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Phytochemical and Bioactive Properties of Phelypaea Tournefortii – Effect of Parasitic Lifestyle and Environmental Factors

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Phytochemical and Bioactive Properties of Phelypaea Tournefortii – Effect of Parasitic Lifestyle and Environmental Factors ACTAACTA UNIVERSITATISUNIVERSITATIS CIBINIENSISCIBINIENSIS 10.2478/aucft-2020-0010 SeriesSeries E: E: Food Food technologytechnology PHYTOCHEMICAL AND BIOACTIVE PROPERTIES OF PHELYPAEA TOURNEFORTII – EFFECT OF PARASITIC LIFESTYLE AND ENVIRONMENTAL FACTORS – Research paper – Renata PIWOWARCZYK*, Ireneusz OCHMIAN**, Sabina LACHOWICZ***, Ireneusz KAPUSTA****, Zofia SOTEK***** *Department of Microbiology and Parasitology, Institute of Biology, Jan Kochanowski University, Uniwersytecka 7 Street, 25-406 Kielce, Poland; [email protected] **Department of Horticulture, West Pomeranian University of Technology Szczecin, Słowackiego 17 Street, 71-434 Szczecin, Poland; [email protected] ***Department of Fermentation and Cereals Technology, Wrocław University of Environmental and Life Sciences, Chełmońskiego 37 Street, 51-630 Wrocław, Poland; [email protected] ****Department of Food Technology and Human Nutrition, University of Rzeszów, Zelwerowicza 4 Street, 35-601 Rzeszów, Poland; [email protected] *****Institute of Marine and Environmental Sciences, University of Szczecin, Adama Mickiewicza 16 Street, 70-383 Szczecin, Poland; [email protected] Abstract: Some holoparasitic species can become cultivated plants due to their unique chemical composition. A lot of bioactive contents are characteristic for them. Holoparasites of the family Orobanchaceae are known to be an important and rich source of polyphenols, especially metabolites of the phenylethanoid glycosides (PhGs) group. However, only a minority of the species in this family have been phytochemically tested. They are reported to have multiple biological and therapeutic effects and have been used for centuries in traditional Chinese medicine. This is the first study to present phytochemical profiling for a representative of genus Phelypaea. The chemical composition and biological activity in particular organs of the parasite, P. tournefortii, were determined. The interaction with its host, Tanacetum polycephalum (Asteraceae), from different places and altitudes was also studied. We presented the determination of polyphenolic compounds with the UPLC-PDA-MS/MS method, antioxidative effects and inhibitory activities, polyphenols, and nitrates content, ABTS•+, DPPH, FRAP, as well as colour parameters. The polyphenols profile of the parasite and host were different in quality and quantity. Identification of polyphenolic compounds revealed 41 compounds, 15 in the parasite (12 phenylethanoids and 3 anthocyanins), and 26 in the host (mainly flavonoids and phenolic acids). The amount and biological activity of polyphenolic compounds present in Phelypaea was very diverse and depended on the host plant and the parasite's organs, as well as on population altitude. The results show that P. tournefortii is a potential source of functional and pro-health components. They also direct researchers' attention to the parasite's organs, host, and environmental influence. Key words: anthocyanins, holoparasite, host, Orobanchaceae, parasitic plant, altitude factor INTRODUCTION and 2,100 species (Nickrent 2020). They occur The extraordinary characteristics of holoparasitic worldwide, but show the greatest diversity in the species are the reason for the increasing popularity Mediterranean basin, and western and central Asia. of some of these plants as 'super foods' (functional The Caucasus, the Near East, and central Asia are foods), characterised by a high amount of bioactive the probable centres of origin of certain contents. Except for a few non-parasitic autotrophs, holoparasitic genera. However, these areas have not the family Orobanchaceae exclusively includes root been sufficiently explored thus far (Piwowarczyk et hemiparasites and holoparasites with 102 genera al., 2019). The Republic of Armenia is part of the Caucasus, one of the most important biodiversity Received: 20.05.2020 hotspots in the world (Mittermeier et al., 2005). In Accepted in revised form:15.06.2020 Armenia occurs about 40 representatives of 1 Corresponding author. E-Mail address: [email protected] Acta Universitatis Cibiniensis Series E: FOOD TECHNOLOGY 113 Vol. XXIV (2020), no. 1 Orobanchaceae holoparasites. These include, occurring primarily in the Caucasus, and less Orobanche L., Phelipanche Pomel, Cistanche frequently in the Middle East, Asia Minor, Crimea, Hoffmanns & Link, and Phelypaea L. (syn. and Balkans. They occur as parasites on the roots of Diphelypaea Nicolson) genera (Piwowarczyk et al., Asteraceae species like Tanacetum, Centaurea, 2019). Holoparasites of the Orobanchaceae family Psephellus, and rarely, Cousinia. Species belonging are non-photosynthetic, achlorophyllous, root to this genus have an unusual appearance compared parasites. They are fully host-dependent for their to other plants; they are parasitic and have nutritional needs which they obtain through an adaptations for the parasitic lifestyle. These intrusive organ called a haustorium. The preferred perennial herbs are achlorophyllous and possess one hosts vary from species to species and can be of the most intense red flowers among all plants classified into three categories: monophagous, worldwide. Phelypaea tournefortii Desf. primarily oligophagous (dominant), and polyphagous occurs in the Caucasus (Armenia, Azerbaijan, (Piwowarczyk et al., 2019). Holoparasites from the Georgia, and Iran) and in Turkey. It occurs as a Orobanchaceae family possess a significant and rich parasite on the roots of Tanacetum. It generally source of metabolites belonging to the class, grows in the central and southern part of Armenia, phenylethanoid glycosides (PhGs). Only a small in the steppe or on rocky slopes, (1200)1800 - part of holoparasitic species from Orobanchaceae in 2100(2500) m above sea level. Its flowering season the world have been studied for their phytochemical is from May to June, and it usually occurs in properties. Despite this, they were found to have populations of a few dozens to a few hundred shoots many biological and therapeutic effects (Piwowarczyk et al., 2019). The host species, (Scharenberg and Zidorn, 2018). PhG species have Tanacetum polycephalum subsp. argyrophyllum (K. pharmacodynamic properties. They also act as a Koch) Podlech [syn. T. argyrophyllum (C. Koch) neuroprotective, anti-inflammatory, antioxidant, Tzvel.], belonging to the Asteraceae family, is seen cytotoxic, antimicrobial, antiviral, in Transcaucasia and Turkey, and is an important immunomodulating, and enzyme inhibitory factors folk medicinal plant with wide biological activities (Xue and Yang, 2016). To date, over 40 different (Mahdavi et al., 2015). PhGs, predominantly including acteoside and To date, the Phelypaea genus has not been studied echinacoside, have been reported in Cistanche spp. for chemical composition. This is the first attempt (Wang et al., 2015; Piwowarczyk et al., 2020). to characterise P. tournefortii for phytochemical Presumably, 70 natural products have been composition and biological activity. The aim of our described in the Orobanche (among 200 species, ca. research was to assess the nutritional value, 30 species have undergone phytochemical analysis) phytochemical composition, and biological activity and Phelipanche genera of the Orobanchaceae of P. tournefortii. Chemical composition of family and 19 natural products have been individual parts of the parasite (flowers and stem sequestered from the host (Scharenberg and Zidorn, with a tuber, separately) and host species were 2018). The Polish team studied six species compared - T. polycephalum, in various localities, belonging to the genera Orobanche and at different altitudes. Additionally, it was unclear Phelipanche and reported that they are rich in PhGs whether the compounds identified were synthesised and their number is greater than in Herba by the holoparasite or obtained from their host Cistanches. This herb has a high and comparable plants. Therefore, we examined the effect of the host antioxidant potential. It is widely used in Chinese species on the chemical composition and bioactivity medicine as a part of nutraceutical and medicinal of P. tournefortii. We have also identified preparations (Jedrejek et al., 2020). Owing to their phytochemical components associated with the unique properties, certain holoparasitic species like antioxidant properties of the parasite and host and Cistanche are being considered for cultivation in the interactions between them. Our research on the specific regions of China (Xu et al., 2009). chemical composition and beneficial health Orobanche crenata is a possible novel functional properties of this species can be used to create an food. In southern Italy, it is used to prepare several innovative product. This species can be treated as a traditional meals (Renna et al., 2018). The genus functional food as well as a pharmacological and Phelypaea includes 3 holoparasitic species therapeutic agent. Piwowarczyk et al., Phytochemical and bioactive properties of Phelypaea tournefortii 114 – effect of parasitic lifestyle and environmental factors MATERIALS AND METHODS MPW-251 (MPW MED. INSTRUMENTS, Warsaw, Poland) at 19,000 × g for 10 min. Before Species studied and plant material analysis, the supernatant was purified using a The study was conducted between May and June hydrophilic PTFE membrane (Millex Samplicity 2017, in four localities of central (Kotayk province) Filter, Merck) of 0.20 µm pore size. All extractions and southern (Vayots Dzor province) Armenia were performed in triplicate (Oszmiański et al., (Western Asia),
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