Plant Physiol. (1999) 119: 1289-1296

Involvement of the Octadecanoid Pathway and Protein Phosphorylation in Fungal Elicitor-Induced Expression of Terpenoid Indole Alkaloid Biosynthetic Genes in Catharanthus roseus

Frank L.H. Menke, Stefanie Parchmann, Martin J. Mueller, Jan W. Kijne, and Johan Memelink^*

Institute of Molecular Plant Sciences, Clusius Laboratory, Leiden University, Wassenaarseweg 64, 2333 AL Leiden, The Netherlands (F.L.H.M., J.W.K., J.M.); and Institute of Pharmaceutical Biology, Munich University, Karlstrasse 29, D-80333 Munich, Germany (S.P., M.J.M.)

	ABSTRACT

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Two key genes in terpenoid indole alkaloid biosynthesis, Tdc and Str, encoding tryptophan decarboxylase and strictosidine synthase, respectively, are coordinately induced by fungal elicitors in suspension-cultured Catharanthus roseus cells. We have studied the roles of the jasmonate biosynthetic pathway and of protein phosphorylation in signal transduction initiated by a partially purified elicitor from yeast extract. In addition to activating Tdc and Str gene expression, the elicitor also induced the biosynthesis of jasmonic acid. The jasmonate precursor -linolenic acid or methyl jasmonate (MeJA) itself induced Tdc and Str gene expression when added exogenously . Diethyldithiocarbamic acid, an inhibitor of jasmonate biosynthesis, blocked both the elicitor-induced formation of jasmonic acid and the activation of terpenoid indole alkaloid biosynthetic genes. The protein kinase inhibitor K-252a abolished both elicitor-induced jasmonate biosynthesis and MeJA-induced Tdc and Str gene expression. Analysis of the expression of Str promoter/gusA fusions in transgenic C. roseus cells showed that the elicitor and MeJA act at the transcriptional level. These results demonstrate that the jasmonate biosynthetic pathway is an integral part of the elicitor-triggered signal transduction pathway that results in the coordinate expression of the Tdc and Str genes and that protein kinases act both upstream and downstream of jasmonates.

	INTRODUCTION

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The initiation of a plant defense response requires the perception of pathogen-derived (exogenous) or plant-derived (endogenous) signal molecules, collectively referred to as elicitors (for review, see Boller, 1995; Yang et al., 1997). Elicitor-induced defense responses include the biosynthesis of secondary metabolites (Darvill and Albersheim, 1984; Côté and Hahn, 1994) and proteinase inhibitors (Pearce et al., 1991). Protein phosphorylation is an essential component of elicitor-induced signal transduction (Chandra and Low, 1995; Suzuki et al., 1995). The lipid-based octadecanoid pathway leading to JA has also been implicated as an integral part of the signal transduction pathway leading to the activation of defense responses. The octadecanoid pathway was first implicated in wounding-induced biosynthesis of proteinase inhibitors (Farmer and Ryan, 1992). Upon wounding, the octadecanoid pathway is activated by the polypeptide systemin and by oligouronides, resulting in elevated levels of JA (Doares et al., 1995b). JA and its octadecanoid precursors activate the synthesis of wounding-inducible proteinase inhibitors (Farmer and Ryan, 1992). Induction of the synthesis of proteinase inhibitors by wounding, systemin, and oligouronides is blocked by several inhibitors of the jasmonate biosynthetic pathway (Farmer et al., 1994; Doares et al., 1995b). Furthermore, Kim et al. (1992) identified a MeJA-responsive element in the promoter of a proteinase inhibitor II gene, indicating that this gene is transcriptionally regulated in response to MeJA.

How elicitors affect JA biosynthesis and how the JA signal is transduced to effect gene expression is largely unknown. Much more is known about the JA biosynthetic pathway itself. Farmer and Ryan (1992) have proposed that a lipase generates -linolenic acid, the first precursor in the octadecanoid pathway. -Linolenic acid is then converted by a lipoxygenase, an allene oxide synthase, and an allene oxide cyclase into the intermediate 12-oxo-phytodienoic acid. This compound is converted into JA through the action of a reductase and three rounds of -oxidation (Vick and Zimmerman, 1984; Mueller, 1997).

JA and its octadecanoid precursors have also been implicated as intermediate signals in elicitor-induced secondary metabolite accumulation (Gundlach et al., 1992; Mueller et al., 1993; Ellard-Ivey and Douglas, 1996; Nojiri et al., 1996). A correlation between elicitor-induced accumulation of endogenous JA and secondary metabolite accumulation was shown in cells of California poppy (Mueller et al., 1993) and rice (Nojiri et al., 1996). In parsley cells phenylpropanoid biosynthetic genes were induced by octadecanoids, and elicitor-induced gene expression was blocked by a lipoxygenase inhibitor (Ellard-Ivey and Douglas, 1996). These reports indicate that in elicitor-induced secondary metabolism JA plays a role that is similar to its role in the accumulation of wound-induced proteinase inhibitors, for which it has been elegantly demonstrated that jasmonates are intermediate signals that transcriptionally activate proteinase inhibitor genes. However, the studies that have been done on various metabolic pathways in different plant species using diverse elicitors lack the integrated approach of measuring jasmonate biosynthesis and studying the effect of JA and octadecanoid pathway inhibitors on gene expression. In general, metabolite accumulation has been studied instead of gene expression. Therefore, in most cases it remains unclear on what regulatory level jasmonates exert their effect on secondary metabolism.

In Catharanthus roseus cell suspensions, the expression of two TIA biosynthetic genes, Tdc and Str, encoding Trp decarboxylase and strictosidine synthase, respectively, is coordinately induced by fungal elicitors such as YE (Pasquali et al., 1992). The enzymes encoded by these genes are important in the TIA biosynthetic pathway (for reviews, see Meijer et al., 1993; Kutchan, 1995). Both genes are present as single copies in the haploid C. roseus genome (Pasquali et al., 1992; Goddijn et al., 1994).

Using the integrated approach of measuring JA biosynthesis and using an inhibitor of the octadecanoid pathway, we show conclusively that elicitor-induced expression of the Tdc and Str genes in C. roseus cells is mediated by the octadecanoid pathway. Furthermore, we provide evidence for the existence of protein phosphorylation steps both upstream and downstream of the octadecanoid pathway. We also show that both elicitor-induced and MeJA-induced gene expression are conferred by the Str promoter, demonstrating that elicitor and MeJA act at the transcriptional level.

	MATERIALS AND METHODS

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Cell Culture

Elicitor and Jasmonate Treatment

1

1

Inhibitor Treatment

RNA Extraction and Northern Analysis

JA Extraction and Quantification

	RESULTS

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Tdc and Str gene expression in suspension-cultured C. roseus cells is coordinately induced by the addition of fungal elicitors (Pasquali et al., 1992). The crude elicitor preparations used by Pasquali et al. (1992) are less suitable for signal transduction studies because they may consist of multiple components that exert different effects on C. roseus cells. Therefore, the purification and characterization of a YE elicitor were undertaken (F.L.H. Menke, M. Harleveld, and J. Memelink, unpublished data), and a PE that induces Tdc and Str gene expression was obtained (Fig. 1).

View larger version (83K): [in this window] [in a new window]   Figure 1. PE and octadecanoids induce the TIA biosynthetic genes Tdc and Str. C. roseus cells were exposed to DMSO as a control (C) or PE, linoleic acid (LE), -linolenic acid (-LA), or MeJA for 6 h, after which time cells were harvested and total RNA was isolated. Northern blots were hybridized with Tdc, Str, and Rps9 cDNAs. The micromolar concentrations of the octadecanoids are given at the top.

Octadecanoids Induce TIA Biosynthetic Gene Expression

PE Induces JA Biosynthesis

1

View larger version (52K): [in this window] [in a new window]   Figure 2. YE elicitor induces JA biosynthesis. A, Amount of JA in C. roseus cells at different times after the addition of water as a control () or PE () or crude () YE. DW, Dry weight. B, Str, Tdc, and Rps9 mRNA levels at different times after the addition of water as a control (C) or of PE or crude (CE) YE. RNA was extracted from the same sample of tissue used to extract JA. The times in hours are indicated (top).

The Octadecanoid Pathway Mediates Elicitor-Induced TIA Biosynthetic Gene Expression

View larger version (31K): [in this window] [in a new window]   Figure 3. A, Effect of DIECA on TIA biosynthetic gene expression. C. roseus cell suspensions were incubated with DIECA for 10 min prior to the addition of water as a control (C), PE, or 50 µM MeJA, and cells were harvested 6 h later. The micromolar concentrations of inhibitors are indicated at the top. B, Effect of octadecanoid inhibitor on PE-induced JA accumulation. C. roseus cells were incubated with water or PE for 3 h. DIECA was added 10 min before the addition of PE. Bars represent SE (n = 3).

In a separate experiment to determine the effect of DIECA (500 µM) on JA biosynthesis, we found an inhibition of 95% relative to the PE-induced accumulation of JA (Fig. 3B). The corresponding northern blot showed that DIECA had a clear inhibitory effect on Tdc and Str mRNA accumulation in this experiment but did not affect the level of Rps9 mRNA. From Figure 3B, it is clear that strong inhibition of JA accumulation by DIECA resulted in a comparably strong inhibition of Tdc and Str mRNA accumulation. The results obtained with DIECA show that elicitor-induced Str and Tdc gene expression in C. roseus was mediated through the octadecanoid pathway.

Involvement of Protein Phosphorylation/Dephosphorylation

View larger version (38K): [in this window] [in a new window]   Figure 4. Protein kinases act upstream and downstream of JA. A, Effect of inhibitors on TIA biosynthetic gene expression. C. roseus cell suspensions were incubated with DSMO as a control (C), K-252a, calyculin A (CalA), or OA for 10 min before the addition of either PE or 50 µM MeJA, and cells were harvested 6 h later. The micromolar concentrations of the inhibitors are indicated at the top. B, Inhibition of PE-induced JA accumulation by a protein kinase inhibitor. C. roseus cells were incubated with 1 µM K-252a for 10 min before the addition of PE, and cells were harvested 3 h later. Bars represent the SE (n = 3).

To investigate whether a protein kinase is also active upstream of the octadecanoid pathway, we measured the effect of PE on JA levels in the presence of K-252a. In cells that were treated with 1 µM K-252a, the amount of JA that accumulated 3 h after the addition of PE was reduced to 15%, relative to the elicitor-induced level (Fig. 4B). In the same sample the amounts of Tdc and Str mRNAs were also reduced compared with the PE-induced sample, whereas the level of Rps9 mRNA was not affected. These results indicate that upstream of the octadecanoid pathway one or more protein kinases mediate the signaling triggered by PE, leading to jasmonate biosynthesis. The fact that K-252a and staurosporine both inhibited a broad range of protein kinases precludes any speculation about their identity.

We tested the effect of the protein phosphatase inhibitors calyculin A and OA on the expression of TIA biosynthetic genes. Addition of the protein phosphatase inhibitor calyculin A at 500 nM induced the accumulation of Tdc and Str mRNA in the absence of elicitor. The protein phosphatase inhibitor OA did not induce TIA biosynthetic gene expression in the absence of elicitor at the concentrations tested (Fig. 4A). We also tested the effect of the protein phosphatase inhibitors in the presence of MeJA. Treatment with either calyculin A or OA at 500 nM had no effect on the amounts of Tdc and Str transcripts induced by MeJA. Calyculin A and OA had no effect on the level of Rps9 mRNA. The induction of gene expression by calyculin A indicates that a protein phosphatase may be involved in the attenuation of TIA biosynthetic gene expression. The results show that protein kinase(s) mediated the elicitor-induced signal both upstream and downstream of the octadecanoid pathway and that protein phosphatase(s) was involved in attenuating the signal.

The Str Promoter Responds to Elicitor and MeJA

View larger version (55K): [in this window] [in a new window]   Figure 5. The Str promoter responds to elicitor and MeJA mRNA levels of gusA, Str and Rps9 in independent transgenic cell lines containing the BH construct (BH#1, BH#2, BH#3, and BH#4). Cells were incubated for 6 h with DMSO as a control (C) or with PE or MeJA. RNA (20 µg) was loaded per lane.

	DISCUSSION

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For wound-inducible proteinase inhibitor synthesis it has been well established that the octadecanoid pathway is involved in signal transduction, leading to transcriptional activation of proteinase inhibitor genes. The involvement of the octadecanoid pathway in elicitor-inducible expression of genes active in secondary metabolism, however, has not been as well characterized. In this study we established the involvement of the octadecanoid pathway in elicitor-induced transcriptional activation of genes of the TIA biosynthetic pathway in C. roseus cells.

Both Str and Tdc were up-regulated in response to low levels of exogenous MeJA and higher levels of the jasmonate precursor -linolenic acid. These results are in agreement with the observation that C. roseus seedlings (Aerts et al., 1994) and suspension-cultured cells (Gantet et al., 1998) can accumulate TIAs in response to MeJA and imply that octadecanoids stimulate TIA metabolism via induction of the biosynthetic genes. Furthermore, we observed a transient stimulation of endogenous jasmonate accumulation by the PE, which corresponded with the induction of the TIA biosynthetic genes Tdc and Str. A similar transient increase in endogenous JA was reported for the Rauvolfia, Agrostis, Eschscholtzia, Phaseolus, and Taxus species, as well as in rice and tobacco cell suspensions in response to elicitors (Gundlach et al., 1992; Mueller et al., 1993; Nojiri et al., 1996; Rickauer et al., 1997). However, it is not just elicitors that can trigger a transient increase in endogenous JA in plants; wounding (Peña-Cortés et al., 1995; O'Donnell et al., 1996) and UV radiation (Conconi et al., 1996) can also cause this increase. Together with our results, these data suggest a general role for the octadecanoid pathway in induced defense responses. Elevation of the level of JA in the plant cell seems to be sufficient to induce defense responses. Alternatively, elevated jasmonate levels could serve to lower the threshold for induction of a specific defense response by a pathogenic signal (Wasternack and Parthier, 1997). According to the latter scenario, a defined signal leads to a distinct response output due to a specific signal transduction cascade in combination with general, obligatory signaling. In both cases, inhibition of the octadecanoid pathway would leave plant cells unresponsive to the stress signal, thus inhibiting the induction of defense responses.

Inhibitors of jasmonate biosynthesis are useful for determining a direct involvement of the octadecanoid pathway in response to external stress. The induction of proteinase inhibitor genes in tomato by wounding and systemin can be blocked by DIECA (Farmer et al., 1994) and by acetyl-salicylic acid (Doares et al., 1995a). Nojiri et al. (1996) showed ibuprofen to be a potent inhibitor of elicitor-induced phytoalexin production in rice suspension cultures. In the current study in which suspension-cultured C. roseus cells were used, DIECA inhibited elicitor-induced TIA biosynthetic gene expression. This octadecanoid pathway inhibitor acts on the octadecanoid intermediate 13-S-hydroperoxylinolenic acid, and inhibited only elicitor-induced Tdc and Str gene expression; it did not affect the levels of Rsp9 mRNA (which encodes the 40S ribosomal protein S9). The results obtained using JA biosynthesis inhibitors should be interpreted with caution because these inhibitors may not be very specific. DIECA, for example, is also used as a free radical scavenger (Jabs et al., 1997). When we used other known inhibitors of the octadecanoid pathway, we found that they were not specific in our system. The lipoxygenase inhibitors ibuprofen and acetyl-salicylic acid inhibited elicitor- and MeJA-induced Tdc and Str mRNA accumulation but also had a strong negative effect on the level of Rps9 transcript. This indicates that these substances may be phytotoxic or that they may down-regulate transcription in general. These observations point out that it is important to evaluate the effect of these inhibitors on so-called housekeeping genes such as Rsp9.

Relatively little is known about the activation of jasmonate biosynthesis in response to stress. There is some evidence for protein kinases acting upstream of the octadecanoid pathway in elicitor- and wounding-induced responses (Blechert et al., 1995; Seo et al., 1995). The inhibition of PE-induced accumulation of endogenous JA in C. roseus cells by the protein kinase inhibitor K-252a suggests the need for protein phosphorylation in elicitor-induced signaling leading to stimulation of JA biosynthesis. Because K-252a inhibits a broad range of protein kinases, no conclusion can be made about the nature of the kinase(s) involved. However, Seo et al. (1995) suggested that a mitogen-activated protein kinase in tobacco may be a mediator of wound signal transduction upstream of the octadecanoid pathway. More recently, Stratmann and Ryan, (1997) showed that wounding and systemin in tomato plants can activate a mitogen-activated protein kinase-related kinase upstream of the octadecanoid pathway. Based on these results one might speculate that the kinase(s) acting upstream of the octadecanoid pathway in C. roseus is a member of the mitogen-activated protein kinase family. Downstream of the octadecanoid pathway one or more protein kinases are involved in transducing the JA signal. A protein kinase (cascade) ultimately changes the activity of transcription factors that regulate the expression of genes through the recognition of specific sequences in the promoter regions.

A number of cis-acting elements in the promoters of defense-related genes in diverse plant species that mediate responses to elicitors (Raventós et al., 1995; Rushton et al., 1996) or to MeJA (Kim et al., 1992; Xiang et al., 1996; Rouster et al., 1997) have been identified. Using transgenic C. roseus suspensions harboring Str promoter/gusA fusions we have demonstrated that elicitor- and MeJA-induced activation of Str gene expression occurs at the transcriptional level. In the Str promoter a region of 396 bp directly upstream of the translational start codon (BH) was sufficient to confer elicitor- and MeJA-responsive expression. This region of the Str promoter contains a G-box, an element that Kim et al. (1992) implicated in MeJA-responsive proteinase inhibitor II gene expression in potato. Detailed analysis of the Str promoter using 5 and internal deletion mutants is required to reveal whether the G-box is an important element in the Str promoter.

Figure 6 shows a hypothetical model that is consistent with the results described in this article. Elicitation of TIA biosynthetic gene expression is mediated through protein phosphorylation and the octadecanoid pathway leading to jasmonate. We have shown here that in C. roseus cells upstream of the octadecanoid pathway and downstream of jasmonate, one or more protein kinases are involved in mediating the signal toward Tdc and Str gene expression.

View larger version (31K): [in this window] [in a new window]   Figure 6. Model for elicitor signal transduction leading to TIA biosynthetic gene expression. The model shows the involvement of protein phosphorylation and the octadecanoid pathway in elicitor-induced TIA biosynthetic gene expression. Figure was adapted from Farmer and Ryan (1992). PK, Protein kinase; PP, protein phosphatase; TAF, transcription-activating factor.

	FOOTNOTES

   Received September 21, 1998; accepted December 8, 1998.

	ABBREVIATIONS

Abbreviations: BH, BglII/HincII. DIECA, diethyldithiocarbamic acid. JA, jasmonic acid. MeJA, methyl jasmonate. OA, okadaic acid. PE, partially purified YE elicitor. TIA, terpenoid indole alkaloid. YE, yeast extract.

	ACKNOWLEDGMENTS

The authors acknowledge Marga Harteveld for excellent assistance with purification of the PE and Leslie van der Fits for help with the transformation of C. roseus suspension-cultured cells.

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