Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets
© Ren and Dai; licensee BioMed Central Ltd. 2012
Received: 27 June 2012
Accepted: 25 July 2012
Published: 2 August 2012
Jasmonic acid (JA) is a well-characterized signaling molecule in plant defense responses. However, its relationships with other signal molecules in secondary metabolite production induced by endophytic fungus are largely unknown. Atractylodes lancea (Asteraceae) is a traditional Chinese medicinal plant that produces antimicrobial volatiles oils. We incubated plantlets of A. lancea with the fungus Gilmaniella sp. AL12. to research how JA interacted with other signal molecules in volatile oil production.
Fungal inoculation increased JA generation and volatile oil accumulation. To investigate whether JA is required for volatile oil production, plantlets were treated with JA inhibitors ibuprofen (IBU) and nordihydroguaiaretic acid. The inhibitors suppressed both JA and volatile oil production, but fungal inoculation could still induce volatile oils. Plantlets were further treated with the nitric oxide (NO)-specific scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (cPTIO), the H2O2 inhibitors diphenylene iodonium (DPI) and catalase (CAT), and the salicylic acid (SA) biosynthesis inhibitors paclobutrazol and 2-aminoindan-2-phosphonic acid. With fungal inoculation, IBU did not inhibit NO production, and JA generation was significantly suppressed by cPTIO, showing that JA may act as a downstream signal of the NO pathway. Exogenous H2O2 could reverse the inhibitory effects of cPTIO on JA generation, indicating that NO mediates JA induction by the fungus through H2O2-dependent pathways. With fungal inoculation, the H2O2 scavenger DPI/CAT could inhibit JA generation, but IBU could not inhibit H2O2 production, implying that H2O2 directly mediated JA generation. Finally, JA generation was enhanced when SA production was suppressed, and vice versa.
Jasmonic acid acts as a downstream signaling molecule in NO- and H2O2-mediated volatile oil accumulation induced by endophytic fungus and has a complementary interaction with the SA signaling pathway.
KeywordsAtractylodes lancea Endophytic fungi Volatile oil Jasmonic acid Medicinal herb
Atractylodes lancea, a member of the Compositae family, is a traditional Chinese medicinal plant [1, 2]. Volatile oils from A. lancea show antimicrobial activities as well. These oils comprise active secondary metabolites, including the characteristic components atractylone, β-eudesmol, hinesol, and atractylodin . Secondary metabolites, such as terpenes, flavonoids, and alkaloids, are believed to be involved in plant responses to many biotic and abiotic stresses [4–6]. Another plant defense response is the activation of multiple signaling events [7, 8]. For example, jasmonic acid (JA) biosynthesis by plants is induced by pathogen infection and elicitor treatment , and salicylic acid (SA) is involved in activating distinct sets of defense-related genes , such as those that encode pathogenesis-related (PR) proteins . Also, many signaling molecules have been revealed to be involved in secondary metabolism [12–14].
Endophytes can coexist with their hosts and have great potential to affect the hosts’ metabolism ; their effects on plant accumulation of medicinal components have received much attention recently [16, 17]. Unlike pathogens, endophytic fungi do not cause strong hypersensitive reactions in the host. But long-term colonization can induce various kinds of metabolites to accrue in hosts [17, 18]. How endophytic fungus-host interactions affect the accumulation of plant secondary metabolites is an intriguing issue.
Jasmonic acid is a well-characterized plant signaling molecule that mediates plant defense responses  by responding to microbial infection and elicitor treatment . Kunkel et al.. found that fungal elicitor caused rapid increases in JA production, secondary metabolite biosynthetic gene expression, and secondary metabolite accumulation in many plants. Exogenous JA application enhanced gene expression of secondary metabolite biosynthetic pathways, while the fungal elicitor-induced secondary metabolite accumulation could be abolished by JA synthesis inhibitors . Most plant defense responses are regulated by many signal molecules, and “cross-talk” among multiple signaling pathways is important in plant cell signal transduction networks . An increasing number of studies have shown that these signals do not function entirely independently; rather, they are influenced the magnitude or amplitude of various other signals .
Although interactions between SA- and JA-mediated signaling pathways have been reported to enhance the expression of plant defense-related genes, studies on interactions between JA and multiple signaling pathways (nitric oxide, hydrogen peroxide, and SA) in mediating plant secondary metabolite accumulation are rare. In this work, we report that JA acts as a downstream signal of nitric oxide (NO)- and hydrogen peroxide (H2O2)-mediated volatile oil accumulation in A. lancea plantlets induced by endophytic fungus Gilmaniella sp. AL12. Furthermore, we reveal an unusual complementary relationship between JA and SA in mediating the biosynthesis of medicinal plant secondary metabolites.
Plant materials and treatments
Meristem cultures of Atractylodes lancea (collected in Maoshan, Jiangsu Province, China) were established according to Wang et al. . The explants were surface sterilized and grown in MS medium  supplemented with 0.3 mg/L naphthaleneacetic acid (NAA), 2.0 mg/L 6-benzyladenine, 30 g/L sucrose, and 10% agar in 150 mL Erlenmeyer flasks. Rooting medium (1/2 MS) contained 0.25 mg/L NAA, 30 g/L sucrose, and 10% agar. All media were adjusted to a pH of 6.0 before being autoclaved. Cultures were maintained in a growth chamber (25/18°C day/night, with a light intensity of 3400 lm/m2 and a photoperiod of 12 h) and subcultured every four weeks. Thirty-day-old rooting plantlets were used for all treatments.
Reagents used as specific scavengers or inhibitors, including ibuprofen (IBU), nordihydroguaiaretic acid (NDGA), 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline −1-oxyl-3-oxide potassium salt (cPTIO), paclobutrazol (PAC), catalase (CAT), diphenylene iodonium (DPI), and 2-aminoindan-2-phosphonic acid (AIP), were purchased from Sigma-Aldrich (St. Louis, MO, USA). All exogenous signaling molecules and inhibitors were filtered using 0.22 μm diameter microporous membranes before use. Unless stated otherwise, inhibitors were applied 1 d before the application of signaling molecules or fungal inoculation.
Fungal culture and treatments
The endophytic fungus AL12 (Gilmaniella sp.) was isolated from A. lancea, cultured on potato dextrose agar, and incubated at 28°C for five days . Thirty-day-old plantlets were inoculated using 5-mm AL12 mycelial disks. An equal size of potato dextrose agar was used as a control. All treatments were conducted in a sterile environment and replicated at least three times to examine reproducibility.
Measurement of H2O2 and NO
Thirty-day-old plants were incubated with fungal mycelia disks with or without inhibitors and were harvested 18 d later for determination of NO or H2O2. Inhibitors were 1.25 mmol L-1 cPTIO, 5.25 mKat L-1 CAT or 3 mmol L-1 DPI.
The generation of H2O2 by A. lancea plantlets was measured by chemiluminescence in a ferricyanide-catalyzed oxidation of luminol according to Schwacke and Hager , with modification. Leaf samples (1 g) were ground with 5 ml double distilled water. The homogenate was centrifuged at 13,000 g for 10 min, then 100 μL supernatant, 50 μL luminol (5-amino-2,3-dihydro-l,4-phthalazinedione), and 800 μL phosphate-buffered saline were mixed in a cuvette. The reaction was initiated with 100 μL K3[Fe(CN)6. To compare independent experiments, we used H2O2 as an internal standard. Fifty microliters of H2O2 (1 μM, freshly prepared) was added to the assay mixture containing 750 μL potassium phosphate buffer. One unit of H2O2 was defined as the chemiluminescence caused by the internal standard of 1 μM H2O2 per gram fresh weight.
The generation of NO was monitored using a NO detection kit (Nanjing Jiancheng Bio-engineering Inst., Nanjing, China) according to the manufacturer’s instructions. Leaf samples (1 g) were ground with 5 ml of 40 mM 4-(2-hydroxyethyl)-1-piperazineethanesulfonic acid (pH 7.2) and the homogenate was centrifuged at 14,000 g for 10 min. The supernatant was used for the NO assays. One unit of NO was defined as the absorbance variation caused by the internal standard of 1 μM NO per gram fresh weight.
At least 15 plantlets were assayed for each time point, and all treatments were performed in triplicate.
Measurement of SA
Thirty-day-old plants were incubated with fungal mycelia disks with or without inhibitors and were harvested 18 d later for determination of SA. Inhibitors were 1 mmol L-1 PAC or 2.5 mmol L-1 AIP.
Salicylic acid was extracted followed the method of Verberne et al. , with some modifications. Five grams of whole plantlets was ground in liquid nitrogen and extracted in 2 ml methanol by sonication. After centrifugation at 14,000 g for 5 min, the supernatant was rotary evaporated, and the residue was resuspended in 250 μl of 5% trichloroacetic acid. The mixture was re-extracted with 800 μl acetic acid ester: cyclohexane (1:1 v/v). Finally, the organic phase was rotary evaporated until dry, dissolved with 600 μl HPLC mobile phase (methanol: 2% acetic acid: H2O, 50:40:10, v: v: v), and filtered with a 0.22-μm microporous membrane for determination.
The SA samples were quantified by HPLC using a reverse-phase column (Hedera Packing Material Lichrospher 5-C18, 4.6 × 250 mm, 5 μm, Bonna-Agela Technologies, Wilmington, DE, USA). The mobile phases flow rate was 1 ml min−1. Salicylic acid was detected at 217 nm at 25°C .
Extraction and determination of volatile oils and JA
Thirty-day-old plantlets of Atractylodes lancea were incubated with 5-mm mycelial disks or PDA disks (control). Inhibitors (0.1 mmol L-1 IBU or NDGA) were added 1 d before fungal inoculation for JA determination.
Volatile oils were extracted from whole plantlets of A. lancea, including leaves and rhizomes (0.8–1.6% oil content in leaves, 2.2–3.4% in rhizomes), according to Zhang et al. . The volatile oils were dried with anhydrous sodium sulfate and stored in dark glass bottles at 4°C for gas chromatograph (GC) analysis.
Following Juergen et al. , JA was extracted by grinding plant material (1 g) frozen in liquid nitrogen and extracting with H2O: acetone (30:70, v:v). Samples were store in dark glass bottles at −21°C for GC analysis.
GC determination was carried out using an 1890 series GC (Hewlett-Packard, Palo Alto, CA) equipped with a flame ionization detector. A DB-5 ms (30 m × 0.25 mm × 0.25 μm) column (Agilent, Santa Clara, CA, USA) was used with the following temperature program: column held at 60°C for 1 min after injection, increased by 10°C/min to 190°C, held for 2 min, increased by 5°C/min to 210°C, held for 2 min, increased by 10°C/min to 220°C, and held for 8 min. Nitrogen was used as carrier and the flow rate was 4 ml/min. Four main components of the volatile oils, atractylone, hinesol, β-eudesmol, and atractylodin, were quantitatively analyzed according to the method of Fang et al. ; their retention times were 14.57, 15.24, 16.21, and 22.18 min, respectively.
Real-time quantitative RT-PCR analysis
Total RNA was extracted from leaves as described by Dong and Beer . First-strand cDNA was synthesized from 1 μg of total RNA (PrimeScript RT Reagent Kit, Takara, Dalian, China). Real-time qPCR was performed using the DNA Engine Opticon 2 Real-time PCR Detection System (Bio-Rad, Hercules, CA, USA) and SYBR green probe (SYBR Premix Ex Taq system, Takara). The constitutively-expressed gene EF1α used as an internal positive control. The gene-specific primers used to amplify EF1α were 5′-CAGGCTGATTGTGCTGTTCTTA-3′ and 5′-TGTGGCATCCATCTTGT-3′ (241 bp product) and for alHMGR were 5′-GGTGAGAAAGGTCCTGAAA-3′ and 5′-CATGGTAACGGAGATATGAA-3′ (154 bp). The GenBank accession numbers of the alHMGR and EF1α genes are EF090602.1 and X97131, respectively.
The thermocycler program was as follows: 90 s at 95°C; 40 cycles of 30 s at 95°C, 30 s at 57°C, and 30 s at 72°C; and 5 min at 72°C. To standardize the data, the ratio of the absolute transcript level of the alHMGR genes to the absolute transcript level of EF1α was calculated for each sample of each treatment.
Data were compiled using Microsoft Excel (Redmond, WA, USA). The values were represented as mean ± SD of three replicates for each treatment. Student’s t-test, one-way ANOVA, and Duncan’s multiple range test were used to identify significant differences (SPSS ver. 13.0, SPSS Inc., Chicago, IL, USA).
Dependence of JA in fungus-induced volatile oil accumulation
Accumulation of volatile oils by Atractylodes lancea over time
4.63 ± 1.41a
4.23 ± 0.74a
5.24 ± 0.94a
4.41 ± 0.67a
4.97 ± 0.56a
8.64 ± 1.19b
13.48 ± 1.54c
23.53 ± 2.76d
28.43 ± 1.54d
15.13 ± 0.93c
4.63 ± 1.27a
4.92 ± 1.02a
3.97 ± 0.42a
5.2 ± 0.55a
3.15 ± 0.75a
3.92 ± 0.48a
4.31 ± 0.39
4.71 ± 0.44a
5.17 ± 0.63a
5.6 ± 0.52a
38.17 ± 4.32a
40.12 ± 3.82a
41.6 ± 4.93a
40.85 ± 5.63a
54.42 ± 4.23b
65.15 ± 5.28c
78.72 ± 6.63d
104.42 ± 8.23e
128 ± 9.42f
52.15 ± 4.45b
38.17 ± 5.36a
32.31 ± 3.52a
38.63 ± 3.78a
35.62 ± 3.29a
43.81 ± 4.22a
46.95 ± 3.04a
37.13 ± 6.27a
46.21 ± 3.23a
46.9 ± 3.32a
50.22 ± 5.24a
80.72 ± 11.37a
85.6 ± 6.01a
92.23 ± 6.43a
96.63 ± 6.48b
104.75 ± 6.12c
104.75 ± 6.06c
116.58 ± 6.19d
119.62 ± 6.25e
123.83 ± 8.07e
99.65 ± 4.18c
80.72 ± 10.75a
78.7 ± 8.32a
81.27 ± 8.53a
88.51 ± 7.95a
93.18 ± 8.28a
94.67 ± 8.05a
98.38 ± 5.04a
96.42 ± 8.15a
85.1 ± 8.18a
94.77 ± 7.84a
98.32 ± 14.53a
109.24 ± 11.31a
111.23 ± 12.95a
118.97 ± 12.74a
125.53 ± 17.85a
131.52 ± 12.34a
137.64 ± 15.31b
152.34 ± 12.92b
171.63 ± 12.04b
183.4 ± 12.39c
98.32 ± 12.75a
110.7 ± 10.61a
114.2 ± 7.76a
115.42 ± 8.23a
121.9 ± 10.28a
111.47 ± 12.71a
116.8 ± 10.07a
118.5 ± 10.63a
121.1 ± 10.75a
134.1 ± 10.68a
221.84 ± 31.63a
239.19 ± 21.88a
250.3 ± 25.25a
260.86 ± 25.52b
289.67 ± 28.76c
310.06 ± 24.87d
346.42 ± 29.67e
399.91 ± 30.15f
451.89 ± 31.07 g
350.33 ± 21.95e
221.84 ± 30.13a
226.63 ± 23.47a
238.07 ± 20.49a
244.75 ± 19.77a
262.04 ± 23.53a
257.01 ± 24.28a
256.62 ± 21.77a
265.84 ± 22.45a
258.27 ± 22.85a
284.69 ± 24.28a
JA acts as a downstream signal of NO and H2O2 pathway
Paclobutrazol is an effective SA biosynthesis-related benzoic acid hydroxylase (BA2H) inhibitor  that also inhibits gibberellin biosynthesis . Therefore, we also used AIP, a specific SA biosynthesis-related phenylalanine ammonialyase (PAL) inhibitor [33, 34], to confirm that SA generation was suppressed. Interestingly, PAC and AIP could abolish the suppression of JA by DPI/CAT with fungus inoculation (Figure 2B). This result implied that the SA and JA signaling pathways were closely linked in endophyte-induced volatile-oil accumulation in A. lancea plantlets.
Complementary interactions between JA and SA in fungus-induced volatile-oil accumulation
Dependence of fungus-induced sesquiterpenoid production on JA production
Secondary metabolite accumulation is a common plant response to biotic or abiotic environmental stress, and secondary messengers are widely employed to mediate the accumulation of plant secondary metabolites. This work demonstrated that the fungus Gilmaniella sp. can induce JA production and promote the accumulation of volatile oils in host plantlets. As an important signal molecule, JA plays key roles in regulating the induction of volatile oils by the endophytic fungus. The specific inhibitors IBU and NDGA could block the JA signaling pathway and reduce the accumulation of related metabolites. Our previous study showed that NO, H2O2, and SA acted as signal molecules to mediate the accumulation of volatile oils in suspension cells of A. lancea caused by endophytic fungal elicitor . Thus, the possible relationships between JA and other known signaling pathways in the accumulation of secondary metabolites were further investigated.
Cross-talk between different signal transduction pathways, as opposed to single signaling pathways, mediates gene expression and the production of secondary metabolites during plant defense responses [37, 38]. Hydrogen peroxide has been reported to be a possible upstream signal for NO production in mung bean plantlets . Nitric oxide also can mediated fungal elicitor-induced taxol biosynthesis in Taxus chinensis suspension cells through reactive oxygen signaling pathways, stimulate SA accumulation in tobacco cell cultures, and induce PAL expression via an SA independent pathway [31, 40, 41]. Moreover, our previous work demonstrated that NO mediates volatile oil accumulation induced by the fungus through SA- and H2O2-dependent pathways. Hydrogen peroxide can enhance SA production but does not act as upstream signal molecule . The present work showed that endophytic fungus-induced JA was directly mediated by H2O2 and acted as a downstream signal molecule for both H2O2 and NO pathways.
In our study, JA had an unusual complementary interaction with the SA signaling pathway. Jasmonic acid is commonly postulated to act antagonistically on the SA signaling pathway and on the expression of SA-dependent genes [42, 43]. Other studies have shown that SA is a potent suppressor of JA signaling pathways and JA-dependent defense gene expression in various pharmacological and genetic experiments [44, 45]. In addition, both JA and SA are important signaling molecules in plant defense responses, such as the activation of distinct sets of defense-related genes and the development of systemic acquired resistance [21, 46]. Our results showed that when JA biosynthesis was suppressed by the inhibitor IBU, accumulation of SA was enhanced to compensate for the loss of JA-mediating function in fungus-triggered volatile-oil production. Similarly, JA production/signaling could substitute for the SA pathway when SA accumulation was impaired.
The value of medicinal herbs relies mainly on the accumulation of active pharmaceutical ingredients; low yield is the main challenge to producing high-quality herbs. In this work, we demonstrated that JA acts as a downstream signaling molecule in NO- and H2O2-mediated volatile oil accumulation induced by endophytic fungus and has a complementary interaction with the SA signaling pathway and clarified that HMGR gene expression was significantly stimulated by JA along with increasing sesquiterpenoid components. This information will help to better understand the relationships between fungal endophytes and their host plants. Furthermore, it also suggests strategies to improve the quality of medicinal herbs.
The authors are grateful to the National Natural Science Foundation of China (grant nos. 31070443 and 30500066) and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions for financial support.
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