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In Vitro Cultures J. Hattori Bot. Lab. No. 76: 283- 291 (Oct. 1994) SECONDARY METABOLITES FROM BRYOPHYTES IN VITRO CULTURES HANS BECKER1 ABSTRACT. In vitro cultures of bryophytes are useful for the production of plant material that otherwise has been available only in minor amounts from field collections. Species of hornworts and liverworts were cultivated, and plant material obtained had qualitatively and quantitatively the same compounds as field collected plants. During the last five years a number of new substances has been isolated from in vitro cultures of bryophytes. In liverworts, these new compounds included various sesqui-, di- and triterpenes, bibenzyl-, bisbibenzyl- and phenanthren derivatives. A new coloring agent of the cell wall was found in cultures of Ricciocarpos natans. The accumulation of the compound could be enhanced by variation of the culture methods. Cultures of mosses produced various ftavonoids and hornworts were rich in phenylpropanoids. In cultures of Anthoceros agrestis a new type of alkaloid was isolated. The paper gives a short review on secondary compounds from bryophyte in vitro cultures based on results from the authors labora-tory and from literature data. INTRODUCTION Bryophytes contain a large variety of secondary metabolites (Asakawa 1982, Zinsmeister et al. 1991). Since less than 5% of known species have been chemically investigated in detail, a large number of interesting substances must remain to be isolated. However, further advances are hindered by the difficulty in obtaining large amounts of pure plant material. Bryophytes typically grow in mixed populations and are strongly attached to the soil by rhizoids. This, in addition to their small size, makes purification a difficult and time-consuming procedure. One day's work with the aid of a binocular microscope may yield a few grams of plant material. For this reason, many of the previously isolated compounds were obtained in amounts that precluded their biological testing. To overcome shortage of plant material, one alternative is the cultivation of bryophytes in the form of aseptic in vitro cultures, as has been done for many years for higher plants. Isolation and maintenenace of callus and cell suspension cultures of bryophytes are described in detail by Katoh (1988). In the following a short review will be given about secondary metabolites obtained during the last five years from bryophytes in vitro cultures. 1 Pharmakognosie und Analytische Phytochemie, Universitat des Saarlandes, D 66041 Saarbrticken, Germany. Publication Nr. 78 of "Arbeitskreis Chemie und Biologie der Moose". 284 J. Hattori Bot. Lab. No. 76 I 9 9 4 RESULTS Phenolic compounds: In vitro cltures of various species of Sphagnum may contain more than 0, 1% of sphagnum acid (Compound l) calculated from dry weight. Part of the acid is excreted to the external medium. Cultures of Sphagnum magellanicum degrade sphagnum acid to ( - )2,5-dihydro-5-hydroxy-4-[ 4'-hydroxyphenyl]-furan-2-one (Compound 2) ab­ breviated as hydroxybutenolide (Wilschke et al. 1989). This hydroxybutenolide is mainly bound to the cell wall and is a naturally occuring component in Sphagnum . In contrast to sphagnum acid, hydroxybutenolide is not excreted into the surrounding medium. Bryophytes are rich in flavonoids (Mues and Zinsmeister 1988, Zinsmeister et al. 1991 ). In contrast to many reports of flavonoids isolated from collected material, little is known about the production of flavonoids from in vitro cultures. In vitro cultures of Reboulia hemisphaerica produced a different flavonoid in light and in dark (Morais and Becker 1990). From cultures cultivated under continuous light 67mg/100g dry weight of 5-hydroxy-7,4' -dimethoxyflavone (Compound 3 = apigenin-7,4' -dimethylether) were isolated. From the dark-grown fermenter cultures 60mg/100g of 5-hydroxy-7,8,4'­ trimethoxyflavone (Compound 4) were obtained. Compound 3 could not be detected in dark grown cultures and compound 4 was absent in light grown cultures. Cultures of the moss Hypnum cupressiforme produced hypnogenol A and B (Sievers 1992), two dimeric flavonoids that have been previously isolated and characterized from collected plant material (Sievers et al. 1992). Luteolin has been isolated from suspension cultures of Jungermannia infusca (Ono et al. 1992). Up to now red pigments had only been isolated from Bryum (Bendz and Martens­ son 1963) and Sphagnum (Mentlein and Vowinkel 1984). Recently Kunz et al. ( 1994) succeeded in isolating two anthocyanidins, riccionidin A (Compound 5) and riccion­ idin B from in vitro cultures of Ricciocarpos natans. The pigments are bound to the cell wall and are hardly soluble in water or organic solvents. Preliminary chromatographic screening revealed that they are also present in various other liverworts such as Marchantia polymorpha, Riccia duplex and Scapania undulata. The amount of the pigment could be enhanced reducing the original nitrate and phosphate concentration of the medium to 1/10 of the original. Homworts are rich in caffeic acid derivatives (Takeda et al. 1990). In vitro cultures of Anthoceros agrestis contained glutamic acid amides of various aromatic acids (Compound 6=p-cumaric acid-glutamic acid amide) and esters of 2-(3,4- dihydroxyphenyl)ethanol with cinnamic acid derivatives (Compound 7 = 2-(3,4- dihydroxyphenyl)ethenyl caffeic ester). The main phenolic compound was rosmarinic acid (Compound 8). A new type of alkaloid anthocerodiazonin (Compound 9) could also be isolated from the cultures (Trennheuser 1992). Lunularic acid (Compound 10), a bibenzyl derivative, has been found in every liverwort that has been screened for this compound (Gorham 1990). Ohta et al (1984) H . BECKER: Secondary metabolites from bryophytes 285 oc11, ;oX)=o CH 0 1100. 3 4 R ~ OCH3 HO HoXXJ:9-f/, . 'Ii:, OH O O OH I ~ HO '- 0 HO LO-OH HO:c! OH R R HO c({ .. OH OH 10: R ~ COOH ll :R~COOH 12: R ~ H 13: R ~ H HO OH h~ HO ~OH OH 14 15 had shown that the genuine precursor of lunularic acid is prelunularic acid (Compound 11). Lunularic acid might be decarboxylated to give lunularin (Compound 12) which is the mother compound of a large variety of bibenzyls and bisbibenzyls. The occurence of prelunularin (Compound 13) in axenic cultures of Ricciocarpos natans leads to the suggestion that lunularin is directly formed from prelunularin and not by decarboxyla­ tion of lunularic acid (Kunz and Becker 1994). In the cultures of the same plant bibenzylglycosides e.g. compound 14 have been found for the first time together with phenylethanoid glycosides, riccardin C, 2,5,4' -trihydroxybibenzyl and a dimeric bisbi­ benzyl (Compound 15 = 6',6"'-bis-riccardin C) (Kunz and Becker, 1992, 1994). 286 J. Hattori Bot. Lab. No. 76 I 9 9 4 OH OH H,co OCH3 OH 16 OH 18 19 OCH3 17 0 CQR Q5' cb )?X" HO i 20: R = CHO lA 21: R = COOH 25 0 24 26 22: R = CH3 23 ~CHO ~~ H ~ I r,R·····K" ~ ~ / 'O" >t( ~ 27 28 29 30 Cultures of Marchantia polymorpha produced a phenanthrene (Compound 16), various biphenanthrenes (e.g. compound 17) and an isocoumarin (Compound 18) along with the fiavonoid aglykons apigenin and luteolin (Adam and Becker, 1994). The same cultures also contained the bisbibenzyl-derivatives marchantin A, B, C, H and perrottetin E (Adam and Becker, 1993). The production of the main bisbibenzyl marchantin A (Compound 19) was induced by lack of nitrate and the addition of cupric sulfate to the medium. Terpenoids: Most liverworts contain oil-bodies. These lipophilic compartments accumulate various mono-, sesqui- and diterpenoids. The presence of blue coloured sesquiterpenoid azulenes can be recognized in the blue oil bodies of Calypogeia azurea (Huneck, 1963). Takeda and Katoh (1981 ) first reported azulenes from in vitro cultures of Calypogeia granulata. Later Nagashima et al. (1990) found azulenes in Calypogeia H . BECKER: Secondary metabolites from bryophytes 287 peruviana, C. tosana, Macro/ejeunea pallescens and Plagiochi/a micropteris. From in vitro cultures of Calypogeia azurea ten different azulenes have been isolated (Siegel et al. 1992). Independently Nakagawara et al. (1992) isolated 4-methylazulene-1-carbalde­ hyde (Compound 20) and 4-methylazulene-1-carboxylic acid (Compound 21) from cultures of the same plant. The authors of the latter paper present a possible scheme for the biosynthesis of sesquiterpenes and azulenes in this liverwort. The rate of production of 1,4-dimethylazulene (Compound 22) in cultured cells of Calypogeia granulata was more than double the control rate after treatment with the abiotic elicitor vanadate (Nakagawara et al. 1993). This increase was preceded by doubling the activity of 3- hydroxy-3-methylglutaryl CoA reductase, an enzyme involved in isoprenoid biosynthe­ sis. Furthermore, addition of hydrogen peroxide to the culture also enhanced the production of 1,4-dimethylazulene to the same extent as vanadate. It was proposed that treatment with the elicitor resulted in oxidative stress due to generation of active oxygen species, which might act as messengers to activate the biosynthetic pathway to the formation of 1,4-dimethylazulene on the one hand and to activation of a system for scavenging active oxygen species on the other. Jamesoniel/a autumna/is contains a large variety of ent-labdanes and furanoditer­ penes (Blechschmidt and Becker, 1992). The same diterpenes together with related diterpenes and lignans were found in cultures of this plant (Tazaki et al. 1994a). The structure of a highly oxygenated diterpene (Compound 23) from J. autumna/is has been elucidated recently by X-ray analysis (Tazaki et al. 1994b). Cultures of Symphyogyna brongniartii, initiated from spores and maintained on Gamborg B 5 medium with 0.3% sucrose, produced the same terpenoids as the plants growing in their natural habitat (Sperle et al. 1991). The main constituent was perrottetianal A (Compound 24) minor constituents were bicylcogermacrene, /3- barbatene, /3-selinene, /3-cubebene, spathulenol, and ( - )-geosmin (Compound 25). The latter compound was hitherto only known from microorganisms. In vitro cultured gametophytes and suspension cells of the liverwort, Heteroscyphus planus, were assayed for the accumulation of mono- and sesquiterpenes (Nabeta et al.
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