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Identification of the Volatile Components of Galium Verum L

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Identification of the Volatile Components of Galium Verum L molecules Article Identification of the Volatile Components of Galium verum L. and Cruciata leavipes Opiz from the Western Italian Alps Aldo Tava 1,* , Elisa Biazzi 1, Domenico Ronga 1,2 and Pinarosa Avato 3 1 CREA Research Centre for Animal Production and Aquaculture, viale Piacenza 29, 26900 Lodi, Italy; [email protected] (E.B.); [email protected] (D.R.) 2 Centro Ricerche Produzioni Animali—CRPA S.p.A., viale Timavo, n. 43/2, 42121 Reggio Emilia, Italy 3 Dipartimento di Farmacia-Scienze del Farmaco, Università, via Orabona 4, 70125 Bari, Italy; [email protected] * Correspondence: [email protected]; Tel.: +39-0371-40471; Fax: +39-0371-31853 Academic Editor: Maria Carla Marcotullio Received: 17 April 2020; Accepted: 15 May 2020; Published: 16 May 2020 Abstract: The chemical composition of the volatile fraction from Galium verum L. (leaves and flowers) and Cruciata laevipes Opiz (whole plant), Rubiaceae, was investigated. Samples from these two plant species were collected at full bloom in Val di Susa (Western Alps, Turin, Italy), distilled in a Clevenger-type apparatus, and analyzed by GC/FID and GC/MS. A total of more than 70 compounds were identified, making up 92%–98% of the total oil. Chemical investigation of their essential oils indicated a quite different composition between G. verum and C. laevipes, both in terms of the major constituents and the dominant chemical classes of the specialized metabolites. The most abundant compounds identified in the essential oils from G. verum were 2-methylbenzaldheyde (26.27%, corresponding to 11.59 µg/g of fresh plant material) in the leaves and germacrene D (27.70%; 61.63 µg/g) in the flowers. C. laevipes essential oils were instead characterized by two sesquiterpenes, namely β-caryophyllene (19.90%; 15.68 µg/g) and trans-muurola-4(15),5-diene (7.60%; 5.99 µg/g); two phenylpropanoids, benzyl alcohol (8.30%; 6.71 µg/g), and phenylacetaldehyde (7.74%; 6.26 µg/g); and the green-leaf alcohol cis-3-hexen-1-ol (9.69%; 7.84 µg/g). The ecological significance of the presence of such compounds is discussed. Keywords: Cruciata laevipes Opiz; Galium verum L.; essential oil composition; GC/FID; GC/MS; Rubiaceae; benzyl alcohol; β-caryophyllene; methylbenzaldehyde; phenylacetaldehyde; VOCs; Alpine plants 1. Introduction Galium verum L. and Cruciata laevipes Opiz (syn. Galium cruciata (L.) Scop.) belong to the Rubiaceae plant family, namely to the Rubieae monophyletic group, the only tribe classified within the family. Phylogenetic studies [1,2] showed that the tribe can be separated into two groups, one of them including both genera, Galium, the largest genus within the tribe with 655 species, and Cruciata including only 9 species. In addition, based on DNA sequence data, it was demonstrated that the two species G. verum and C. laevipes fall into two separated clades, whose members are also characterized by some morphological differences. G. verum L., is a herbaceous perennial species largely spread across most of Europe, North Africa, and temperate Asia. It grows between 0 and 1800 m above the sea level in different habitats, including dry-sand meadows, rocky outcrops, roadsides, dunes, and seashores. G. verum is a scrambling plant, with 60–120 cm long stems that root frequently when they touch the soil. The leaves are linear Molecules 2020, 25, 2333; doi:10.3390/molecules25102333 www.mdpi.com/journal/molecules Molecules 2020, 25, 2333 2 of 11 needle-like, shiny dark green, with prominently revolute margins, covered with hair underneath, grouped in whorls of eight–twelve. It blooms in July–September producing fragrant yellow flowers, clustered in dense panicles. The fruits are black schizocarps [3]. The name of the genus derives from the Greek term “gala”, milk, referring to the common use of plants of this species to curdle milk when producing cheese. G. verum is well-known by the common name of lady’s bedstraw or yellow spring bedstraw (madder family), from the old practice to use its foliage to stuff mattresses. In addition, the flowers give a yellow pigment that has been employed traditionally to color food, and the roots produce a red dye that is used to color wool. The plant also has some traditional medical uses as a diuretic, choleretic, and spasmolytic [4]. C. laevipes Opiz, commonly known as crossword or smooth bedstraw, is also distributed across Europe and Asia, growing between 0 and 1500 m above the sea level. It is a perennial herb, 10 to 60 cm tall; with quadrangular stems; and leaves that are three-nerved and whorled in clusters of four. The flowers are yellow, between five and nine on each top, blooming in May–June; their peduncles carry two bracteoles each and are filled with dense hairs [3]. This species grows in open woodland, waysides, and pastures, and prefers calcareous soils [5]. C. laevipes has long been known in folk medicine for its wound-healing properties, and it was employed in the past in both external and internal applications. These latter include remedies to treat obstructions of the stomach and bowels, to stimulate appetite and as a remedy for rheumatism and dropsy [6]. The two plant species, G. verum and C. laevipes are also widespread in Italy, all over the country, especially in the Alpine regions, and were also commonly found in the Western Italian Alpine pasture vegetation [7]. Phytochemical studies have shown that both Galium and Cruciata genera synthesize many different classes of specialized metabolites, such as iridoid glycosides, antraquinones, phenolics, flavonoids, and coumarins [8–17], possibly accounting for the biological properties highlighted for some of the species. They also produce terpenoids and aromatic essential oils [18–21]. The aim of this work was to determine the flavor constituents of G. verum L. and C. laevipes Opiz collected in the wild Italian alpine region, in order to fully characterize their volatile fraction for the first time. 2. Results Volatiles identified in the aerial parts of G. verum and C. laevipes are reported in Table1, listed in order of elution on a DB-5 column. Leaves and flowers from G. verum were analyzed separately, while, due to their small size, flowers from C. laevipes could not be isolated and for this species the whole plant was analyzed. In total, more than 70 compounds were identified in both species, on average amounting to 92%–98% of the total. Chemical investigations of their essential oils indicated a quite different composition between G. verum and C. laevipes, both in terms of major constituents and the dominant chemical classes of the specialized metabolites (Table1; Figure1). The chemical structures of the most abundant detected compounds are reported in Figure2. Aldhehydes were the most abundant chemical class of components amounting to 43.71 0.01% ± (18.91 0.44 µg/g) and to 42.64 0.46% (94.93 2.33 µg/g) in G. verum essential oils from leaves ± ± ± and flowers, respectively. The second major chemical class was represented by alcohols in the leaves (25.70 1.67%, 11.11 0.47 µg/g) and by terpenes in the flowers (32.42 1.24%, 72.15 1.77 µg/g). ± ± ± ± Alcohols were also present in high amount (12.09 0.24%, 26.92 0.89 µg/g) in the essential oils from ± ± the flowers of G. verum (Table1). Molecules 2020, 25, 2333 3 of 11 Table 1. Composition (% and µg/g fresh weight) of volatiles from Galium verum leaves and flowers and Cruciata laevipes whole plant. Galium verum Cruciata laevipez Leaves Flowers Whole Plant Compound a AI tab b AI c % µg/g % µg/g % µg/g 1 3-Methyl-3-buten-1-ol 731 737 - - 1.78 0.12 3.96 0.21 0.22 0.03 0.17 0.02 ± ± ± ± 2 3-Methyl-1-butanol 740 741 - - - - 0.36 0.06 0.29 0.04 ± ± 3 Pentanol 765 768 tr tr 1.07 0.19 2.38 0.46 0.33 0.12 0.27 0.09 ± ± ± ± 4 cis-2-Penten-1-ol 771 775 1.73 0.57 0.75 0.26 tr tr 0.29 0.08 0.23 0.06 ± ± ± ± 5 Hexanal 799 799 0.81 0.26 0.35 0.11 0.52 0.07 1.15 0.17 0.55 0.06 0.44 0.06 ± ± ± ± ± ± 6 4-Hydroxy-4-methyl pentan-2-one 831 837 - - - - 0.51 0.07 0.41 0.06 ± ± 7 trans-2-Hexenal 851 851 tr tr - - 0.47 0.06 0.38 0.06 ± ± 8 cis-3-Hexen-1-ol 855 854 17.34 2.41 7.49 0.87 3.35 0.13 7.47 0.40 9.69 1.18 7.84 1.17 ± ± ± ± ± ± 9 Hexanol 870 869 0.39 0.11 0.17 0.04 2.26 0.10 5.03 0.14 0.27 0.04 0.22 0.04 ± ± ± ± ± ± 10 Heptanal 904 902 0.10 0.04 0.04 0.02 - - 0.16 0.02 0.13 0.02 ± ± ± ± 11 trans-2-Heptenal 958 955 - - - - 0.26 0.01 0.21 0.01 ± ± 12 Benzaldehyde 960 959 1.08 0.06 0.47 0.04 0.30 0.03 0.67 0.08 2.05 0.21 1.66 0.21 ± ± ± ± ± ± 13 Oct-1-en-3-ol 980 981 0.20 0.02 0.09 0.00 tr tr 1.92 0.38 1.56 0.35 ± ± ± ± 14 6-Methyl-5-hepten-2-ol 992 991 tr tr - - 0.17 0.03 0.14 0.03 ± ± 15 Decane 1000 999 - - - - 0.29 0.02 0.24 0.02 ± ± 16 cis-3-Hexenylacetate 1004 1005 3.46 1.30 1.50 0.60 1.12 0.02 2.50 0.04 2.44 0.27 1.97 0.28 ± ± ± ± ± ± 17 2,4-Heptadienal 1005 1007 0.16 0.02 0.07 0.01 - - 0.21 0.01 0.17 0.01 ± ± ± ± 18 Benzyl alcohol 1042 1034 4.37 0.01 1.89 0.04 1.98 0.04 4.42 0.15 8.30 0.24 6.71 0.24 ± ± ± ± ± ± 19 Phenylacetaldehyde 1051 1042 5.19 0.62 2.25 0.32 3.43 0.23 7.63 0.62 7.74 0.41 6.26 0.52 ± ± ± ± ± ± 20 Linalool 1099 1099 0.51 0.07 0.22 0.04 0.29 0.02 0.65 0.05 0.21 0.02 0.17 0.02 ± ± ± ± ± ± 21 Nonanal 1104 1104 0.38 0.10 0.16 0.04 1.85 0.02 4.12 0.02 0.48 0.04 0.38 0.0.3 ± ± ± ± ± ± 22 2-Phenylethanol 1106 1110 1.68 0.28 0.73 0.14 1.64 0.08 3.66 0.24 1.16 0.12 0.91 0.09 ± ± ± ± ± ± 23 2-Methylbenzaldehyde 1152 d 1153 26.27 1.07 11.59 0.73 24.04 1.07 53.54 3.12 0.21 0.02 0.16 0.01 ± ± ± ± ± ± 24 4-Methylbenzaldehyde 1171 d 1173 7.31 1.49 3.16 0.57 8.45 0.57 18.80 1.01 0.33 0.05 0.26 0.03 ± ± ± ± ± ± 25 Borneol 1165 1174 - - - - 4.07 0.43 3.21 0.32
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