Phytochemical Information and Pharmacology of European Orchids: Comparison
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Please note this is a comparison between Version 2 by Sirius Huang and Version 1 by Miriam Bazzicalupo.

The Orchidaceae family has thousands of members, and most of them are mentioned in the folk medicine of nations around the world. The use of terrestrial orchids in European and Mediterranean regions has been reported since ancient times. Plant collection for human use is still listed as one of the main threats for terrestrial orchids (i.e. harvesting for Salep), alongside other menacing factors such as wrong habitat management and disturbance to symbionts, such as pollinators and mycorrhizal fungi.

Here, phytochemical data are discussed to evaluate the presence of bioactive compounds of pharmacological relevance. Furthermore, it is debated whether the presence of these compounds could support the therapeutic employment of the different orchid organs.

  • ethnobotany
  • Orchidaceae
  • biological properties
  • threatened species

1. Introduction

Family Orchidaceae, with approximately 28,000 species distributed worldwide except in the poles and deserts, is considered one of the most fascinating and diverse group of plants among angiosperms [1,2][1][2]. In fact, orchids show a wide variety of life forms, habitat preferences, reproductive strategies, sizes, colours, and scents, characteristics that have placed them at the centre of the attention of many researchers and passionate people [2,3,4][2][3][4]. Despite their evolutionary success, orchids are among the most endangered plants in the world [2[2][5],5], mainly because of their strict dependency on interactions with pollinators and mycorrhizal fungi for spreading and persistence, which leads to species being negatively affected by climate change, use of pesticides, anthropogenic pressure, human harvesting, etc. According to recent estimates, hundreds of species are threatened, with terrestrial orchids particularly represented in the IUCN Red list [6,7,8][6][7][8]. All members of Orchidaceae have therefore been included in Appendix II or higher of the Convention on International Trade in Endangered Species, CITES. Orchids are indeed highly represented in the commerce, being traded legally or not for their ornamental value, or as source of components for cosmeceuticals and medicine, or as food [9,10][9][10]. Orchids are also known in the folk tradition of many nations around the world [11,12,13][11][12][13]. Since ancient times, orchids have been used as nourishment and have also been employed in medicinal preparations. The first descriptions of orchids and their therapeutic utilizations have been found in China since 2800 B.C. [14], while in ancient Ayurvedic preparation Ashtavarga, four terrestrial orchids are included (Herminium edgeworthii (Hook.f. ex Collett) X.H. Jin, Schuit., Raskoti and Lu Q. Huang; Habenaria intermedia D. Don, Crepidium acuminatum (D. Don) Szlach., and Malaxis muscifera (Lindl.) Kuntze) [12,13,15][12][13][15]. It is reported that orchids were used for the treatment of diseases and ailments such as tuberculosis, paralysis, gastrointestinal problems, chest pains, syphilis, arthritis, cholera, cancers, piles, boils, muscular pains, menstrual disorders, diarrhoea, leucorrhoea, hepatitis, spermatorrhea, rheumatism, wounds, sores, and others [11,12,13,15][11][12][13][15]. Therefore, it has been stated that orchids possess a high medicinal potential as a source of drugs [11,13,15,16,17][11][13][15][16][17].
Orchids are known to produce secondary metabolites of physiological, ecological, and pharmacological relevance [13,18,19,20,21,22,23][13][18][19][20][21][22][23]: among these, compounds such as stilbenes, dihydrostilbenoids, phenanthrenes, alkaloids, terpenes, flavonoids, anthocyanins, and phenolic acids have been found [12,13,23][12][13][23]. However, notwithstanding the number of species in the family, relatively few studies were dedicated to orchid phytochemistry and biological activities, and many traditional uses remain unvalidated [12,15][12][15]; this is particularly evident for European species, although it is known that Europe has a well-established traditional use of these plants [12,13,24,25,26,27,28][12][13][24][25][26][27][28]. One of the first reporting orchids in medicine was the Greek Theophrastus (c.372–288 B.C.), who named orchids on the base of the similarity of their tubers with male testicles (“όρχεις”) and suggested their use as an aphrodisiac [29]. Pliny the Elder (23–79 A.C.) stated that sexual desire could be increased by consuming the harder/bigger bulb, while it could be repressed by consuming the softer/smaller one. Furthermore, according to Pliny, underground portions of orchids could be employed to cure mouth sores or to clear the phlegm from the chest [13,30][13][30]. The belief that the orchids could influence the sexual sphere has been then proposed for centuries: Petronius, in his Satyricon (1st century A.C.), described the consumption of orchids among prostitutes; in the texts of Dioscorides and Galen, these plants were cited following the Doctrine of Signatures, as also reported by Paracelsus (1493–1551) and Linnaeus (1707–1778) [31].
The European Union, in addition to applying the CITES, started establishing the Habitat Directive and the Natura 2000 Network about thirty years ago, purportedly created for the protection of habitats and animal and plant species. Various orchids are also included in national and regional red lists, thus the collection of threatened species is now regulated or forbidden [5,27][5][27].

2. Phytochemical Information and Pharmacology of European Orchids

Researchers found phytochemical information for 88 orchids diffused in European territories, of which 85 were selected based on the presence of known bioactive compounds; details on infraspecific taxa were also included. Most of the available information consists in metadata collected from articles written for very different aims, namely works on chemical ecology for the evaluation of plant–pollinator interactions, or phytochemical analyses on the presence of specific classes of compounds compared in different taxa, even in a phylogenetic key (i.e., Strack et al. [168][32]). From a phytochemical point of view, the flowers/inflorescence are therefore the portions on which more information is reported, with more than 70 species being investigated; the most studied are O. mascula s.l., A. coriophora s.l., G. conopsea, H. robertianum, Ophrys sphegodes complex, and P. bifolia. Specific groups of chemical components of the leaves were found for 33 species, especially thanks to the work of Williams [169][33], van Damne and colleagues [170[34][35],171], and Balzarini [172][36]; the most cited orchids are E. atrorubens (Hoffm.) Besser, E. helleborine, N. ovata, and A. papilionacea. Phytochemical details for the hypogean apparatus (tuber/rhizome) are available for a total of 17 species, especially deriving from investigations on phytoalexin compounds and their production in response to external stimuli (see below). Many authors focused on the biochemicals and biological properties of extracts from tuber of D. viridis (L.) R.M. Bateman, Pridgeon and M.W. Chase, and G. conopsea (two orchids presenting a wide global distribution); the latter taxon has been already the subject of a review [16]. These two species in particular (and a few others as well, i.e., Goodyera repens (L.) R.Br., Orchis mascula), being also present in the folk traditions and pharmacopoeia of other extra-EU countries, have therefore been studied by non-European working groups. Finally, starch [173][37], ash, sugar, sucrose [13], and glucomannan [38,84][38][39] were detected in orchid tubers.

2.1. Bioactive Compounds, Tissue Distribution and Main Biological Properties

Among secondary metabolites, polyphenols and derivatives are largely studied, and the various polyphenol subgroups have been frequently reported in the investigated species. These subgroups consist in compounds such as flavonoids (including flavanones, anthocyanins, flavonols) and phenolic acids (including caffeic acid or chlorogenic acid). Among the health-promoting activities of polyphenols, antioxidant, cytotoxic, anti-inflammatory, antihypertensive, skin-preserving, and anti-diabetic properties have been evaluated by both in vitro and in vivo assays [240][40].
The extensive investigation performed by Strack et al. [168][32] and Uphoff [177][41] on the anthocyanin content and relative patterns of abundance allowed to obtain information for many European orchids. Interestingly, the relative content of identified pigments (chrysanthemin, cyanin, seranin, orchicyanin I, ophrysanin, serapianin, orchicyanin II, mecocyanin, and epipactin), and unidentified ones from this water-soluble class of flavonoids was found to be highly variable but genus specific. According to these authors, Arditti and Fisch [241][42] and Uphoff [242][43], the mixture of acylated and non-acylated anthocyanins underlies the great variability of orchid flower colours, with orchicyanin I recognized as one of the key compounds responsible for intensive flower pigmentation. With about 600 identified compounds, anthocyanins have strong antioxidant properties and a validated defensive role for plants against biotic or abiotic stressors. These pigments are also active in delaying organ senescence, therefore contributing to the prolongation of tissue survival and increasing reproductive success. Patterns of anthocyanins also have a well-documented role in pollinator attraction [243,244][44][45]; i.e., in the case of Ophrys species, chrysanthemin and ophrysanin have been traced to the darker pigmentation of the labellum [168][32], which is typically one of the traits helping the flower in mimicking the female of the insect by which it is pollinated. Intriguingly, Vignolini and colleagues [218][46] found that the appearance of the speculum in O. speculum depends not only on the morphology of the surface cell layer, but also on the concentrated localization of cyanidin pigments. Colourful pigmentation (which is based on anthocyanins) has also been linked to the increased attention of people in regards of plants [4].
In orchid species, compounds with a recognized role as phytoalexins have been found (see [13,16,178,179,194,227,245,246,247][13][16][47][48][49][50][51][52][53]). These secondary metabolites are a super-group of compounds (such as flavonoids, terpenoids, coumarins, stilbenoids/phenanthrenes and derivatives, glycosteroids and alkaloids). They are categorized as phytoalexins if their production starts in response to microbial attacks [248][54], playing a key role in the resistance against groups of microorganisms. For instance, they are known for exerting antibacterial [17] and fungistatic activity ([13] and references therein, [227][50] and references therein). Among phenanthrenes and derivatives recognized as phytoalexins, hircinol, militarine, loroglossol, and orchinol are the most common molecules recorded [13,249][13][55]. Studies on orchid phytoalexins have been conducted, especially on the hypogean portions (i.e., Orchis mascula, O. militaris, H. robertianum). However, these compounds, such as loroglossin in A. papilionacea [179][48], were also reported in flowers and leaves. Phytoalexins such as loroglossol and hircinol recently re-isolated from the tuber of H. robertianum by Badalamenti et al. [17], showed in vitro antioxidant and immuno-stimulatory effects, together with anti-microbic and anti-cancer activities. 4-hydroxybenzyl alcohol (or p-hydroxybenzyl alcohol) is another well-known molecule that has been detected in different orchid tissues and species, for example, in the tuber of A. coriophora ([13] and references therein) or in the flowers of D. maculata [184][56]. This compound has interesting biological activities as assessed by both in vitro and in vivo tests, such as: effects on the central nervous system (sedative, hypnotic, sleep-promotion properties [250][57], neuroprotective and anti-Parkinson activity [251][58], antioxidant, antimicrobial, and skin preserving properties, including anti-tyrosinase activity [13,252][13][59]).
Alkaloids were found in different portions of several orchids, including leaves and flowers. These molecules, in addition to being in some cases recognized as phytoalexins [248][54], are well-known for their activity on the animal nervous system. Alkaloids were detected in species like C. longifolia, Goodyera repens and E. helleborine [13,182,204][13][60][61]. In this latter orchid, oxycodone and other morphinan/indole derivatives were also found in the flower nectar by Jakubska et al. [205][62], which proposed that these molecules could be at the basis of the sluggish effect and the disorientation of visiting insects.
Phytochemicals detected in the flowers/inflorescence (whose presence has been mainly collected from anthecology articles) belong to several classes: apart from polar compounds/less volatile ones like polyphenols [176[56][63][64],184,253], saturated and unsaturated hydrocarbons, fatty acids and derivatives, and ketones are frequently found and proposed to contribute to pollinator attraction or herbivory avoidance ([175][65] and references therein); the same role has been hypothesized for other classes such as aldehydes, alcohols, esters, coumarins, or terpenes, which are well-known as fragrant compounds. Among these, coumarin and terpenes are important metabolites that possess various physiological, ecological, and therapeutic functions. For example, orchid-derived compounds belonging to diterpenoids, sesquiterpenoids, and triterpenoids have shown interesting antiviral activities, including anti-SARS-CoV-2 properties due to the inhibitory competition on 3CL viral protease. Other compounds such as eugenol and methyl–eugenol are recognized as spicy and have several biological properties, among which are anaesthetic and hepatotoxic [13].

2.2. Causes of Biochemical Variations

Some species have been chemically analysed in several studies, but the guilds of compounds were found to be very variable. This may depend on several aspects, including the extraction methods and the analytical tools chosen [20,254,255][20][66][67]. For instance, more polar compounds such as polyphenols are less volatiles and therefore the use of protic solvents (such as methanol, diethyl ether or water–ethanol) results in substantially different chemical characterizations in respect to dynamic headspace sorption methods (i.e., [176,185,192][63][68][69]). Individual situations also contribute to changing metabolic processes and thus varying phytochemical profiles. It is known that the concentration of antioxidants such as polyphenols or carotenoids can change depending on plant physiological/phenological status ([256][70] and references therein). For example, Maleva et al. [237][71] found that leaves from plants belonging to disturbed habitats showed an increased content of flavonoids. The sources of variability in orchid floral colour and scent have been already reviewed by Dormont et al. [257][72]. Concerning the content of anthocyanins in particular, changes have been recorded in plants collected in different populations [168][32] or in individuals facing nutrient deficiency ([243][44] and references therein). Differences in alkaloid content between plants from diverse countries have been noted ([13] and references therein). Chemical patterns can also differ due to random genetic drift [233][73]; some species were found to be phylogenetically similar but chemically distant [258][74], showing significant differences even between subspecies. Ayasse et al. [259][75] demonstrated that odour variation between plants of Ophrys sphegodes favoured cross pollination; furthermore, Schiestl and Ayasse [260][76] observed that pollinated flowers increased the production of the repellent farnesyl hexanoate. In support to these reports, Dormont et al. [261][77] confirmed that factors such as habitat characteristics, flower age, pollination, circadian rhythm, herbivory, and inflorescence morphology are responsible for chemical variations in Orchis mascula. Finally, as previously mentioned, the production of phytoalexins increases in tissues under microbial colonization. In this context, it is still to define whether the content of these secondary metabolites is dependent on the plant, or on hosts such as mycorrhizal fungi [13,262,263][13][78][79]. The relative abundance of the biochemical components should therefore be considered rather as a “snapshot” of the species’ phytochemistry in response to a given environmental (physiological or ecological) situation.

2.3. Validation of Traditional Uses

When comparing the data on portions used as herbal remedies and the available scientific literature on phytochemistry/biological activities, only a few direct matches can be found. In the following cases, however, only a partial explanation that usually stops at in vitro evaluations is available.
Dactylorhiza romana subsp. georgica: Tuber was cited for the cure of cough. Kotiloğlu et al. [190][80] and Bozkir et al. [191][81] recently analysed different extracts, including ethanol extracts from both dried and fresh tuber. Polyphenols and flavonoids were detected. Among constituents, p-hydroxybenzoic acid, kaempferol, rosmarinic acid, and caffeic acid were present. In both these studies, extracts demonstrated antioxidant and antimicrobial activities.
Gymnadenia conopsea: In Europe, the tuber was cited for the treatment of lung diseases [49][82]. As mentioned, this species is widespread; thus, other available reports on its medicinal use are originally from Asia, as well as scientific studies on its phytochemistry/biological activities. Compounds such as gymconopins, gymnosides, dactylorhins, bulbocodins, arundinins, batatasin, dactylose A-B, coelovirins A-E, loroglossin militarine, coumaric acids, 4-hydroxybenzyl alcohol, vanillic acid, syringol, eugenol, gastrodin, arctigenin, lappaol, quercitin-3, and 7-di-O-β-D-glucopyranoside have been detected thanks to the work of several authors ([16] and references therein). Among the biological properties tested, antioxidant, antimicrobial, anti-viral, antianaphylaxis, immunoregulatory, sedative, and hypnotic activities have been reported.
Himantoglossum robertianum: The tuber was prepared in infusion as medicinal tea and was cited for the cure of coughs. Badalamenti et al. [17], as mentioned above, worked on two phenanthrenes, loroglossol and hircinol, isolated from the tuber. The compounds exhibited in vitro antioxidant and immune–stimulatory activity, increasing the activity of superoxide dismutase (SOD), catalase (CAT), and glutathione S-transferase (GST) in polymorphonuclear leukocytes (PMN); they also have antimicrobial properties as demonstrated by tests with Escherichia coli and Staphylococcus aureus; they have also anti-proliferative effect on gastric tumour cell lines by induction of apoptotic effect. However, the importance of other components of the plant complex in the entire traditional preparation cannot be excluded.
As mentioned above, glucomannan, ash, mucilage, water, and starch have been detected in orchid hypogean portions, therefore justifying their alimentary consumption, and indirectly, that of Salep. However, in this case, some authors in the XIX century already argued that its nutritive potential was overestimated ([13] and references therein). No scientific evidence has been found demonstrating the claimed beneficial and aphrodisiac activities of Salep or constitutive portions of the species employed. Some of the secondary metabolites from orchid tubers (i.e., polyphenols/flavonoids) have well-documented biological properties ([240][40] and references therein) but have no confirmed role in Salep. It should also be remembered that orchid tubers are strongly processed before pulverisation [264][83] and that spices such as cinnamon or ginger are added as flavours [13].
Some of the traditional uses cited can be at least partially explained by the available literature on phytochemicals. Compounds such as p-hydroxybenzyl alcohol (see above) can underline uses of tubers as anti-inflammatory or for the treatment of skin/gastrointestinal problems (i.e., A. coriophora or A.morio); the same can be hypothesized for antimicrobial molecules such as orchinol, loroglossol, militarine, or orchinol found in different species (i.e., Orchis spp., Anacamptis spp., Himantoglossum spp., Dactylorhiza spp., Gymnadenia spp., N. ovata). The presence of p-hydroxybenzyl alcohol, known as neuroactive and sedative, could be also at the basis of the alleged psychoactive properties of A. pyramidalis tuber or of D. maculata flowers. The tuber of D. osmanica was used to cure coughs, inflammation, ulcers, and skin boils: Kiziltas et al. [188][84], while investigating the tuber extract to evaluate other biological properties, found that fumaric acid, p-coumaric acid, rosmarinic acid, and vanillic acid were present. A contribution of these compounds to the beneficial effect of D. osmanica’s tuber use cannot be excluded. Leaves and flowers of D. sambucina were prepared in infusion and cited for cough treatment: these portions were chemically investigated by Pagani [176][63], who listed health-promoting compounds such as coumarin, quercetin derivatives, or chlorogenic acid. In this species, water-soluble antioxidant anthocyanins such as cyanin, seranin, ophrysanin, orchicyanin II were recognized by Strack et al. [168][32]; quoted antibacterial terpenoids such as caryophyllene were found in the floral scent [192][69]. Leaves of E. helleborine, used to cure wounds, showed the presence of the antioxidant, antimicrobial, and wound healer quercetin [169][33]. Furthermore, alkaloids were detected in this species by Lüning [204][61].
Finally, leaves/aerial parts of both P. bifolia and P. chlorantha were employed as herbal remedies, to cure rheumatism, neuralgias, and skin ulcers, respectively. In the case of P. bifolia, well-known flavonoids like quercetin and kaempferol were detected in these tissues by Williams [169][33]; the presence of phenolic compounds, although variable between polluted and unpolluted sites, was confirmed by Maleva et al. [237][71].
Finally, there are species whose selected portions have been analysed phytochemically and for testing biological activities not reported in the ethnobotanical literature.
Anacamptis coriophora subsp. fragrans: Essential oil isolated from the inflorescence bearing mature seeds was characterized by El Mokni et al. [174][85]. Constituents were mainly methyl-(E)-p-methoxycinnamate, 13-heptadecyn-1-ol, 2,5-dimethoxybenzyl alcohol, 4-(1,1,3,3-tetramethylbutyl)-phenol; 7,9-di-tert-butyl-1-oxaspiro (4,5) deca-6,9-diene-2,8-dione; 10-dodecenol, p-cresol, methyl (Z) p-methoxycinnamate, 2-dodecenal, and methyl cinnamate. Though the EO showed a weak antioxidant activity, anti-proliferative effect on carcinoma cells BxPC3 and human ovarian cancer cells OV2008 was observed.
Anacamptis pyramidalis: Mahomoodally et al. [181][86] analysed water and ethanol tuber extracts, which showed the presence of flavonoids, gastrodin/dihydroxybenzoic acid/caffeic acid/acacetin derivatives, parishin, and citric acid. Extracts exhibited high antioxidant activity and inhibitory potential against tyrosinase, α-amilase, and α-glucosidase.
Himantoglossum robertianum: Hydroalcoholic flower extract was phytochemically characterized: among the different compounds, researchers found scopoletin, kaempferol-3-O-rutinoside, caffeic acid, chlorogenic acid, epicatechin, roifolin, protocatecuic acid, vitexin, isovitexin, coumaric acid, catechin, and apigenin. The extract exhibited antioxidant and skin-preserving properties. Inhibitory activity against skin matrix-degrading enzymes (elastase, collagenase) was evidenced, together with improvement of HaCat keratinocytes viability after treatment with H2O2, and improvement of cell migration rate [213][87].
Dactylorhiza romana subsp. georgica: Antioxidant and antimicrobial activities of the tuber from this species have been already cited above. Kotiloğlu et al. [190][80] and Bozkir et al. [191][81] also observed antidiabetic properties by evaluating α- amylase and α-glucosidase inhibitory activity during in vitro assays.
Dactylorhiza osmanica: This species and its phytochemicals have been already mentioned above. Kiziltas et al. [188][84] also found that both tuber and flowering stem extracts have anti-Alzheimer and anti-diabetes properties, as evaluated by in vitro enzymatic assays (inhibitory activity against acetylcholinesterase (AChE), α-glycosidase, and α-amylase).
Epipactis helleborine and N. ovata: The rhizomes of these species were cited as medicinal, but information on compounds and biological properties is available only for the leaves. Mannose-specific lectins obtained from homogenate plant material were tested on MT-4, HEL, HeLa, and MDCK cell lines and showed several antiviral activities against HIV-1, HIV-2, CMV, RSV, and influenza A [170,171,172][34][35][36].
Orchis mascula: Ethanolic flower extracts showed saponins, flavonoids, anthraquinone, terpenoids, tannins, cyanogenic glycosides, and cardiac glycosides [226][88]. Compounds such as 2-methyl-Z,Z-3,13-octadecadienol, n-hexadecanoic acid, 2 furancarboxaldehyde 5-(hydroxymethyl), 2-propanone, 1,1-diethoxy, D-allose, 1,6-anhydro-α-D-galactofuranose, 3-acetylthymine, DL-4-amino-3-hydroxybutyric acid have been found. Antimicrobial activity against various pathogens such as Salmonella paratyphi, Klebsiella oxytoca or Staphylococcus aureus has been assessed.

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