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Lithospermum Officinale</Emphasis> Biologia, Bratislava, 61/4: 463—467, 2006 Section Botany DOI: 10.2478/s11756-006-0077-x Lithospermum officinale callus produces shikalkin Kamahldin Haghbeen1*, Valiolah Mozaffarian2, Fatemeh Ghaffari1, Elahe Pourazeezi1, Mohammad Saraji3 & Morteza Daliri Joupari1 1The National Institute for Genetic Engineering and Biotechnology, Tehran, Iran 2Iran Research Institute of Forests and Range lands, Tehran 3Department of Chemistry, Isfahan University of Technology, Isfahan, Iran Abstract: To study biosynthetic abilities of Lithospermum officinale, callus formation from young leaves and stems of the plant was induced on Linsmaier-Skoog medium supplemented with 2,4-D (10−6 M) and kinetin (10−5 M). Maintaining the calli on this medium resulted in polyphenolic compounds production. Their transfer onto White medium containing IAA (10−7 M) and kinetin (10−5 M) resulted in the production of a red naphthoquinonic pigment named shikalkin. Shikalkin production from callus cultures was suppressed on the White medium containing NAA instead of IAA. This observation indicates that both shikalkin and polyphenolic acids biosynthetic pathways exist in the L. officinale callus cells and a regulatory system counterbalances the ratio of shikalkin to polyphenolic acids. Key words: biosynthetic potential, callus, Lithospermum officinale, polyphenolic acids, shikalkin Abbreviations: NAA – 1-naphthaleneacetic acid; 2,4-D – 2,4-dichlorophenoxyacetic acid; IAA – 3-indoleacetic acid; 4CCA – 4-coumaroyl CoA; GPP – geranylpyrophosphate; LS – Linsmaier-Skoog; MS – Murashige-Skoog; PHBA – p- hydroxybenzoic acid; PPA – polyphenolic acids; RA – rosmarinic acid; THF, tetrahydrofuran. Introduction ways share a common biosynthetic sequence, at least in the early steps. Hence, both routes can be triggered in Shikalkin refers to the mixture of shikonin and alkannin the L. erythrorhizon cell culture and a regulatory sys- (Khan et al., 1983, Fig. 1). These enantiomers are nat- tem balances the ratio of shikalkin to PPA (Gaisser urally produced in different ratios in the roots of some &Heide, 1996). Therefore, the presence or absence of plants of Boraginaceae family alongside with a num- one of these two classes of compounds does not essen- ber of their corresponding esters (Papageorgiou et tially relate to the genetic potential of the plant cells al., 1999). Shikalkin is famous to plant biotechnologists in Boraginaceae family. It could depend on the condi- since Fujita et al. (1981a,b) introduced its successful tions governing the regulatory points somewhere in the large scale production plan based on the root suspen- phenylpropanoid pathway. To evaluate this idea, it was sion cell culture of the Lithospermum erythrorhizon in decided to search this common biosynthetic course in 1981. Fruitful in vitro cell culture of the L. erythrorhi- another member of the Boraginaceae family. This pa- zon root provided the plant scientists with a suitable per qualitatively supports this proposal through reveal- model to study phenolic secondary metabolites path- ing the results of a study on the cell culture of Lithos- ways in detail. Results of such studies have disclosed permum officinale, whose root is normally rich in PPA that the L. erythrorhizon callus is also able to produce (Kelley et al., 1975). In contrast to L. erythrorhizon, polyphenolic acids (PPA) like rosmarinic acid (RA) restricted to East Asia, L. officinale is a wide-spread (Mizukami et al., 1992) and lithospermic acid (Ya- and readily cultivated plant (Kelley et al., 1975). mamoto et al., 2000) not observed in the root of this species naturally. Besides, it has been shown that the L. erythrorhizon yield of PPA production by the cell Material and methods culture can be enhanced, if the production of shikalkin derivatives is inhibited by light (Gaisser & Heide, Chemicals 1996). All chemicals used in this work were taken from the au- These results suggest that shikalkin and PPA path- thentic samples. Sephadex LH-20, naphthazarin and phy- * Corresponding author: P.O.Box:14155-6343 Tehran, Iran, e-mail: [email protected], phone No: +98(21)4580372 c 2006 Institute of Botany, Slovak Academy of Sciences 464 K. Haghbeen et al. HO OH OH CO2H PHB HO OH 4CCA CO2H OH Shikimic acid CO-SCOA CO2H COOH PHB-geranyl PPO transferase GPP OH OH Rosmarinic acid synthase OH 3 -(4-Hydroxyphenyl)lactic acid CO2H O OH COOH O HO 2-O-(4-Coumaroyl)-3-(4-hydroxyphenyl)lactic acid OH O RR' OH O COOH HO O OH OH O HO Rosmarinic acid (RA) Shikonin (R = OH, R' = H) Alkannin (R = H, R' = OH) Fig. 1. The biosynthetic pathways of shikalkin (shikonin and alkannin) and PPA like RA are two branches of phenylpropanoid route, which is separated from each other at 4CCA point. tohormones were purchased from SigmaTM Chemical and Induction of shikalkin production Biochemical Company. Calli of L. officinale on LS medium were transferred on White medium supplemented with IAA and kinetin. The Plant samples concentration of copper, as abiotic elicitor, in the applied L. officinale samples were collected from Bagh-shad in the −1 medium was raised to the level of 0.3 mg L mentioned for east of Tehran (Iran) at the end of June. Arnebia euchroma M9 medium (FUJITA et al., 1981) and the sugar content was samples were collected from Dena strict in the central Za- −1 reduced to 25 g L . All the experiments were carried out gross Mountain at 3200 to 3500 m altitudes. The plant speci- ◦ in the dark at 25 C. The most effective concentrations of mens were determined by the botanist of the scientific board −7 IAA and kinetin for pigment production were 10 Mand of the Iran Research Institute of Forests and Range Lands, −6 10 M, respectively. Dr V. Mozaffarian, and the head of the Tehran University Herbarium, Professor A. Ghahreman. UV-Vis studies on the constituents of the L. officinale and Seed germination and callus induction A. euchroma roots L. officinale seeds were collected, weighed and sterilized. Spectrophotometric measurements were carried out using Healthy seeds were differently germinated, however, with a Beckman model V-550, UV-Vis-NIR spectrophotometer. negative results. Therefore, the hard crusts of some seeds Roots of all samples were cleaned and dried at 37 ◦C for 48 h. were scratched and the seeds were put onto Murashige- The dried roots of A. euchroma were powdered. L. officinale Skoog (MS) hormone-free medium or MS medium supple- root is composed of two distinct parts. The outer part (skin) mented with 2,4-D (10−6 M) and kinetin (10−5 M). Both is dark brown colored and the inner part is cream colored. groups of seeds were germinated in the green-house at 25 ◦C, Both parts were dried separately, then, grinded to powder. 24h photo-period, under 10 000 lux light intensity in less On the basis of the solubility and stability tests (data than two weeks. Then the explants excised from roots, not shown), radical-free tetrahydrofuran (THF) was se- leaflets, and stems were transferred onto MS and Linsmaier- lected as the most suitable solvent for extracting secondary Skoog (LS) media and kept at 25 ◦C in the dark. The leaf metabolites of both dried calli and roots of these plants. The and stem explants produced calli on both MS and LS me- THF extract of A. euchroma was neatly divided into three dia supplemented with 2,4-D and kinetin. The most effective fractions with water, n-hexane and CHCl3. Water soluble concentrations of kinetin and 2,4-D for the L. officinale seed fraction was without red pigment. Both the skin and the germination and callus formation were 10−5 Mand10−6 M, core parts of the L. officinale root were also extracted by respectively. Sucrose (50 g L−1) was used as carbon source THF, then, partitioned by n-hexane and acetonitrile. in all the above mentioned experiments. The resulting calli Each of the collected fractions was chromatographed were sub-cultured every three weeks. on a Sephadex LH-20 column (2.5 cm diameter and 75 cm Lithospermum officinale callus produces shikalkin 465 height) using a mixture of water and methanol as the mo- bile phase. The ratio of H2O/MeOH was varying between 1/99 up to 25/75 to bring about neat separation of the con- stituents on the column. Each of the collected components was dried at room temperature in the dark. UV-Vis of each constituent in the corresponding solvent was recorded in a range of 200 to 700 nm. The stability of each component in basic and acidic media was also determined by UV-Vis spectra. Mass spectroscopy experiments Chemical ionization mass spectroscopy experiments were carried out by a Trio 1000 mass spectrometer (Fisons Instru- Fig. 2. The spectra of the THF extract from the inner part (core) ments, Manchester, England) using methane as the reagent of the L. officinale root; 1 – in acidic milieu and, 2 – in basic gas. The ion source temperature was 150 ◦C, Electron energy milieu. Spectra 3 and 4 in the inset section belong to the THF extract of the outer part (skin) of the L. officinale root in acidic at 58eV, and the scan rate was 2 scans/sec. The tempera- and basic milieu, respectively. ture of the solid probe was programmed as follow: Initially 30 ◦C for 2 min, then increased to 140 ◦C (100 ◦Cmin−1,1 min hold) and subsequently 340 ◦C (300 ◦Cmin−1, 2 min hold). The recorded spectra were analyzed by the software provided by the company, Masslab version 1.3. Results and discussion It is well known that shikalkin derivatives are natu- rally produced in the roots of some Boraginaceae plants like L. erythrorhizon, A.euchroma and Alkanna tincto- ria (Papageorgiouet al., 1999; Tanaka et al., 1986; Xu-Qing & De-Wei, 1999). However, L. officinale is known for its PPA content (Kelley et al., 1975; De- Eknamkul & Ellis, 1984).
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