxide (83), copaene (84), italicene (85), (−)-α-panasinsene (86), β-cubenene (87), trans-α-bergamotene (88), and hexahydrofarnesyl acetone (89) (Figure 5). Finally, 3 ent-kaurene-type diterpenes were identified: ent-kaurene (30), ent-kaurenoic acid (31), and grandiflorenic acid (28), in addition to the labdane epimanool (32) (Figure 3). Furthermore, phytol, squalene, nonacosane, 1-pentadecene, 1-octadecene, 1-nonacosane, (Z)-n-heptadec-8-ene, 1,12-tridecadiene, tetracosanol, dodecanal, (E,E)-2,4-decadienal, tetracosanal, hexadecenoic acid, tetracosanoic acid, methyl hexadecanoate, and cyclohexadecanolide were also reported. The stereochemistry of several compounds described in these works is uncertain, so the formulas in Figures 3 to 5 correspond to those found in the NIST database,²⁴ the Merck-Sigma-Aldrich catalogue, and in the work of Dewick.²⁵ The main essential oil metabolites were camphor (47), β-caryophyllene (54), and germacrane D (69), while ent-kaurenoic acid (31) and grandiflorenic acid (32), were the major lipophilic metabolites.

Figure 3.

Chemical structure of sterols and diterpenes identified in Zaluzania spp.

Figure 4.

Chemical structure of monoterpenes identified in Zaluzania montagnaefolia.

Figure 5.

Chemical structure of sesquiterpenes identified in Zaluzania montagnaefolia.

Sesquiterpene Lactones in Infusion of Z. augusta, Z. parthenioides, and Z. triloba

Since Z. augusta, Z. parthenioides, and Z. triloba have been traditionally used as infusions in the state of Hidalgo, Mexico,⁴ the content of sesquiterpene lactones in the infusion of aerial parts of these species was investigated. Some years ago, P. Joseph-Nathan and 2 co-authors of this work reported the isolation and characterization of zaluzanin A (1) from the infusion of aerial parts of Z. augusta.²⁶ Herein, we replicated the method with the same species, plus Z. parthenioides and Z. triloba. Dried and ground flowers and leaves were subjected to extraction with hot water and extracted with EtOAc. The extract was purified by column chromatography as described elsewhere²⁶ to afford 1 and 2 from Z. augusta; 3 and 4 from Z. parthenioides; and 6, and ivalin acetate (7) from Z. triloba. In addition, samples from EtOAc fractions (60 mg) were analyzed by HPLC to quantify zaluzanin A (1), zaluzanin C (3), and ivalin (6). The extracts contained 26 mg of 1, 30 mg of 3, and 28 mg of 6, respectively. Compounds 1-4, 6, and 7 were characterized by physical and spectroscopic data (see Supplemental information), including X-ray diffraction analysis for 3 and 6 (Figure 6). To the best of our knowledge, the crystallographic structures of these 2 sesquiterpene lactones have not been reported, although X-ray diffraction data of the bromoacetate derivative of ivalin were reported by Coetzer et al (1982).²⁷

Figure 6.

X-ray crystal structure of zaluzanin C (3) and ivalin (6).

Specimens of Z. parthenioides and Z. triloba were collected in the municipality of Ixmiquilpan and Mineral de la Reforma, State of Hidalgo, Mexico, respectively. Morphologically, both species are very similar, which may have caused them to be confused or considered synonyms. The sesquiterpene lactones identified in the infusion of their aerial parts suggested that Z. parthenioides biosynthesizes mainly guaianolides (zaluzanin C), whereas Z. triloba predominantly produces eudesmanolides (ivalin), so these compounds may serve as biomarkers to distinguish between both shrubs.

Conclusions

Chemical studies have been conducted on 10 out of the 14 species accepted in the genus Zaluzania. These studies have demonstrated the presence of 12 sesquiterpene lactones, 13 flavonoids, 5 diterpenes, 18 monoterpenes, 39 other sesquiterpenes, β-sitosterol, stigmasterol, and squalene. The infusion of aerial parts of Z. augusta contains zaluzanins A (1) and B (2), Z. parthenioides contains zaluzanins D (3) and C (4), while ivalin (6) and its acetate ester (7) are present in Z. triloba. The chemical structures and biological activities of the major metabolites identified in these plants are consistent with some of their traditional uses and their attributed therapeutic properties.

Experimental

General

Chromatographic separations were carried out on Merck silica gel 60 (230-400 mesh ASTM). TLC assays were performed on sheets of silica gel 60 F₂₅₄, using ceric sulfate as developer and λ = 254 and 365 nm as fluorescence excitatory wavelengths. ¹H and ¹³C nuclear magnetic resonance (NMR) spectra were obtained on a Bruker Ascend instrument (400 MHz for ¹H; 100 MHz for ¹³C) from CDCl₃ solutions, using TMS as an internal standard. Optical rotation was recorded in CHCl₃ on a PerkinElmer 341 polarimeter. Melting points were measured on a Fisher–Johns apparatus and are uncorrected. Infrared spectra were obtained on a PerkinElmer FT-IR System 2000 spectrophotometer using cesium iodide (CsI) cells and diffuse attenuated reflectance.

Plant Material

Specimens of Zaluzania augusta (Lag.) Schultz Bip., Zaluzania parthenioides (DC.) Rzed., and Zaluzania triloba (Ortega) Pers. were collected during September–October 2019 from the municipality of Epazoyucan (98°36′54″W, 20°03′08″N), Ixmiquilpan (99°07′05″W, 20°23′47″N), and Mineral de la Reforma (98°42′13″W, 20°05′36″N), respectively, in the state of Hidalgo, México, and identified by Professor Manuel González Ledesma. Voucher specimens (JM Torres-Valencia 168, JM Torres-Valencia 131, and JM Torres-Valencia 130, respectively) are preserved in the Herbarium of the Universidad Autónoma del Estado de Hidalgo, Mineral de la Reforma, Hidalgo, Mexico.

Ethyl Acetate Extracts from Z. augusta, Z. parthenioides, and Z. triloba Infusion

Aerial parts (100 g) of Z. augusta, Z. parthenioides, and Z. triloba were extracted with hot water (750 mL) for 30 min, filtered and extracted with EtOAc (750 mL). The organic phase was dried over anhydrous Na₂SO₄ and concentrated to obtain the EtOAc extracts (2.13, 1.90, and 1.37 g, respectively).

Zaluzanins A (1) and B (2)

The EtOAc extract (1 g) from Z. augusta was subjected to chromatographic separation as described elsewhere²⁶ to obtain 1 (65 mg). Another aliquot of the extract (1 g) was purified on a silica gel column (138 g) using hexane-i-PrOH (4:1, 800 mL) as eluent, and collecting 20 mL fractions. Compound 2 (54 mg) was recovered as an amorphous solid from fractions 20 and 21. Physical and spectroscopic data of 1 and 2 were consistent with previous reports.^{6,14,15,26,28} For ¹H and ¹³C NMR data, see Supplemental information.

Zaluzanins C (3) and D (4)

The EtOAc extract (1 g) from Z. parthenioides was passed through a silica gel column (138 g), using hexane-EtOAc (3:1, 2:1, 1:1, 1:2, and 0:1) as eluent. Fractions of each polarity (300 mL) were collected and labeled A–E. A second chromatographic separation of fractions B (105 mg), and E (87 mg) under the same conditions afforded 4 (51 mg) and 3 (34 mg), respectively. Physical and spectroscopic data were consistent with previous reports^7,17 (see Supplemental information). Zaluzanin C (3) was obtained as colorless prisms after crystallization from CH₂Cl₂-MeOH, which were suitable for X-ray diffraction analysis.

Ivalin (6) and Ivalin Acetate (7)

The EtOAc extract (1 g) from Z. triloba was subjected to separation under the conditions described above for Z. parthenioides. Fraction B (97 mg) was purified on a silica gel column, with hexane-EtOAc (2:1, 500 mL, and 1:3, 150 mL) as eluent, collecting 20 mL eluates. Compound 7 (13 mg) was isolated from eluates 11-16, while 6 (21 mg) was obtained from eluates 32-43. Physical and spectroscopic data were consistent with previous reports^29,30 (see Supplemental information). Ivalin (6) was obtained as colorless prisms by slow evaporation from a hexane-EtOAc (1:3) solution at room temperature, which were suitable for X-ray diffraction analysis.

Quantification of Sesquiterpene Lactones in Infusion of Aerial Parts of Z. augusta, Z. parthenioides and Z. triloba

A portion of the EtOAc fraction (60 mg) of each infusion of Z. augusta, Z. parthenioides, and Z. triloba was analyzed by HPLC in triplicate to quantify zaluzanin A (1), zaluzanin C (3), and ivalin (6). Samples of these fractions (2.5 mg) were dissolved in CH₃CN (5 mL) and analyzed using standard curves constructed from solutions (0.10, 0.15, 0.25, 0.3, and 0.4 mg/mL) of pure samples of 1, 3, and 6 in CH₃CN. The extracts (60 mg) contained 26, 30, and 28 mg of 1, 3, and 6, respectively.

Single Crystal X-ray Diffraction Analysis of Compound 3

Data were acquired on a Bruker Smart 6000 CCD diffractometer, using Mo Kα radiation (λ = 0.7073 Å). A total of 1321 frames were collected, at a scan width of 0.3° and an exposure time of 10 s/frame. These data were processed with the SAINT software package, provided by the diffractometer manufacturer, by using a narrow-frame integration algorithm. An empirical absorption correction was applied. Crystal data were, C₁₅H₁₈O₃, M = 246.29, monoclinic, space group P2₁, a = 11.927(5) Å, b = 12.998(5) Å, c = 13.102(5) Å, V = 2008.7(1) Å³, Z = 2, Z′ = 3, ρ = 1.22 mg/mm³, μ(MoKα) = 0.084 mm⁻¹, total reflections = 13 495, unique reflections = 6719 (R_int 0.07%), observed reflections = 3025. The structure was solved by direct methods using the SHELXS-97 program. For structural refinement, nonhydrogen atoms were treated anisotropically, and hydrogen atoms, included in the structure factor calculation, were refined isotropically. Final R indices were [I > 2σ(I)] R1 = 4.8% and wR2 = 9.5%. Largest difference peak and hole, 0.105 and −0.135 e.Å³.

Single Crystal X-ray Diffraction Analysis of Compound 6

The data were collected on an Agilent Xcalibur Atlas Gemini diffractometer using the enhance CuKα X-ray source radiation (λ = 1.54184 Å) at 293(2) K in ω scan mode. Unit cell refinements using 5022 machine-detected reflections were made with the software CrysAlisPro, Agilent Technologies, v.1.171.34.49. Crystal data were C₁₅H₂₀O₃, M = 248.31, orthorhombic, space group P2₁2₁2₁, a = 6.89340(1) Å, b = 11.3914(3) Å, c = 34.7740(8) Å, V = 2730.7(1) Å³, Z = 4, Z′ = 2, ρ = 1.21 mg/mm³, μ(CuKα) = 0.666 mm⁻¹, total reflections = 13 339, unique reflections = 5315 (R_int 0.01%), observed reflections = 4684. The structure was solved by direct methods using the SHELXS-97 program. For structural refinement, nonhydrogen atoms were refined anisotropically, and most hydrogen atoms were refined at geometrically idealized positions on their parent atoms. Final R indices were [I > 2σ(I)] R1 = 3.3% and wR2 = 7.9%. Largest difference peak and hole, 0.146 and −0.110 e.Å³. The software Olex2 v.1.1.5³¹ allowed to calculate Flack parameter³² x = 0.00(19) and Hooft parameter³³ y = 0.08(8). For the inverted structure, these parameters were x = 0.99(19) and y = 0.92(8), respectively.

Crystallographic data (excluding structure factors) of 3 (deposition number 227001) and 6 (deposition number 2270010) were archived in the Cambridge Crystallographic Data Centre from where they can be obtained, free of charge, via http://www.ccdc.ac.uk./data_request/cif.

Supplemental Material

sj-docx-1-npx-10.1177_1934578X231184010 - Supplemental material for Chemical Composition of Plants of the Genus Zaluzania

Supplemental material, sj-docx-1-npx-10.1177_1934578X231184010 for Chemical Composition of Plants of the Genus Zaluzania by J. Martín Torres-Valencia, Reyna Zeferino-Díaz, Laura A. Ortiz-León, Miriam Téllez-Reyes and R. Inés Escamilla-Baños in Natural Product Communications

Footnotes

Acknowledgments

Partial financial support from CONACYT-Mexico (grant No. 238206) is acknowledged. RZD thanks CONACYT for fellowship No. 418442. We are grateful to Professor Manuel González Ledesma of the Área Académica de Biología (U.A.E.H.) for the identification of Z. parthenioides and Z. triloba, and to Angelina Hernández Barragán, Department of Chemistry, CINVESTAV-IPN, Mexico, for her invaluable support on X-ray diffraction analysis.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Consejo Nacional de Ciencia y Tecnología (grant number 238206).

ORCID iD

J. Martín Torres-Valencia

Supplemental Material

Supplemental material for this article is available online. Spectroscopy data and NMR spectra of compounds 1–4, 6, and 7 are available free of charge at

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