Interactive Effects of Wide-Spectrum Monochromatic Lights On
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molecules Article Interactive Effects of Wide-Spectrum Monochromatic Lights on Phytochemical Production, Antioxidant and Biological Activities of Solanum xanthocarpum Callus Cultures Hazrat Usman 1, Muhammad Asad Ullah 1 , Hasnain Jan 1, Aisha Siddiquah 1, Samantha Drouet 2,3, Sumaira Anjum 4 , Nathalie Giglioli-Guviarc’h 5, Christophe Hano 2,3,* and Bilal Haider Abbasi 1,* 1 Department of Biotechnology, Quaid-i-Azam University, Islamabad 45320, Pakistan; [email protected] (H.U.); [email protected] (M.A.U.); [email protected] (H.J.); [email protected] (A.S.) 2 Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), INRA USC1328 Unversité d’, CEDEX 2, 45067 Orléans, France; [email protected] 3 COSMACTIFS, Bioactifs et Cosmétiques, CNRS GDR3711, CEDEX 2, 4506 Orléans, France 4 Department of Biotechnology, Kinnaird College for Women, Lahore 54000, Pakistan; [email protected] 5 EA2106 Biomolecules et Biotechnologies Vegetales, Universite de Tours, 37000 Tours, France; [email protected] * Correspondence: [email protected] (B.H.A.); [email protected] (C.H.); Tel.: +92-51-90644121 or +92-300-5125822 (B.H.A.); +33-2-37-30-97-53 (C.H.); Fax: +92-51-90644121 (B.H.A.) Academic Editors: Hosam O. Elansary and Vincenzo De Feo Received: 28 January 2020; Accepted: 31 March 2020; Published: 8 May 2020 Abstract: Solanum xanthocarpum is considered an important traditional medicinal herb because of its unique antioxidant, and anti-diabetic, anti-aging, and anti-inflammatory potential. Because of the over exploitation linked to its medicinal properties as well as destruction of its natural habitat, S. xanthocarpum is now becoming endangered and its supply is limited. Plant in vitro culture and elicitation are attractive alternative strategies to produce biomass and stimulate biosynthesis of medicinally important phytochemicals. Here, we investigated the potential influence of seven different monochromatic light treatments on biomass and secondary metabolites accumulation in callus culture of S. xanthocarpum as well as associated biological activities of the corresponding extracts. Among different light treatments, highest biomass accumulation was observed in white light-treated callus culture. Optimum accumulation of total flavonoid contents (TFC) and total phenolic contents (TPC) were observed in callus culture kept under continuous white and blue light respectively than control. Quantification of phytochemicals through HPLC revealed that optimum production of caffeic acid (0.57 0.06 mg/g DW), methyl-caffeate (17.19 mg/g 1.79 DW), scopoletin ± ± (2.28 0.13 mg/g DW), and esculetin (0.68 0.07 mg/g DW) was observed under blue light callus ± ± cultures. Compared to the classic photoperiod condition, caffeic acid, methyl-caffeate, scopoletin, and esculetin were accumulated 1.7, 2.5, 1.1, and 1.09-folds higher, respectively. Moreover, high in vitro cell free antioxidant, anti-diabetic, anti-aging, and anti-inflammatory activities were closely associated with the production of these secondary metabolites. These results clearly showed the interest to apply multispectral light as elicitor of in vitro callus cultures S. xanthocarpum to promote the production of important phytochemicals, and allow us to propose this system as an alternative for the collection of this endangered species from the wild. Keywords: Solanum xanthocarpum; elicitation; multispectral lights; caffeic acid; coumarins; anti-diabetic; anti-inflammatory Molecules 2020, 25, 2201; doi:10.3390/molecules25092201 www.mdpi.com/journal/molecules Molecules 2020, 25, x FOR PEER REVIEW 2 of 25 Molecules 2020, 25, 2201 2 of 25 1. Introduction 1. Introduction Medicinal plants are used by mankind as a source of primary health care for thousands of years, in an Medicinalattempt to plants cure diseases are used because by mankind of their as wide a source pharmaceutical of primary health and therapeutic care for thousands applications of years, [1]. Medicinalin an attempt plants to cure are diseasesused widely because in both of their developed wide pharmaceutical and developing and countries. therapeutic According applications to the [1]. WHOMedicinal report plants on aretraditional used widely medicine in both strategy developed 2014 and–2023, developing 70% population countries. Accordingof the world to the rely WHO on traditionalreport on traditional medicines, medicine mostly of strategy plant origin 2014–2023,, whereas 70% 80% population population of of the developing world rely countries on traditional uses medicinalmedicines, plants mostly for of treatment plant origin, of diseases whereas [1] 80%. With population a paradigm of developing shift in the countries20th century uses to medicinalward the useplants of synthetic for treatment chemicals, of diseases reputed [1 to]. be With more a paradigmeffective and shift safer in to the combat 20th century diseases, toward the interest the use in medicinalof synthetic plants chemicals, has temporarily reputed tofailed be more and some effective studies and reported safer to combatthat the diseases,use of medicinal the interest plants in wasmedicinal reduced plants by one has- temporarilyfourth during failed thatand period some [2,3] studies. However, reported numerous that the usestudies of medicinal show that plants the excessivewas reduced use of by synthetic one-fourth drugs during could that have period side [effects2,3]. However, and considerably numerous increase studies the show incidence that theof someexcessive diseases use of[3] synthetic. With the drugs development could have of side modern effects approaches and considerably, such as increase biotechnological the incidence plant of sourcing,some diseases analyt [ical3]. Withtools for the compounds development identification of modern,approaches, and isolation such or molecular as biotechnological investigation plant of biologicalsourcing, analyticalactivity mechanism tools for compoundss, herbal medicine identification, is back in and the isolation spotlights or molecular[4]. Solanum investigation xanthocarpum of Schrad.biological and activity Wendl mechanisms,(Solanaceae; aka herbal Solanum medicine virginianum is back L. in or the Solanum spotlights mairei [4 ].H.Solanum Lév.) is a xanthocarpum wild annual herb.Schrad. The and plant Wendl is also (Solanaceae known under; aka Solanum the vernacular virginianum namesL. of or KantakariSolanum maireior Bhatkatiya.H. Lév.) isIts a fruits, wild annualedible yellowherb. Theberries plant surrounded is also known by enlarged under thecalyx, vernacular are largely names used as of traditional Kantakari medicine or Bhatkatiya. to cure Its various fruits, ailments.edible yellow Several berries biological surrounded activities by enlarged relevant calyx, with are their largely traditional used as traditionaluses have medicinebeen reported to cure, includingvarious ailments. antioxidant Several [5–7] biological, anti-diabetic activities [8,9] relevant, anti-inflammatory with their traditional [10,11], as uses well have as effects been reported, on skin appearanceincluding antioxidant [12]. Phytochemical [5–7], anti-diabetic profiling of [8 S.,9 ],xanthocarpum anti-inflammatory extracts [ 10revealed,11], as the well presence as effects of ondiverse skin classesappearance of bioactive [12]. Phytochemical secondary metabolite profilings ofincludingS. xanthocarpum alkaloidextracts glycoside revealeds [13,14] the, saponin presences [15,16] of diverse, but alsoclasses of ofhigh bioactive levels secondaryof coumarins metabolites [17], in particular including alkaloidof scopoletin glycosides and esculetin [13,14], saponins (Figure [1).15 ,From16], but a biosyntheticalso of high levelspoint of coumarinsview, these [ 17coumarins], in particular derived of scopoletinfrom the phenylpropanoid and esculetin (Figure pathway,1). From more a preciselybiosynthetic from point trans of- view,cinnamic these acid, coumarins rather derivedvia umbelliferone from the phenylpropanoid than through lactonization pathway, more reaction precisely of thefrom caffeictrans -cinnamicacid derivative, acid, rather2’-hydroxy via umbelliferone-caffeic acid lead than to through esculetin lactonization formation [18] reaction. Scopoletin of the is ca ffalsoeic producedacid derivative, from 2’-hydroxy-catrans-cinnamicffeic acid acid but lead via to esculetincaffeic acid formation ester [18derivatives]. Scopoletin (Figure is also 1) produced [18,19]. Alternatively,from trans-cinnamic caffeic acidacid but is stored via caff ineic its acid methylated ester derivatives form, i.e. (Figure, methyl1)[-caffeate18,19]. Alternatively,, in S. xanthocarpum caffeic (Figureacid isstored 1) [20] in. its methylated form, i.e., methyl-caffeate, in S. xanthocarpum (Figure1)[20]. O OH NH2 L-Phenylanine FLAVONOIDS PAL O O O HO HO OH OH OCH3 HO HO trans-cinnamic acid caffeic acid methyl-caffeate HO HO H3C O HO O O HO O O HO O O umbelliferone esculetin scopoletin Figure 1. SchematicSchematic view view of of the the phenylpropanoid phenylpropanoid pathway pathway leading leading to to the the production production of of flavonoids, flavonoids, phenolics (in (in particular, particular, caffeic caffeic acid acid and and methyl methyl-ca-caffeateffeate)) and and coumarins coumarins (in particular, (in particular, esculetin esculetin and and scopoletin). PAL: l-phenylalanine ammonia-lyse. Adapted from Bourgaud et al. [18] and Karamat et al. [19]. Molecules 2020, 25, 2201 3 of 25 Because of the over exploitation linked to its medicinal properties as