Changes in phenolic content of wild and greenhouse-grown Hypericum triquetrifolium during plant development
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- Albert Morgan
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1 Turkish Journl of Agriulture nd Forestry Reserh Artile Turk J Agri For () 7: 7- TÜBİTAK doi:.9/tr-- Chnges in phenoli ontent of wild nd greenhouse-grown Hyperium triquetrifolium during plnt development Cüneyt ÇIRAK, *, Jolit RADUŠIENĖ, Birute KARPAVICIENE, Nedet ÇAMAŞ, Mehmet Serht ODABAŞ Ondokuz Myıs University, Votionl High Shool of Bfr, 55 Smsun, Turkey Nture Reserh Centre, Institute of Botny, Vilnius LT-, Lithuni Reeived: 7.. Aepted:.. Pulished Online: 5.5. Printed: 5.. Astrt: Hyperium triquetrifolium is promising mediinl plnt from estern Europe nd the Mediterrnen re. The present study ws onduted to determine ontogeneti nd morphogeneti vrition of hlorogeni id, rutin, hyperoside, isoqueretin, queritrin, nd queretin ontent in this speies. The wild-growing nd greenhouse-grown plnts were hrvested t vegettive, florl udding, full, fresh, nd mture stges nd were disseted into stem, lef, nd reprodutive tissues, whih were dried seprtely nd susequently ssyed for iotive ompounds y high performne liquid hromtogrphy. Chemil ontents in whole plnts inresed during plnt phenology nd, generlly, higher umultion levels were oserved in wild plnts. Depending on the development stges, the reprodutive prts umulted the highest level of hyperoside nd queretin, ut the leves produed higher mount of hlorogeni id, rutin, isoqueretin, nd queritrin. Aording to the results, there is lose reltionship etween the hemil ontent in plnt prts nd development stges during the phenologil yle. The rw mteril of H. triquetrifolium should e hrvested during flower ontogenesis for mediinl purposes. Key words: Chemil vrition, high performne liquid hromtogrphy, Hyperium triquetrifolium, phenolis, plnt phenology. Introdution The genus Hyperium L. enompsses pproximtely speies ommodted in setions nd hs nerly worldwide distriution, sent only from tropil lowlnds, deserts, nd Arti regions (Roson 977). The genus is represented in Turkey y 9 speies, of whih re endemi (Bingol et l. ). The genus Hyperium hs een reeiving muh puliity reently euse it is soure of the most importnt iologilly tive onstituents, nmely the phlorogluinol derivtives hyperforin nd dhyperforin; the nphthodinthrones hyperiin nd pseudohyperiin; severl phenolis suh s the flvonoids hyperoside, rutin, queritrin, queretin, nd ipigenin; nd the phenylpropnes ffei id nd hlorogeni id, whih possess wide rry of iologil properties (Ksper et l. ). Among the hemils, phenoli ompounds re importnt for their ontriution to the olor, sensory ttriutes, nd nutritionl nd ntioxidnt properties of plnts. Flvonoids espeilly hve ttrted onsiderle interest s dietry onstituents, nd results from linil studies indited their possile role in preventing rdiovsulr diseses nd severl kinds of ner (Chu et l. ). Although hyperiins nd hyperforin hve * Correspondene: uneyt@omu.edu.tr een reported to minly ontriute to the phrmologil effets of Hyperium extrts, flvonoids hve lso mde n importnt ontriution to the ntidepressnt tivity (Gstpr nd Zeller 5). Hyperium triquetrifolium Turr, ntive to estern Europe nd the Mediterrnen re, is n hereous perennil plnt from the fmily Hyperiee fmily nd grows in open, dry, stony, sndy ground nd ultivted fields in Turkey. It hs trditionlly een used in the tretment of urns nd gstrointestinl disese in Turkish folk mediine (Bytop 999). Results from reent studies reporting the ntinoieptive (Apydın et l. 999), ntiinflmmtory (Ozturk et l. ), ntioxidnt (Conforti et l. ), ntiteril (Pistelli et l. 5), ntifungl (Frternle et l. ), nd ytotoxi (Conforti et l. 7) tivities of H. triquetrifolium signl the gret potentil of this speies s promising mediinl plnt. Inresed mrket demnd for Hyperium-derived produts hs led to mny investigtions on seondry metolite vritions in severl Hyperium speies. These previous investigtions were generlly rried out on Hyperium perfortum L. nd did not give homogeneous results. Furthermore, they were limited y only studying 7
2 ÇIRAK et l. / Turk J Agri For hyperiins (Sirvent et l. ; Çırk et l. ), hyperforins (Kirkosyn et l. ), or essentil oils (Rdusiene et l. 5; Çırk et l. ), nd plnt developmentl stges were ignored in most of them. To dte, little effort hs een dedited to the study of vrition of flvonoids suh s queritrin, isoqueritrin (Mrtonfi nd Repk 99), nd queretin (Tekel ová et l. ). In prtiulr, phenologil hnges in the ontent of voltile omponents nd severl phenolis in wild-growing H. triquetrifolium plnts were reported previously from Tunisi y Hosni et l. (). However, no study, to our knowledge, hs een done on the vrition of hemil ontents in greenhouse-grown H. triquetrifolium plnts. Thus, the present study ws onduted to determine the reltionships etween the ontent of min flvonoids, nmely hlorogeni id, rutin, hyperoside, queritrin, queretin, nd isoqueretin, in plnt mterils nd development stges in oth wild nd greenhouse-grown H. triquetrifolium. This study lso desries the ttempt to ompre hemil ontents of the sme speies from wild nd modified ulture onditions.. Mterils nd methods.. Plnt mterils The speies ws identified y Dr Hsn Korkmz, Deprtment of Biology, Fulty of Siene nd Arts, Ondokuz Myıs University, Smsun, Turkey. Vouher speimens were deposited in the herrium of the Ondokuz Myıs University Agriulturl Fulty (OMUZF #)... Experimentl proedures Wild H. triquetrifolium plnts t different stges of their development were olleted from the Er distrit of Tokt Provine, Turkey ( N, E; 7 m ove se level) etween April nd Otoer of. The mteril represented rndomly gthered plnts in 5 phenologil stges: vegettive, florl udding, full, fresh, nd mture. Newly emerged shoots with leves were onsidered to e plnts in the vegettive stge. Only shoots with florl uds were seleted s plnts of florl udding stge. At the full stge, only shoots with fully opened flowers were hrvested. For the fresh nd mture stges, the shoots tht hd green nd drk rown psules, respetively, were hrvested. For the greenhouse ultivtion experiment, seeds were germinted in flot system, ommonly used for seedling prodution of rod-lef toos Burley nd Flue-Cured Virgini, under -h light, -h drk yle. Newly emerged seedlings were trnsplnted into pots of m in dimeter filled with ommeril pet try sustrte; its hemil nd physil hrteristis re presented in Tle. The pots with seedlings were moved to greenhouse onditions of h light, h drkness, 5 C, 75% reltive humidity, nd µmol m s PAR nd were wtered dily until they rehed mturity, then wtered only times week. A totl of pots were prepred for eh of the 5 phenologil stges; thus, plnts from totl of 5 pots were evluted. The tops of / wild nd ultured plnts, in whih mny phytohemils tend to umulte, were hrvested etween nd hours. Ten individuls were kept s whole plnts; the remining were disseted into florl, lef, nd stem tissues, were dried t room temperture ( ± C), nd were then ssyed for hemil ontents y high-performne liquid hromtogrphy (HPLC)... Preprtion of plnt extrts Air-dried plnt mteril ws mehnilly ground with lortory mill to otin homogeneous drug powder. Smples of out.5 g (weighed with. g preision) were extrted in 5 ml of % methnol y ultrsonition t C for min in Sonorex Super model RK 5H ultrsoni th. The prepred extrts were filtered through memrne filter with pore size of. µm (Crl Roth GmH, Krlsruhe, Germny) nd kept in refrigertor t C for no longer thn h until nlysis... HPLC nlysis A Shimdzu Prominene LC-A (Shimdzu Europ GmH, Duisurg, Germny) hromtogrphi system equipped with LC - AD model pumps, n SIL - AC utoinjetor, CTO - AC thermostt, nd n SPD - MA detetor ws used for HPLC nlysis. Seprtion of ll the ompounds ws rried out using YMC Pk Tle. Min hemil nd physil properties nd verge mount of dded nutrients for pet tested. Chemil dt Averge mount of dded nutrients Physil properties PH rnge (H O): 5.5. Nitrogen (mg N I ): Fertilizer (g L ):.5 Phosphorus (mg P O 5 I ): Blk sphgnum pet: % Potssium (mg K O I ): 7 White sphgnum pet: 7% Mgnesium (mg Mg I ):
3 ÇIRAK et l. / Turk J Agri For Pro - C (YMC Europe GmH, Dinslken, Germny) olumn (5 mm mm i.d.; -µm prtile sizes) with -mm gurd preolumn. For the moile phse,.% queous trifluoroeti id (TFA) ws used s eluent A nd etonitrile ontining.% TFA s eluent B. The following inry grdient elution progrm ws used: min (B 5% 5%), min (B 5% %), min (B % %), min (B % %), 9 min (B % %), min (B % 5%), nd min (B 5% 5%). The moile phse ws delivered with flow rte of. ml min ; the volume of extrt injeted ws µl. Detetion ws performed t the 79 nm wve length rnge with onstnt olumn temperture of C. The eluted ompounds were identified y ompring their retention time nd UV wvelengths with those of referene stndrds. The mximl sorption in the UV spetr of ompounds ws otined s follows: hlorogeni id, 5 nm; rutin, hyperoside, nd isoqueretin, 5 nm; queritrin, 7 nm; nd queretin, nm. The quntities of ompounds were lulted from n externl stndrd lirtion urve estlished from onentrtions in the following rnges:. µg ml for hlorogeni id nd rutin,. µg ml for hyperoside nd isoqueretin, nd. μg ml for queritrin nd queretin. All lirtion urves showed good liner regression (r.999) within the test rnge. Eh smple ws nlyzed twie, nd the men vlue ws used for lultion. The onentrtion of ompounds ws expressed s mg g dry mss (DM). The HPLC hromtogrm of H. triquetrifolium methnoli extrts t 5 nm is shown in Figure. mau ( ) 5 nm, nm (.) A Rt (min) mau ( ).5 5 nm, nm (.) B Rt (min) Figure. Typil HPLC hromtogrms of wild () nd greenhouse-grown () Hyperium triquetrifolium flowers extrt deteted y UV t 5 nm wvelength. Peks identified: hlorogeni id (Rt 9. min), rutin (Rt 5.79 min), hyperoside (Rt. min), isoqueretin (Rt. min), 5 queritrin (Rt 7.5 min), nd queretin (Rt. min). 9
4 ÇIRAK et l. / Turk J Agri For.5. Chemils The referene sustnes hlorogeni id (purity: 9.%), rutin trihydrte (purity: 99.%), isoqueretin (purity: 99.%), nd queritrin (purity: 99.%) were purhsed from Krl Roth (Germny). Hyperoside (purity: 9.%) nd queretin (purity: 95.%) referene mterils were otined from ChromDex (USA). Aetonitrile nd methnol of HPLC grde were supplied y Krl Roth (Germny)... Dt nlysis Dt for hlorogeni id, rutin, hyperoside, isoqueretin, queritrin, nd queretin ontents of the plnt mteril inluding whole plnt, stem, lef, nd reprodutive prts were sujeted to ANOVA seprtely for wild nd ultured plnts. Signifint differenes mong men vlues were tested with the Dunn multiple rnge test (P <.) y using MSTAT-C sttistil softwre (Russell D Freed, Crop nd Soil Sienes Deprtment, Mihign Stte University, USA).. Results The differenes mong hlorogeni id, rutin, hyperoside, isoqueretin, queritrin, nd queretin ontents of the whole plnt t different development stges were found to e signifint (P <.). Chemil ontents in whole plnts inresed during plnt phenology nd, generlly, higher umultion levels were oserved in wild plnts thn in ultivted ones. The highest levels of hlorogeni id, hyperoside, nd queritrin were rehed t full (7., 5.7, nd 7.9 mg g DM, respetively), nd wild plnts hrvested t florl udding produed the highest mounts of rutin, queretin, nd isoqueretin (5.9,.9, nd.5 mg g DM, respetively) (Tle ). In greenhouse-grown plnts, similrly, the hemil ontent in whole plnts inresed during plnt phenology nd plnts hrvested t full produed the highest mounts of rutin, hyperoside, queritrin, queretin, nd isoqueretin (.5,.9,.9,.99, nd 5. mg g DM, respetively). However, s n exeption, hlorogeni id ontent in the whole plnt ws the highest t the florl udding stge (9.9 mg g DM) (Tle ). After the development of uds nd flowers, the ontent of those ompounds deresed with the dvning of fruit development, nd the lowest level of eh ompound ws deteted t the mture stge in oth wild nd greenhouse-grown plnts. Tle. Chlorogeni id, rutin, hyperoside, queritrin, queretin, nd isoqueretin ontent (mg g DM) in vritions of wild-growing Hyperium triquetrifolium whole plnt during its phenologil yle. Phenologil stge Chlorogeni id Rutin Hyperoside Queritrin Queretin Isoqueretin Vegettive.5.7. d Florl udding d. d. d Mture. e. e.7 e.9.9. e Vlues followed y different letters in eh olumn re signifintly different (P <.) ording to the Dunn multiple rnge test. Tle. Chlorogeni id, rutin, hyperoside, queritrin, queretin, nd isoqueretin ontent (mg g DM) in vritions of greenhousegrown Hyperium triquetrifolium whole plnt during its phenologil yle. Phenologil stge Chlorogeni id Rutin Hyperoside Queritrin Queretin Isoqueretin Vegettive. d Florl udding Mture. e..9 d.7.7. d Vlues followed y different letters in eh olumn re signifintly different (P <.) ording to the Dunn multiple rnge test.
5 ÇIRAK et l. / Turk J Agri For Signifint differenes were lso oserved mong stem, lef, nd reprodutive tissues with regrd to hemil umultion nd phenologil flutution of eh ompound (P <.). Depending on development stges, reprodutive prts umulted the highest level of hyperoside nd queretin; however, leves produed higher mounts of hlorogeni id, rutin, isoqueretin, nd queritrin. In wild plnts, hyperoside nd queretin ontents were the highest in fully opened flowers nd florl uds (.7 nd.59 mg g DM, respetively) (Figures nd ). Leves hrvested t the florl udding stge produed the highest ontents of rutin nd isoqueretin (. nd. mg g DM, respetively). Similrly, hlorogeni id nd queritrin ontents were the highest in lef tissues of plnts hrvested t full nd fresh stges (.5 nd 9. mg g DM, respetively) (Figures f). The sme hemil umultion mnner ws lso oserved mong different plnt prts in greenhouse-grown plnts. Hyperoside nd queretin were umulted minly in reprodutive prts, nd their highest level ws deteted in fully opened flowers nd fresh fruits (.55 nd.5 mg g DM, respetively) (Figures nd ). On the ontrry, leves were found to e superior over reprodutive prts in terms of rutin, isoqueretin, hlorogeni id, nd queritrin umultions (Figures f).. Disussion Seondry metolite onentrtions in given plnt speies nd/or tissues n vry signifintly during the ourse of ontogenesis, whih my e relevnt for the utiliztion of mediinl plnts. In the present study, the Hyperoside (mg g DM) Rutin (mg g DM) Chlorogeni id (mg g DM) Vegettive Vegettive Vegettive Florl udding Florl udding Florl udding () () (e) Mture Mture Mture Queretin (mg g DM) Isoqueretin (mg g DM) Queritrin (mg g DM) Vegettive Vegettive Vegettive Florl udding Florl udding Florl udding Stems Leves Reprodutive prts () (d) (f) Mture Mture Mture Figure. Phenologil hnges in hyperoside (), queretin (), rutin (), isoqueretin (d), hlorogeni id (e), nd queritrin (f) ontent of stem, lef, nd reprodutive tissues in wild-growing Hyperium triquetrifolium (vlues with different letters within olumns for eh development stge differ signifintly t the level of P <.).
6 ÇIRAK et l. / Turk J Agri For Hyperoside (mg g DM) Vegettive Florl udding Mture Queretin (mg g DM).5.5 Vegettive Florl udding Mture Rutin (mg g DM) Chlorogeni id (mg g DM) Vegettive Vegettive Florl udding Florl udding () () (e) Mture Mture Isoqueretin (mg g DM) Stems Leves Reprodutive prts Vegettive Vegettive Florl udding Florl udding () (d) Mture Mture Figure. Phenologil hnges in hyperoside (), queretin (), rutin (), isoqueretin (d), hlorogeni id (e), nd queritrin (f) ontent of stem, lef, nd reprodutive tissues in greenhouse-grown Hyperium triquetrifolium (vlues with different letters within olumns for eh development stge differ signifintly t the level of P <.). Queritrin (mg g DM) (f) highest levels of ll tested hemils in whole plnts were rehed t time in oth wild nd greenhousegrown H. triquetrifolium plnts. Similrly, the highest levels of rutin, hyperoside, queritrin (Hosni et l. ), hyperiin, nd pseudohyperiin (Ayn nd Çırk ) in wild H. triquetrifolium were identified t. These results lso lrgely orrespond to those otined for other Hyperium speies. Kzlusks nd Bgdonite () reported tht the highest umultion of hyperiin, s well s rutin, queretin, nd isoqueretin, ws oserved during the development of uds nd t time in Hyperium perfortum L., well-known nd glolly distriuted speies. Areu et l. () reported tht the highest onentrtion of rutin, queretin, nd severl phenolis ws found during in greenhouse-grown Hyperium rsiliense Choisy. Similrly, hlorogeni id, hyperoside, queritrin, queretin, nd hyperiin ontents in the whole plnt inresed during the ourse of ontogenesis, nd the highest levels were rehed during flower ontogenesis in Hyperium orignifolium Willd. (Çirk et l. 7), Hyperium perfolitum L. (Çırk et l. 7), nd Hyperium montretii Sph (Çırk et l. ). The differenes in hemil omposition etween leves nd flowers found in the present study did not mth those desried for H. perfortum, whose flowers umulted lrger mounts of hyperiin, hyperforin, rutin, queretin, nd queritrin nd whose leves hd the highest level of hyperoside (Büter nd Büter ; Kzlusks nd Bgdonite ; Bgdonite et l. ). In other speies of Hyperium, similrly, queritrin, rutin, hyperiin, pseudohyperiin, nd hyperforin were
7 ÇIRAK et l. / Turk J Agri For umulted minly in florl prts, while the leves produed higher mounts of queretin, hlorogeni id, nd hyperoside in H. orignifolium nd H. perfolitum (Çırk et l. 7, Çirk et l. 7). The differene is not surprising nd proly depends on geneti differenes of Hyperium speies. In the present study, it is interesting to note tht generlly higher umultion levels of the tested ompounds were oserved in wild plnts. Plnts in the wild re sujeted to mny ioti/ioti stress ftors nd hve evolved different defense systems to void the dmge used y these stress ftors (Estn-Crrso et l. ). The first step of defense is sed on the tivtion of preexisting omponents, resulting in overprodution of toxi ompounds. In this sense, most phenolis hve een onsidered to e involved in the hemil defense rsenl of plnts ginst ioti/ioti stress, i.e. herivores, plnt pthogens, nd soil slinity (Close nd MArthur ). In previous studies on severl Hyperium speies, the ontent of phenoli ompounds, nmely rutin, queretin, nd totl solule phenols, ws reported to inrese signifintly in response to wter nd temperture stress in H. rsiliense (Areu nd Mzzfer 5). H. perfortum plnts sujeted to rief drought stress showed n inrese of queretin, rutin (Gry et l. ), nd hyperforin (Zoyed et l. 7). Germ et l. () pointed out the defensive roles of flvonoids nd tnnins in plnt metolism y oserving the inresed lef onentrtions of flvonoids in H. perfortum plnts exposed to high level of UV-B rdition. The higher seondry metolite umultion in wild H. triquetrifolium plnts in the present study my e ttriuted to the ioti/ioti stress ftors, possily present in the experimentl olletion site. Bsed on ontogeneti nd morphogeneti hnges in the ontent of hlorogeni id, rutin, hyperoside, isoqueretin, queritrin, nd queretin in wild nd greenhouse-grown H. triquetrifolium, it n e onluded tht there is lose reltionship etween the hemil ontent of plnt prts nd developmentl stges during the phenologil yle of the plnts. For mediinl purposes, plnt mteril should e hrvested during flower ontogenesis, during whih the ontent of the tested iotive sustnes rehed their highest level. The present results lso indited tht this mediinl plnt n e ultivted esily in greenhouse onditions, ut ulturing the speies in pots resulted in derese in the hemil ontent, possily due to the ontrolled environment. Nevertheless, this derese n e omitted when onsidering the ft tht the min issue in mediinl plnt stndrdiztion is the huge vriility in seondry metolite profile of given plnt mteril. Further studies re urrently underwy on lrge-sle prodution of the mediinl plnt under field onditions. Aknowledgment This study ws supported y Ondokuz Myıs University (Projet No.: PYO.BMY.9..). Referenes Areu IN, Mzzfer P (5) Effet of wter nd temperture stress on the ontent of tive onstituents of Hyperium rsiliense Choisy. Plnt Physiol Biohem :. Areu IN, Porto ALM, Mrsioli AJ, Mzzfer P () Distriution of iotive sustnes from Hyperium rsiliense during plnt growth. Plnt Si 7: Apydın S, Zeyek U, Ine I, Elgin G, Krmenderes C, Ozturk B, Tuglulr I (999) Hyperium triquetrifolium Turr. extrt exhiits ntinoieptive tivity in the mouse. J Ethnophrmol : 7. Ayn AK, Çırk C () Vrition of hyperiins in Hyperium triquetrifolium Turr growing in different lotions of Turkey during plnt growth. Nt Prod Res : 597. Bgdonitė E, Mártonfi P, Repčák M, Loks J () Vrition in the ontents of pseudohyperiin nd hyperiin in Hyperium perfortum from Lithuni. Biohem Syst Eol :. Bytop T (999) Türkiye de Bitkilerle Tedvi. İstnul Universitesi Yyınlrı, No: 7, İstnul (in Turkish). Bingol U, Cosge B, Guruz B () Hyperium speies in flor of Turkey. In: Hyperium (Eds. MS Ods, C Çırk). Mediinl Aromti Plnt Si Bioteh 5 (Speil Issue ): 9. Büter KB, Büter B () Ontogeneti vrition regrding hyperiin nd hyperforin levels in four essions of Hyperium perfortum L. J Hers Spies Med Plnts 9: 95. Chu YH, Chng CL, Hsu HF () Flvonoid ontent of severl vegetles nd their ntioxidnt tivity. J Si Food Agri : 5 5. Close DC, MArthur C () Rethinking the role of mny plnt phenolis - protetion from photodmge not herivores? Oikos 99: 7. Conforti F, Loizzo MR, Sttti AG, Menihini F (7) Cytotoxi tivity of ntioxidnt onstituents from Hyperium triquetrifolium Turr. Nt Prod Res :. Conforti F, Sttti GA, Tundis R, Menihini F, Houghton P () Antioxidnt tivity of methnoli extrt of Hyperium triquetrifolium Turr eril prt. Fitoterpi : 79. Çırk C, Bertoli A, Pistelli L, Seyis F () Essentil oil omposition nd vriility of Hyperium perfortum from wild popultions of northern Turkey. Phrm Biol : 9 9. Çırk C, Rdusiene J, Arsln B () Vrition of iotive sustnes in Hyperium montretii during plnt growth. Nt Prod Res : 5.
8 ÇIRAK et l. / Turk J Agri For Çırk C, Rdušienė J, Jnulis V, Ivnusks L (7) Seondry metolites in Hyperium perfolitum: vrition mong plnt prts nd phenologil stges. Bot Helv 7: 9. Çirk C, Rdušienė J, Jnulis V, Ivnusks L (7) Vrition of iotive seondry metolites in Hyperium orignifolium during its phenologil yle. At Physiol Plnt 9: 97. Çirk C, Sğlm B, Ayn AK, Kevseroğlu K () Morphogeneti nd diurnl vrition of hyperiin in some Hyperium speies from Turkey during the ourse of ontogenesis. Biohem Syst Eol :. Estn-Crrso A, Lopez-Serrno M, Zpt JM, Ster B, Mrtin M () Oxidtion of phenoli ompounds from Aloe rdensis y peroxidse tivity: possile involvement in defene retions. Plnt Physiol Biohem 9: Frternle D, Bertoli A, Gimperi L, Buhini A, Rii D, Menihini F, Trinirelli E, Pistelli L () Antifungl evlution of Hyperium triquetrifolium polr extrts ginst Fusrium spp. Nt Prod Commun : 7. Gstpr M, Zeller K (5) Hyperium-extrkt STW und Sertrlin zur Behndlung der mittelshweren depression. Psyhophrmkotherpie : 5. Germ M, Stiilj V, Kreft S, Gersik A, Kreft I () Flvonoid, tnnin nd hyperiin onentrtions in the leves of St. John s wort (Hyperium perfortum L.) re ffeted y UV-B rdition levels. Food Chem : 7 7. Gry DE, Pllrdy SG, Grrett HE, Rottinghus GE () Effet of ute drought stress nd time of hrvest on phytohemistry nd dry weight of St. John s wort leves nd flowers. Plnt Med 9:. Hosni K, Msd K, Târit MB, Mrzouk B () Phenologil vritions of seondry metolites from Hyperium triquetrifolium Turr. Biohem Syst Eol 9: 5. Ksper S, Cri F, Forti B, Drgo F, Agugli E () Effiy nd tolerility of Hyperium extrt for the tretment of mild to moderte depression. Eur Neuropsyhophrm : Kzlusks S, Bgdonite E () Quntittive nlysis of tive sustnes in St. John s wort (Hyperium perfortum L.) y the high performne liquid hromtogrphy method. Mediin (Kuns) : Kirkosyn A, Gison D, Sirvent T () A omprtive survey of Hyperium perfortum plnts s soures of hyperiins nd hyperforin. J Hers Speies Med Plnts :. Mrtonfi P, Repk M (99) Seondry metolites during flower ontogenesis of Hyperium perfortum L. Zhrdnitvi : 7. Ozturk B, Apydin E, Goldeli E, Ine I, Zeyek U () Hyperium triquetrifolium Turr. extrt exhiits ntiinflmmtory tivity in the rt. J Ethnophrmol : 7 9. Pistelli L, Bertoli A, Morelli I, Menihini F, Musmnno RA, Di Mggio T, Cortz G (5) Chemil nd ntiteril evlution of Hyperium triquetrifolium Turr. Phytother Res 9: Rdusiene J, Judzentiene A, Bernotiene G (5) Essentil oil omposition nd vriility of Hyperium perfortum L. growing in Lithuni. Biohem Syst Eol :. Roson NKB (977) Studies in the genus Hyperium L. (Guttifere) I. Infrgeneri lssifition. Bull Br Mus Nt Hist (Bot) 5: Sirvent T, Wlker L, Vne N, Donn G () Vrition in hyperiins from wild popultions of Hyperium perfortum L. in the Pifi Northwest of the U.S.A. Eon Bot 5: 9. Tekel ová D, Repák M, Zemková E, Tóth J () Quntittive hnges of dinthrones, hyperforin nd flvonoids ontent in the flower ontogenesis of Hyperium perfortum. Plnt Med : Zoyed SMA, Afreen F, Kozi T (7) Phytohemil nd physiologil hnges in the leves of St. John s wort plnts under wter stress ondition. Environ Exp Bot 59: 9.
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