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First published online February 3, 2006; 10.1104/pp.105.070334 Plant Physiology 140:1475-1483 (2006) © 2006 American Society of Plant Biologists
Cholic Acid, a Bile Acid Elicitor of Hypersensitive Cell Death, Pathogenesis-Related Protein Synthesis, and Phytoalexin Accumulation in RiceFood and Health R&D Laboratories, Meiji Seika Kaisha, Ltd., Sakado, Saitama 350–0289, Japan (J.K., H.K., T.K.); Microbiological Resources and Technology Laboratories, Meiji Seika Kaisha, Ltd., Odawara, Kanagawa 250–0852, Japan (S.G.); Agricultural and Veterinary Research Laboratories, Meiji Seika Kaisha, Ltd., Kohoku-ku, Yokohama 222–8567, Japan (K.U.); and Department of Bioresource Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080–8555, Japan (M.O.)
When plants interact with certain pathogens, they protect themselves by generating various defense responses. These defense responses are induced by molecules called elicitors. Since long ago, composts fermented by animal feces have been used as a fertilizer in plant cultivation, and recently, have been known to provide suppression of plant disease. Therefore, we hypothesized that the compounds from animal feces may function as elicitors of plant defense responses. As a result of examination of our hypothesis, an elicitor of rice defense responses was isolated from human feces, and its structure was identified as cholic acid (CA), a primary bile acid in animals. Treatment of rice (Oryza sativa) leaves with CA induced the accumulation of antimicrobial compounds (phytoalexins), hypersensitive cell death, pathogenesis-related (PR) protein synthesis, and increased resistance to subsequent infection by virulent pathogens. CA induced these defense responses more rapidly than did fungal cerebroside, a sphingolipid elicitor isolated from the rice pathogenic fungus Magnaporthe grisea. Furthermore, fungal cerebroside induced both types of rice phytoalexins, phytocassanes and momilactones, whereas CA mainly induced phytocassanes, but not momilactones. In the structure-activity relationship analysis, the hydroxyl groups at C-7 and C-12, and the carboxyl group at C-24 of CA contributed to the elicitor activity. These results indicate that CA is specifically recognized by rice and is a different type of elicitor from fungal cerebroside. This report demonstrated that bile acid induced defense responses in plants.
In animals, bile acids play important roles in the absorption of dietary lipids, regulation of cholesterol catabolism, and detoxification of secondary bile acids (Chiang, 2002  ). Cholic acid (CA) and chenodeoxycholic acid (CDCA) are known as representative primary bile acids, and deoxycholic acid (DCA) and lithocholic acid (LCA) metabolized from the primary bile acids by intestinal microorganisms as representative secondary bile acids. Among them, in animals, CDCA and LCA are known to act as ligands for nuclear receptors, such as farnesoid X receptor (FXR; Makishima et al., 1999; Parks et al., 1999; Wang et al., 1999), vitamin D receptor (VDR; Makishima et al., 2002), and pregnane X receptor (PXR; Staudinger et al., 2001). By contrast, to our knowledge, no reports have yet demonstrated the specific function for CA in plants and animals.
When plants interact with certain pathogens, they protect themselves by generating various defense responses, such as the accumulation of antimicrobial compounds (phytoalexins), the induction of pathogenesis-related (PR) proteins (chitinases,
Since long ago, composts fermented by animal feces have been used as a fertilizer in plant cultivation and, recently, have been known to provide suppression of plant disease (Haug, 1993
Purification and Structural Determination of an Elicitor from Human Feces When plants interact with pathogens, they produce antimicrobial compounds called phytoalexins as a defense response. To examine whether the compounds in animal feces function as elicitors of plant defense response, we tested the elicitor activity of an extract from human feces by measuring phytoalexin induction in rice bioassay systems. As a result, an ethyl acetate extract from an acidic water suspension of human feces effectively induced the accumulation of phytoalexins in rice leaves. The active material in the feces apparently had acidic and hydrophobic properties. On the basis of this observation, we purified elicitor from the ethyl acetate extract by monitoring the ability to induce phytoalexin production. After HPLC fractionation in three steps, one purified elicitor was isolated and designated compound 1 (Table I ). Compound 1 was purified about 255-fold and 10.9% of the initial activity was recovered. The specific activity of compound 1 was 1.07 units/µg.
The 1H-NMR spectrum of compound 1 (Fig. 1 ) was identical to that of authentic CA. In the negative electrospray ionization mass spectrometry spectrum of compound 1, the molecular ion [M-H]– at mass-to-charge ratio (m/z) 407.3 was identical to that of CA. Furthermore, elicitor activity of compound 1 was 1.07 ± 0.13 units/mg, which was the same activity with CA (1.11 ± 0.11 units/mg). From these results, the structure of compound 1 was identified as CA, a primary bile acid in animals. To the best of our knowledge, this report is the first to demonstrate that bile acids have elicitor activity in plants.
In our previous study, fungal cerebrosides have been isolated as sphingolipid elicitors from the membrane of the rice pathogenic fungus Magnaporthe grisea (Koga et al., 1998b ). Fungal cerebrosides induced the production of phytoalexins, PR proteins, cell death, active oxygen, and complete resistance to subsequent infection by virulent pathogens (Koga et al., 1998b; Umemura et al., 2000). Furthermore, the methyl group at C-9 in the sphingoid-base moiety, a structure unique to fungal sphingolipids, was specifically recognized by rice plants (Koga et al., 1998b). Therefore, to examine the differences between elicitors from pathogens and animal feces, we examined differences in the induction of phytoalexins by CA and fungal cerebroside. So far, five cassane-type diterpenes, phytocassanes A, B, C, D, and E (Koga et al., 1995; Koga et al., 1997; Fig. 2A
), eight pimarane-type diterpenes, momilactones A and B (Cartwright et al., 1977; Fig. 2A), oryzalexins A, B, C, D, E, and F (Akatsuka et al., 1985; Sekido et al., 1986; Kato et al., 1993; Kato et al., 1994), one stemarane-type diterpene, oryzalexin S (Tamogami et al., 1993), and one flavonoid, sakuranetin (Kodama et al., 1992), have been isolated as rice phytoalexins. Dose-response curves for the phytocassanes and momilactones induced by CA or fungal cerebroside are shown in Figure 2, B and C. Fungal cerebroside induced the production of significant amounts of phytocassanes and momilactones. On the other hand, CA induced the production of significant amounts of phytocassanes, but induced the production of negligible amounts of momilactones in rice leaves.
Induction of Various Defense Responses by Treatment with CA
Plant defense response to pathogen invasion (hypersensitive response) is accompanied by induction of a variety of chemical and physiological barriers as well as phytoalexins (Keen, 1992
 -1,3-Glucanase induced in the hypersensitive response is considered to degrade -1,3-glucan, a component of pathogenic fungal cell wall. Therefore, second, we measured the induction of -1,3-glucanase, a PR protein belonging to the PR-2 family (Cote et al., 1991). As shown in Figure 3B, significant amounts of -1,3-glucanase activity were induced 24 h or more after treatment with CA as compared with the control treatment. Finally, we examined whether treatment with CA could induce significant resistance to a virulent pathogen. The data presented in Figure 3C show that treatment of rice plants with CA 16 h or more before inoculation of the pathogen resulted in resistance to infection by a virulent race of M. grisea. However, treatment with CA 0 to 8 h before inoculation hardly enhanced resistance to infection. These results indicate that CA did not inhibit proliferation of the pathogen but, rather, it induced resistance against the pathogen. The three sets of results described above clearly show that CA induced hypersensitive response in rice plants.
Treatment of rice leaves with 20 µM or more of CA induced significant amounts of phytocassanes (Fig. 2B). Therefore, to examine whether such a low concentration of CA (20 µM) has physiological significance in rice defense responses, we measured minimal amounts of CA to induce resistance to a virulent pathogen. The data presented in Figure 4A show that treatment of rice leaves with 20 µM or more of CA before inoculation of the pathogen resulted in significant resistance to infection by a virulent race of M. grisea. Although high concentrations of CA (about 10 mM) are used as a surfactant for membrane solubilization, our results indicate that such a low concentration of CA (20 µM) acts as a specific elicitor in rice plants rather than as a nonspecific surfactant.
Since the composts fermented by animal feces should contact with plant roots, we examined whether treatment of rice roots with CA could induce significant resistance to a virulent pathogen. The data presented in Figure 4B show that the treatment of rice roots with 20 µM or more of CA before inoculation of the pathogen resulted in significant resistance to infection by a virulent race of M. grisea.
To examine the differences between elicitors from pathogens and animal feces, we tested the timing of induction of rice defense responses. First, significant amounts of phytocassanes were induced 24 h or more after treatment with CA, but they were not induced until 36 h or more after treatment with fungal cerebroside (Fig. 5A
). Thus, induction by CA was clearly more rapid relative to the induction by fungal cerebroside. Second, significant cell death was induced 24 h or more after treatment with CA, whereas fungal cerebroside did not induce cell death until 48 h or more after treatment (Fig. 5B). Thus, CA clearly induced cell death more rapidly than did fungal cerebroside. Finally, CA induced
Elicitor Activity of a Number of Bile Acids and Their Derivatives To examine the structure-activity relationship, we tested a number of bile acids and their derivatives for elicitor activity by measuring phytoalexin induction in rice leaves (Fig. 6B ). CA had higher elicitor activity than similar compounds that lack either the hydroxyl group at C-12 (CDCA) or at C-7 (DCA; Fig. 6A). Furthermore, LCA and hyodeoxycholic acid (HDCA), both of which lack the hydroxyl groups at C-12 and C-7 (Fig. 6A), had lower activity than CDCA and DCA, suggesting that the hydroxyl groups at C-12 and C-7 are important for the activity. Methylation of the carboxyl group at C-24 of CA (cholic acid methyl ester [methyl-CA]) led to a 7-fold decrease in activity, and conjugate bile acids, such as taurocholic acid (tauro-CA), glycocholic acid (glyco-CA), and tauroglycocholic acid (tauroglyco-CA) had lower activity than CA, suggesting that the carboxyl group at C-24 also contribute to the activity. Thus, the hydroxyl groups at C-7 and C-12, and the carboxyl group at C-24 of CA seem to be key elements determining the activity, and CA is specifically recognized by rice.
Comparisons of the elicitor activity of bile acid derivatives provide some important insights into the structural features required for elicitor activity in rice plants. The hydroxyl groups at C-7 and C-12, and the carboxyl group at C-24 of CA were key elements determining the elicitor activity. Such specificity for CA indicates that rice plants can specifically recognize CA in feces and thereby induce various defense responses. Furthermore, the low concentration of CA required for elicitor activity provides further evidence that CA is specifically recognized by rice. In animals, bile acids play important roles in the absorption of dietary lipids, regulation of cholesterol catabolism, and detoxification of secondary bile acids (Chiang, 2002 ). In particular, bile acids have attracted attention as natural ligands for nuclear receptors such as FXR (Makishima et al., 1999; Parks et al., 1999; Wang et al.,1999), VDR (Makishima et al., 2002), and PXR (Staudinger et al., 2001). When FXR receptor, an orphan nuclear receptor bound to CDCA, repressed transcription of the gene encoding cholesterol 7 -hydroxylase, the rate-limiting enzyme in bile acid synthesis, and activated the gene encoding intestinal bile acid-binding protein, a candidate bile acid transporter (Makishima et al., 1999; Parks et al., 1999; Wang et al.,1999). Activation of VDX or PXR by LCA induced the expression of CYP3A, a cytochrome P450 enzyme that detoxifies LCA in the liver and intestine (Staudinger et al., 2001; Makishima et al., 2002). CDCA and LCA have been extensively studied as natural ligands for nuclear receptors as mentioned above, whereas no reports have yet demonstrated the presence of any specific receptor for CA in animals. Hence, the molecular mechanisms in the absorption of dietary lipids and regulation of cholesterol catabolism by CA have not been fully elucidated yet. From this point of view, the isolation of rice receptor for CA in defense responses might assist bile acid studies in animals.
Until now, both types of phytoalexins, phytocassanes and momilactones, had always been induced together under various conditions (e.g. infection with pathogens such as M. grisea [Koga et al., 1995
In light of the two facts that bile acids regulate gene transcription by acting as natural ligands for nuclear receptors such as FXR, PXR, or VDR in animals and that CA might directly act downstream in the defense signaling pathway in rice, it seems possible that CA operates as a ligand for a nuclear receptor that regulates phytocassane and PR protein synthesis and cell death in a manner similar to that observed in animal systems. Recently, a gene encoding ent-cassa-12,15-diene synthase, an enzyme that specifically catalyzes phytocassane synthesis, has been cloned (Cho et al., 2004
Recently, because of environmental pollution by chemically synthesized fungicides, natural substances that induce plant disease resistance have attracted attention as alternatives (Koga, 2003
Analysis Procedures
1H-NMR spectrum was recorded in CDCl3 solutions on a Varian UNITY plus 500 spectrometer (500.2 MHz), using SiMe4 as an internal standard. Electrospray ionization mass spectrometry was recorded on a LCT mass spectrometer. Electron ionization mass spectra (EI-MS) were recorded on a Nippondenshi DX-303 mass spectrometer. Momilactones and phytocassanes were analyzed by reverse-phase HPLC using a TSKgel ODS-120T (4.6 mm i.d. x 30 cm; TOSOH) column at a flow rate of 1.2 mL/min at 50°C as described (Koga et al., 1995
Magnaporthe grisea (virulent race 007) was kindly provided by Dr. Michiaki Iwata (Meiji Seika Kaisha, Ltd.). Fungal cerebroside, (4E,8E)-N-D-2'-hydroxy-(E)-3'-hexadecenoyl-1-O-
Six rice (Oryza sativa) leaves treated with the elicitor solution were collected and cut into pieces. The sample was shaken with 5 mL of ethyl acetate and 5 mL of 0.1 N Na2CO3 (pH 10.5) for 16 h to yield ethyl acetate and aqueous layers. The ethyl acetate layer was evaporated to yield a crude extract, which was dissolved in 1.6 mL of ethanol before adding 2.4 mL of 0.02 N HCl. The solution was mixed and centrifuged at 15,000g for 30 min. The supernatant (0.2 mL) was subjected to HPLC on a TSKgel ODS-120T column (4.6 mm i.d. x 30 cm; TOSOH) eluted with 45% acetonitrile. The peaks of phytoalexins were monitored with an UV detector at 280 nm for phytocassanes and at 215 nm for momilactones as described. The structures of the compounds were confirmed by EI-MS as described (Koga et al., 1995
A bioassay for measuring elicitor activity was performed according to the modified method as described (Koga et al., 1998a
A total of 1,031 g of human fecal samples was suspended in 5 L of water and homogenized five times for 1 min at intervals of 20 min at 4°C. The homogenized sample was centrifuged 18,000g for 30 min at 4°C and the supernatant was adjusted to pH 3 with HCl and extracted with ethyl acetate. The ethyl acetate extract was evaporated, then fractionated by HPLC on a TSKgel ODS-120T column (7.8 mm i.d. x 30 cm; TOSOH) that was eluted with a linear gradient of 20% to 100% ethanol containing 0.3% acetate. This chromatography was repeated and fractionated. A resultant fraction with the highest elicitor activity was then fractionated by HPLC on an ODS-120T column (4.6 mm i.d. x 30 cm; TOSOH) that was eluted with a mixture of ethanol, acetate, and water (45:0.3:54.7, v/v). This chromatography was also repeated and fractionated. A resultant fraction with the highest elicitor activity was then fractionated by HPLC on an ODS-120T column (4.6 mm i.d. x 30 cm; TOSOH) that was eluted with a mixture of acetonitrile, acetate, and water (40:0.2:59.8, v/v) yielded one purified elicitor.
Cell death was assayed by measuring ion leakage from leaf discs as described (Mittler et al., 1996
Rice plants (Oryza sativa L. cv Akitakomachi) were cultivated in a phytotron as described earlier. When the fifth leaf was half expanded, 40 rice leaves were sprayed with 4 mM potassium phosphate, pH 6, plus 0.01% Tween 20 (control) or with the same solution plus 20 µM of CA at different times (0–60 h) before inoculation with M. grisea as described earlier. Plants were then grown at 24°C during the day and 18°C at night with cycles of 12 h of high intense light (25,000 lux) and 12 h of darkness daily. Humidity was set at 80%. For each measurement, the leaves 0 to 60 h after treatment were sprayed with a spore suspension of a virulent race (007) of M. grisea that was prepared as described (Matsumoto et al., 1980
We thank Prof. Hisakazu Yamane (University of Tokyo) for helpful advice and critical suggestions. This article is dedicated to the memory of Mr. Tarozaemon Kera (Konokan High School), who passed away in October 2001. Received August 25, 2005; returned for revision November 22, 2005; accepted January 5, 2006.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jinichiro Koga (jinichiro_koga{at}meiji.co.jp). Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.070334. * Corresponding author; e-mail jinichiro_koga{at}meiji.co.jp; fax 81–492–84–7598.
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