Nematicidal natural products from the aerial parts of Rubus niveus

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Nematicidal natural products from the aerial parts of Rubus niveus

Nighat Sultanaa; Musarrat Akhterb; Zakia Khatoonb a Pharmaceutical Research Center, PCSIR Laboratories Complex, Karachi, Pakistan b Food & Marine Resources Research Centre, PCSIR Laboratories Complex, Karachi, Pakistan Online publication date: 17 March 2010

To cite this Article Sultana, Nighat , Akhter, Musarrat and Khatoon, Zakia(2010) 'Nematicidal natural products from the

aerial parts of Rubus niveus', Natural Product Research, 24: 5, 407 — 415 To link to this Article: DOI: 10.1080/14786410802696429 URL: http://dx.doi.org/10.1080/14786410802696429

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Natural Product Research Vol. 24, No. 5, 20 March 2010, 407–415

Nematicidal natural products from the aerial parts of Rubus niveus Nighat Sultanaa*, Musarrat Akhterb and Zakia Khatoonb a

Pharmaceutical Research Center, PCSIR Laboratories Complex, Karachi, Pakistan; bFood & Marine Resources Research Centre, PCSIR Laboratories Complex, Karachi, Pakistan

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(Received 22 June 2008; final version received 18 December 2008) Studies on the aerial parts of Rubus niveus yielded six known compounds, 3,5-dihydroxy benzoic acid C7H6O4, (1), gallic acid C7H6O5 (2), ethyl galactoside (3), oleanolic acid (4), -sitosterol (5) and 3-O-[ -D-galactopyranosyl-(12)-D-glucopyranoside (6). Besides this, a gallic acid derivative with methyl substitution was synthesised as tetramethyl gallate (3). Together with this derivative, compounds 1, 2, the alcohol soluble, chloroform soluble and petroleum ether soluble extracts of the aerial parts of R. niveus were screened for its nematicidal activity against freshly hatched second stage juveniles of Meloidogyne incognita (root-knot nematode), exhibiting 100, 94, 100, 52, 45 and 14% mortality, respectively of M. incognita after 48 h at 0.5% concentration. Compounds 1, 2 and 3 were found to be more potent than the nematicide Azadirachta indica at the same concentration. Negative results were obtained for nematicidal activity of the petroleum ether extract of R. niveus leaf extract. This is the first report on the isolation of chemical constituents as well as the nematicidal activity of compounds and any part of R. niveus. Keywords: Rubus niveus; nematicidal activity; 3,5-dihydroxy benzoic acid; ethyl galactoside; tetramethyl gallate; gallic acid

1. Introduction Plant-parasitic nematodes constitute one of the most important pest groups affecting economic crops, especially in the developed and developing countries of the world. The use of plants and plant products is one of the promising methods for nematode control. They are cheap, easy to apply, produce no pollution hazards and have the capacity to structurally and nutritionally improve soil health. In view of these facts, investigations have been undertaken by various groups of scientists (Gommers, 1981; Nogueira, de Oliveira, & Ferraz, 1996; Qamar, Kapadia, Khan, & Badar, 1995), which have shown effective control of root-knot nematodes. In the present article, studies on the nematicidal activity of the alcoholic, chloroform, petroleum ether extract, and pure compounds isolated from the air-dried aerial parts of Rubus niveus are described. Rubus niveus is native from Indian to southeastern Asia, the Philippines and Indonesia (Gerrish, Stemmermann, & Gardner, 1992). Several known pharmacological activities are attributed to the genus. It is clear that Rubus fruit represents a valuable source of potentially healthy compounds and can represent an important component of a balanced diet. It *Corresponding author. Email: [email protected]

ISSN 1478–6419 print/ISSN 1029–2349 online ß 2010 Taylor & Francis DOI: 10.1080/14786410802696429 http://www.informaworld.com

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also enhances the bioavailability of the active ingredient of the pharmaceutical compound. A literature survey of the genus Rubus revealed the isolation of various natural products, including 1-caffeoylxylose (Du & Francis, 1973), cyanidin 3-glycosides (Du & Francis, 1973; Gla¨ßgen, Wray, Strack, Metzger, & Seitz, 1992; Hussein, Ayoub, & Nawwar, 2003; Ji, Saito, Yokoi, Shigihara, & Honda, 1992; Lowry, 1976; Shoyama et al., 1990; Strack, Wray, Metzger, & Grosse, 1992; Terahara, Saito, Toki, Sakata, & Honda, 1992), 9,10-dihydro1,2, 3,4, 6,7, 8-heptahydroxy-10-oxo-9-anthraceneacetic acid (Hussein, Ayoub, & Nawwar, 2003), 9,10-dihydro-1,2, 3,4, 6,7, 8-heptahydroxy-10-oxo-9-anthracene acetic acid (Flamini, Catalano, Caponi, Panizzi, & Morelli, 2002), di-p-coumaroyl putrescine (Ohtani et al., 1992), 13,16-dihydroxy-19-kauranoic acid (Ohtani et al., 1992), 9,13-dihydroxy-16-kauren19-oic acid, 13,17-dihydroxy-15-kauren-19-oic acid, 3,7-dihydroxy-12-oleanen-28-oic acid (Chatterjee, Basak, Barus, Mukherjee, & Roy, 1979), 2,19-dihydroxy-3-oxo-1,12-ursadien28-oic acid (Hattori et al., 1988), 3,15-dihydroxypregn-5-en-20-one, 9CI (Bhavnani & Stanczyk, 1972), 3,19-dihydroxy-12-ursene-24,28-dioic acid (Agarwal, Singh, Siddiqui, & Singh, 1995; Sarkar, Ganguly, 1978; Taketa et al., 2004; Wang, Shen, Yang, & Jia, 1997; Zhao et al., 1997), 3,7-dihydroxy-12-ursen-28-oic acid (Mukherjee, Ghatak, Ganguly, & Antoulas, 1984), ellagic acid, INN (Asami et al., 2003; Correˆa, Guerra, De Pa´dua, & Gottlieb, 1985; El-Toumy & Rauwald, 2003; Gijsen, Wijnberg, Stork, & de Groot, 1991; Ito et al., 2002; Kim et al., 2001; Lin, Yeh, Yang, Liu, & Hsu, 2001; Khac, Tran-Van, Campos, Lallemand, & Fetizon, 1990; Malhotra & Misra, 1981; Pakulski & Budzianowski, 1996; Rahman et al., 2001; Sata, 1987; Sinha, Taylor, Khan, McDaniel, & Esko, 1999; Tanaka, Jiang, & Kouno, 1998; Tanaka et al., 2001; Yang et al., 1998; Yoshida, Amakura, Liu, & Okuda, 1994), 10,11-epoxyguaiane (Gupta, Al-Shafi, Layden, & Hasiam, 1982; Nishiya, Kimura, Takeya, & Itokawa, 1992; Southwell, 1977), 5-eudesmen-11-ol, 2,3-dihydroxy-19oxo-18,19-seco-11,13 (18)-ursadien-28-oic acid (Okuda, Yoshida, Ashida, & Yazaki, 1983), 2,3 : 4,6-bis (hexahydroxydiphenoyl) glucose (Nonaka, ishimatsu, Ageta, & Nishioka, 1989; Ohtani et al., 1990; Okuda, Yoshida, Kuwahara, Memon, & Shingu, 1984; Sulyok, & Bencsik, 1985), coreanogenic acid, cyanidin 3,5-diglycosides (Birkinshaw & Bracken, 1942; Du & Francis, 1973; Gla¨ßgen et al., 1992; Ji et al., 1992; Lowry, 1976; Shoyama et al., 1990; Strack et al., 1992; Terahara et al., 1992; Yoshida, Konda, Kameda, & Goto, 1990), and 3, 6-dicaffeoylglucose. The Rubus species is a rich source of gallic acid and ellagic acid. Ellagic acid is a phenolic compound, which scientists have proven contributes to significant inhibition of colon, oesophageal, liver, lung, tongue and skin cancers. A literature survey reveals that gallic acid is an active ingredient from Rubus species, and is a highly potent compound which shows variety of biological activities. It also induced down-regulation of the survival Akt/mTOR pathway. Gallic acid is cyclooxygenase inhibitor, antiinflammatory, antioxidant, and a antiperoxidant. Gallic acid demonstrated a significant inhibition of cell proliferation in a series of cancer cell lines and induced apoptosis in oesophageal cancer cells (TE-2) but not in non-cancerous cells (CHEK-1). Observation of the molecular mechanism of apoptosis showed that gallic acid up-regulated the pro-apoptosis protein, bax, and induced caspase-cascade activity in cancer cells. On the other hand, gallic acid down-regulated anti-apoptosis proteins such as Bcl-2 and Xiap. These results suggest that gallic acid might be a potential anticancer compound. Keeping in view the pharmacological significance of the plant, phytochemical studies were undertaken on the constituents of the aerial parts of the plant in this laboratory two years earlier, which resulted in the isolation and characterisation of sugars and pentacyclic triterpenoids.

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2. Results and discussion Gallic acid (2) was isolated as a white crystalline compound from the ethyl acetate extract of R. niveus by column and thin-layer chromatography. A bioassay-guided isolation of the alcohol soluble extract of the air-dried aerial parts of R. niveus yielded two nematicidal aromatic compounds, 1 and 2, showing nematicidal activity at 0.5, 0.25, 0.125 and 0.05% concentrations, respectively (Tables 1–4). These compounds were identified as 3,5dihydroxy benzoic acid (1) and gallic acid (2) through spectral studies. Gallic acid (2) Table 1. Nematicidal activity of different fractions isolated from R. niveus on the larval mortality of M. incognita (root-knot nematode) after 24 h.

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Percent mortality/concentration after 24 h Fractions

0.5%

0.25%

0.125%

0.05%

0.00% (Control)

RN-AS RN-PS RN-CS A. indica

50 14 38 80

50 10 34 80

40 10 30 77

35 5 20 58

00.00% 00.00% 01.00% 02.00%

Notes: Values represent the mean of three experiments. RN-AS (R. niveous alcohol-soluble part); RN-PS (R. niveous petroleum ether-soluble part); RN-CS (R. niveous chloroform-soluble part).

Table 2. Nematicidal activity of different fractions of R. niveus on the larval mortality of M. incognita (root-knot nematode) after 48 h. Percent mortality/concentration Fractions

0.5%

0.25%

0.125%

0.05%

0.00% (Control)

RN-AS RN-PS RN-CS A. indica

52 14 45 88

44 12 38 85

40 13 30 80

37 08 28 50

0.00 0.00 1.00 3.00

Note: Values represent the mean of three experiments.

Table 3. Nematicidal activity of compounds (1, 2 and 3) on M. incognita larvae after 24 h. Percent mortality/concentration Compounds

0.5%

0.25%

0.125%

0.05%

0.00% (Control)

3,5-Dihydroxy benzoic acid (1) Gallic acid (2) Tetramethyl gallate (3) A. indica

96.00 92.00 95.00 80.00

97.00 74.00 96.00 80.00

96.00 66.00 92.00 77.00

94 60.00 88 50.0

0.00 2.00 1.00 2.00

Note: Values represent the mean of three experiments.

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Table 4. Nematicidal activity of compounds (1, 2 and 3) on M. incognita larvae after 48 h. Percent mortality/concentration after 48 h Compounds

0.5%

0.25%

0.125%

0.05%

0.00% (Control)

3,5-Dihydroxy benzoic acid (1) Gallic acid (2) Tetramethyl gallate (3) A. indica

100.00 94.00 100.00 88.00

100.00 90.00 100.00 85.00

100.00 70.00 94.00 80.00

98 60 90 50.0

0.00 2.00 1.00 3.00

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Note: Values represent the mean of three experiments.

(C7H6O5) was identified by comparison of its data with that reported previously, which was originally isolated from the leaves of Kalanchoe bloesfeldiana and from an Indonesian plant, Phaleria macrocarpa (Scheff.) Boerl.; this is the first report of its isolation from this species. 3,5-Dihydroxy benzoic acid (1) (C7H6O4) (resorcylic acid, 8CI, resorcinol-5carboxylic acid) was identified by comparison of its data with those reported earlier (Scott, 1970; Scott, 1972; Walpole et al., 1993), which was originally isolated from constituents of Arachis hypogaea (peanuts), Cicer arietinum (chickpea) seeds and in Pterocarpus santilinus and this is the first report of its isolation from this species. A gallic acid derivative with tetramethyl substititions was synthesised and evaluated for its nematicidal inhibitory activity against root-knot nematodes Meloidogyne incognita at different concentrations. This is the first report on the nematicidal activity of any part of R. niveus. Thus compounds 1, 2, 3 and R. niveus plant extracts might be beneficial as potent nematode inhibitors under specified conditions. The nematicidal activity of the crude alcoholic extract, its fractions (RN-AS, RN-PS and RN-CS) as well as pure compounds 1, 2 and the derivative of compound 2, tetramethyl gallate (3), were tested against a root-knot nematode (M. incognita). The direct antinemic action shown by RN-AS, and its fractions RN-CS and RN-PS in the in vitro investigation against second-stage juveniles of M. incognita is presented in Tables 1 and 2. The crude alcoholic extract of R. niveus (RN-AS) showed 50% mortality at 0.5% concentration after 24 h, while 52% mortality at 0.5% concentration after 48 h, whereas the petroleum ether soluble fraction (RN-PS) showed 14% mortality, and the chloroform soluble fraction (RN-CS) showed 45% mortality at the same concentration after 48 h. Conventional nematicide Azadirachta indica showed 88% mortality after 48 h. The alcoholic soluble (RN-AS), petroleum ether soluble (RN-PS) and chloroform soluble (RN-CS) fractions showed 50, 14 and 38% mortality, respectively of M. incognita larvae after 24 h.

HO

3 4

OH

2 1 5

HO

6

(1) OH

O

O

O

HO

3 4

2 5

OH

1

H3CO

6

(2) OH

H3CO

3 4

OCH3

2 1 5

6

OCH3

(3)

Two pure compounds (1 and 2) were isolated from the chloroform fractions and their nematicidal activity was tested on M. incognita larvae. The results of the in vitro valuation are shown in Tables 3 and 4. Compounds 1 and 3 showed the highest mortality (96 and 95%, respectively) at 0.5% concentration, while 2 showed 92% mortality at the same concentration after 24 h.

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Compounds 1 and 3 showed 100% mortality at 0.5% concentration after 48 h, while compound 2 showed 94% mortality at 0.5% concentration after 48 h. Conventional nematicide A. indica showed 88% mortality at the 0.5% concentration used in the present studies. It was noted that at all concentrations, all tested fractions and pure compounds exhibited significant larval mortality against the test nematode, but the activity decreased with a decrease in concentration in all cases (Tables 1–4).

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3. Experimental 3.1. General experimental procedures The mass spectra were recorded on a Jeol HX-110 instrument. The 1H and 13C NMR spectra were recorded in CDCl3 at 500, 400 and 125, 75 MHz, respectively, on a Bruker AM-500, 400 NMR spectrometer. The UV and IR spectra were recorded on Shimadzu UV-240 and Jasco A-320 spectrophotometers, respectively. Optical rotations were measured on a polatronic D polarimeter. The purity of the compounds was checked on TLC (Si gel, Merck PF254, 0.25 mm thickness). Melting points were determined in glass capillary tubes using a Buchi 535 and a Gallenkamp 30/MF-370 melting point apparatus.

3.2. Plant material The aerial parts of R. niveus (15 kg) were collected from Kashmir in December. A voucher specimen (KUH # 58106) was deposited in the Herbarium of the Department of Botany, University of Karachi.

3.3. Extraction and isolation Air-dried aerial parts of R. niveus (15 kg dry weight) were dried and extracted with EtOH (100 L). The EtOH extract was concentrated to a gum (712 g), dissolved in distilled water and extracted thoroughly with petroleum ether (40 L). The petroleum ether soluble portion was evaporated under reduced pressure to yield a gum (61.11 g) which was chromatographed on a silica gel column (Merck, 70–230 mesh, 2025.01 g). The elution of the column was initiated with petroleum ether. The combined column sub-fractions 1–8 (5.91 g) obtained by elution with 5 : 95 ethyl acetate–petroleum ether, which showed similar TLC behaviour upon spraying with ceric sulphate reagent, were combined and again subjected to CC using silica gel (type 60, 70–230 mesh, 200.10 g) and the column was eluted with petroleum ether–ethyl acetate (99 : 1). The sub-fractions 6–30 (1.86 g), which showed similar TLC behaviour, were combined and further purified on preparative TLC plates using a solvent system of petroleum ether–ethyl acetate (98 : 2) to afford pure compound 3 (19.5 mg, 9.5  105% yield). The fractions obtained on elution of the column with n-hexane–ethyl acetate (10 : 90) were checked on TLC. Fractions 7–18 that showed similar behaviour on TLC were combined and further purified by preparative TLC (Merck PF254, 0.2 mm) using CHCl3 as eluent to afford pure -sitosterol (5) (28 mg, 1.4  104% yield). Elution of the major column, which was loaded with 61.11 g of petroleum ether soluble material, was eluted with 30% ethyl acetate–petroleum ether, yielding an impure mixture (7.83 g). This mixture was again subjected to CC (silica gel, 70–230 mesh, 61.11 g). The fractions obtained with 20 : 80 ethyl acetate–petroleum ether yielded an impure

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compound 4, which was further purified by preparative TLC using a solvent system of petroleum ether–ethyl acetate (20 : 80) to obtain pure 4 (20 mg, 10  104% yield). The remaining aqueous layer was acidified with acetic acid to pH 3, then extracted with CHCl3. The remaining aqueous layer was basified with NH4OH to pH 12 and extracted with CHCl3 (35 L). The CHCl3 soluble portion was dried (74.96 g). The acidic chloroform soluble portion was dried as a crude mixture, which was chromatographed on a silica gel column (Merck, 70–230 mesh, 2015 g). Elution of this column with 95% CHCl3–MeOH (18 L) yielded an impure mixture (15 g, Fr. 20–26, 500 mL each) containing compounds 2 and 6. This mixture was chromatographed on a SiO2 gel column (2.5 cm  70 cm, Merck, 70–230 mesh, 322 g) and eluted with CHCl3 (100%), followed by 2 : 8 MeOH : CHCl3. Fractions 85–98 (500 mL each), 4.96 g obtained on elution with 2 : 8 MeOH : CHCl3 (3 L) were again subjected to CC over silica gel (70–230 mesh size, 100 g). The column (1.5 cm  50 cm) was initially eluted with CHCl3–MeOH (92 : 8, 9 L) to afford 20 fractions. These were combined and further purified by repeated TLC (Merck, PF 254,0.5 mm) using CHCl3 : MeOH (7 : 3) to afford 2 (18.13 mg, 7.0  105%) and 6 (19.13 mg, 7.2  105%). The remaining aqueous layer was extracted with methanol. The methanol-soluble portion was dried as a crude mixture, which was chromatographed on a silica gel column (Merck, 70–230 mesh, 30.28 g). Elution of this column with 95% CHCl3–MeOH (5 L) yielded an impure mixture (1.5 g, Fr. 3–25, 500 mL each) containing compound 1. This mixture was chromatographed on a SiO2 gel column (2 cm  70 cm, Merck, 70–230 mesh, 322 g) and eluted with CHCl3 (100%), followed by 3 : 7 MeOH : CHCl3 to afford 40 fractions. Fractions 6–11 afforded 1.

4. Nematicidal activity Experiments were performed under laboratory conditions, at 28  2 C. Fresh egg masses collected from stock culture maintained on tomato root tissues were kept in water for egg hatching. The larvae emerged after 48 h from the egg masses incubated at 30 C and were used as test species for larval mortality studies. The movements of the nematodes were checked by touching them with a needle. Stock solutions (30 mg mL1) of the fractions and pure compounds were prepared. To determine the nematicidal effect of the crude fractions and the pure compounds, 100 freshly-hatched second-stage juveniles were taken in 5 mL of tap water. A measured amount of stock solution was added to make dilutions of 0.5, 0.25, 0.125 and 0.05%. Standard nematicide A. indica was taken for comparison and tap water was taken as the control. After 48 h of exposure with R. niveus fractions and pure compounds, the larvae were counted for mortality and non-mortality under stereoscopic microscope. The death of the nematodes was confirmed by keeping them in tap water for 24 h. The percent mortality was worked out from an average of three replicates.

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