Doi:10.1016/j.plantsci.2003.12.027

The rolB and rolC genes activate synthesis of anthraquinones in Rubia cordifolia cells by mechanism independent V.P. Bulgakov , G.K. Tchernoded , N.P. Mischenko , Yu.N. Shkryl , a Institute of Biology and Soil Science, Far East Branch of Russian Academy of Sciences, 159 Stoletija Street, Vladivostok 690022, Russia b Pacific Institute of Bioorganic Chemistry, Far East Branch of Russian Academy of Sciences, Vladivostok 690022, Russia Received 22 December 2003; accepted 22 December 2003 Abstract
Several studies have recently revealed an interesting ability of the rolC and rolB oncogenes of Agrobacterium rhizogenes to stimulate secondary metabolite production in plant cells. We have studied the role of the octadecanoid signaling pathway in the signal transductioninitiated by the rol genes in transformed Rubia cordifolia cell cultures. None of the octadecanoid pathway inhibitors tested (diethyldithiocar-bamate, propyl gallate, salicylhydroxamic acid and piroxicam) inhibited anthraquinone accumulation in the normal and transformed cultures.
This result indicates that the octadecanoid pathway is not involved in the rolB and rolC gene-mediated increase of anthraquinone produc-tion. Summarizing the data of previously reported and present investigations, we suggest that the rolB and rolC genes act downstream ofCa2+ signaling, H2O2-generating NADPH oxidase, as well as downstream of salicylic acid-mediated and octadecanoid pathways or perturbsecondary metabolism by unknown for plants way. An unusual effect of piroxicam, a member of non-steroidal anti-inflammatory drugs onanthraquinone production was detected: this inhibitor stimulated anthraquinone production in a greater extent then methyl jasmonate.
2004 Elsevier Ireland Ltd. All rights reserved.
Keywords: Rubia cordifolia; Anthraquinone; Octadecanoid pathway; rolB and rolC genes; Transformed plant culture 1. Introduction
tures of Panax ginseng tropane alkaloid production inAtropa belladonna hairy root cultures anthraquinone Agrobacterium rhizogenes causes formation of hairy roots production in callus cultures of Rubia cordifolia in plants, inserting a part of its plasmid DNA (T-DNA) Some data revealed that the rolC gene could affect activity into the plant genome. Numerous investigations showed that of defense proteins, such as 1,3-␤-d-glucanases. Expression hairy roots, being cultured in vitro, produced high levels of the rolC gene in ginseng cells caused significant increase of secondary metabolites Two T-DNA genes, the rolC of 1,3-␤-d-glucanase activity by production of a new en- and rolB oncogenes, are thought to be causal agents of this zyme isoform. Activities of other glucanases tested, such as phenomenon The single rolC and rolB genes were 1,6-, 1,4-␤-d-glucanases and 1,4-␣-d-glucanase, which are able to stimulate secondary metabolite production in trans- known to be unrelated to defense proteins, were unchanged genic plant tissues, e.g. nicotine production in Nicotiana tabacum root cultures, indole alkaloid production in Catha- Thus, it becomes apparent that the rol genes generate ef- rantus roseus cultures ginsenoside production in cul- fects which resemble defense reactions of plants. Such afunction of the rol genes would establish an interesting par-allel between processes of neoplastic transformation of plant Abbreviations: AQ, anthraquinone; MeJA, methyl jasmonate; DIECA, cells and events related to defense responses. Interestingly, diethyldithiocarbamic acid; PG, n-propyl gallate; SHAM, salicylhydrox- plant nuclear protooncogene homologs, such as myb and amic acid; SA, salicylic acid; NSAIDs, non-steroidal anti-inflammatory myc have multiple regulatory functions in metabolic path- ∗ Corresponding author. Tel.: +7-4232-312129; fax: +7-4232-310193.
ways not existing in mammalian cells. They are involved E-mail address: [email protected] (V.P. Bulgakov).
not only in the regulation of developmental processes, such 0168-9452/$ – see front matter 2004 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.plantsci.2003.12.027 V.P. Bulgakov et al. / Plant Science 166 (2004) 1069–1075 as trichome differentiation and seed development, but also was dissolved in dimethyl sulfoxide, PG (n-propyl gal- late) and SHAM (salicylhydroxamic acid) were dissolved Little is known about mechanisms by which the rol genes in ethanol. DIECA (diethyldithiocarbamic acid, trihydrate, perturb secondary metabolism. Studying the transgenic for sodium salt) was used as an aqueous solution. The NSAID the rolB and rolC genes callus cultures of R. cordifolia, piroxicam (4-hydroxy-2-methyl-3-[pyrid-2-yl-carbamoyl]- we have found that anthraquinone production was greatly 2H-1,2-benzothiazine 1,1-dioxide) was solubilized in hot increased in both transformed cultures compared with the ethanol, cooled and added to the medium. Sterile solu- non-transformed culture The induction of AQ biosyn- tions of the inhibitors were added to the autoclaved me- thesis by rol genes did not proceed through the activation of dia aseptically in desired concentrations. Equal volumes the common Ca2+-dependent NADPH oxidase pathway that of the appropriate solvents were added to the control mediates signal transduction between an elicitor–receptor complex via transcriptional activation of defense genes Okadaic acid and cantharidin, inhibitors of protein phos- 2.3. Estimation of the anthraquinone content phatases 1 and 2A, caused an increase of AQ production intransgenic cultures. Okadaic acid stimulated AQ accumu- Purpurin and munjistin were previously isolated from lation in the non-transformed culture, whereas cantharidin R. cordifolia calluses and analysed as described by Mis- had no effect. These results have shown that different phos- chenko et al. Anthraquinone content was determined phatases are involved in AQ synthesis in normal and trans- in 30-days cultures photometrically Briefly, 100 mg of the dried powdered calluses with 0.3 ml 5 N HCl added Octadecanoid signaling pathway plays a key role in syn- were extracted with 3 ml ethanol at room temperature and thesis of phytoalexin-type secondary metabolites during absorption spectra were recorded. The purpurin content of plant-microbe interaction To test whether stimu- the ethanol extract was determined by absorption at 515 nm.
lation of anthraquinone phytoalexins by the rol genes is The content of munjistin was quantified by absorption at mediated by the octadecanoid pathway, we used a phar- 421 nm, subtracting the absorption due to purpurin at this macological approach. Inhibitors of jasmonate biosynthesis wavelength. All cultures produced only two major AQs, with are useful for determining a direct involvement of the oc- munjistin and purpurin representing 90% of the total AQ tadecanoid pathway in response to external stimuli Several researchers successfully applied inhibitors, such asPG, DIECA and SHAM, to show necessity of the func-tional octadecanoid pathway in the stimulation of phy- 3. Results
toalexins and defense proteins Our results indicatethat octadecanoid signaling pathway is not involved in 3.1. Stimulatory effect of MeJA on AQ production the rol-gene-mediated increase of AQ accumulation in thetransformed R. cordifolia calluses.
Anthraquinone content was reported to be 0.2% DW for R. cordifolia wild-growing roots and 0.62–1.22% DWfor non-transformed callus cultures, derived from dif- 2. Materials and methods
ferent organs of R. cordifolia The AQ levels inRc culture ranged from 0.4 to 1.2% DW, whereas those of the Rc-rolC3 and Rc-rolB cultures was 1.4–2.3 and1.9–3.2% DW, respectively The highest level of Transgenic cultures Rc-rolC3 and Rc-rolB were es- biosynthetic ability of R. cordifolia calluses, which we de- tablished from leaves of a 3-week-old axenic R. cordi- tected in different elicitor experiments, was 5.0–5.2% DW folia plant Plasmid vectors pPCV002-CaMVBT and pPCV002-CaMVC used to obtain the transformed We studied effect of MeJA on the rolB calluses for callus cultures. The non-transformed Rc callus culture was ten month. Within this period the Rc-rolB culture accu- established from the leaves of the same plant and cultivated mulated 1.53–4.47% of AQs. shows a relation- in the identical conditions as the transformed cultures. All ship between initial content of AQs in MeJA-treated rolB cultures were cultivated in 100 ml Erlenmeyer flasks on calluses and stimulatory effect of MeJA. High negative WB/A solid medium supplemented with 0.5 mg l−1 correlation dependence (r = −0.97) was found between 6-benzylaminopurine and 2.0 mg l−1 ␣-naphthaleneacetic these parameters: the more initial level of AQs, the less acid, in the dark, at 25 ◦C with 30-day subculture intervals.
stimulatory effect of MeJA. Thus, when the rolB cul-ture produced some ‘saturating’ level of AQs, MeJa no longer activated AQ synthesis. Such dependence was notfound for the Rc and Rc-rolC cultures (r = −0.09 and Reagents for tissue culture and MeJA were obtained from −0.37, respectively), probably because they produced less Sigma, the others were from ICN Pharmaceuticals. MeJA V.P. Bulgakov et al. / Plant Science 166 (2004) 1069–1075 (When added to the culture media simultaneously Growth of R. cordifolia cultures in the presence of octadecanoid pathway with MeJA, DIECA did not prevent stimulatory effect of MeJA Moreother, AQ accumulation was enhanced in the Rc, Rc-rolC and Rc-rolB cultures on 36, 68 and 35%, The similar paradoxical effect of DIECA on phytoalexin production was firstly found and explained by Jabs et al. These authors have shown that DIECA treatment of pars- The values are represented as percentage from values of the cultures of the oxidative burst maximum, caused by elicitors. Addi- growing on inhibitor-free medium. Values are means ± S.E. from two tion of DIECA to the parsley cells in the absence of elicitor experiments with 10 replicates each.
prevented rapid degradation of O − and thus stimulated ac- P < 0.05 vs. Rc culture, Student’s t-test.
cumulation of furanocoumarin phytoalexins to 18 ± 4% ofthe elicitor response 3.2. Effect of DIECA, PG and SHAM on anthraquinone PG is often used as an inhibitor of lipoxygenases PG inhibited expression of those genes, which activity isregulated via the octadecanoid pathway, e.g. the thionin To explore the involvement of the octadecanoid pathway in the rol-gene-mediated increase of AQ accumulation in R. ajmalicine synthesis in C. roseus cells cordifolia cultures, we tested different inhibitors of this path- The patterns of AQ inhibition in Rc and Rc-rolC R. cordi- way. We used those concentrations of inhibitors that sup- folia cultures by PG were similar to those observed in the ex- pressed growth of the R. cordifolia cultures approximately periment with DIECA (Interestingly, the Rc-rolB culture, which in this experiment accumulated high level of cultures were more resistant to PG, SHAM and piroxicam AQs (5.3% DW) without any treatment, was not susceptible to PG and MeJA treatments (However, when both In plants, DIECA inhibits the octadecanoid signal- effectors were applied simultaneously, the rise of AQ pro- ing pathway downstream of lipoxygenase by shunting duction was detected (It is noteworthy that the rolB 13-hydroperoxylinolenic acid to 13-hydroxylinolenic acid, culture has accumulated in this experiment 34-fold more thereby reducing the precursor pool leading to cyclization AQs (6.8% DW) than wild-growing roots.
and eventual synthesis of jasmonic acid y suppressing PG limited the availability of Fe2+ and prevented the of the octadecanoid pathway, DIECA inhibited ajmalicine generation of hydroxyl radicals thus protecting cells from synthesis elicitor-induced terpenoid indole alkaloid H2O2-induced damage However, PG induced sin- biosynthetic gene expression in C. roseus gle strand breaks in DNA at concentrations higher than In our experiments, DIECA failed to inhibit AQ syn- 0.25 ␮M, changing the antioxidative and cytoprotective thesis in non-transformed and both transformed cultures properties to prooxidative and cytotoxic properties, when tion,
la
u
m
AQ content, % DW
Fig. 1. Effect of MeJA (10 ␮M) on AQ accumulation in Rc-rolB calluses in dependence of background AQ levels. Cultures were grown for 4 weeks onWB/A medium.
V.P. Bulgakov et al. / Plant Science 166 (2004) 1069–1075 it was combined with copper Copper sulfate is a com- Rc-rolC3
B/A medium, which we use for cultivation of R. cordifolia calluses. In a separate experiment, we culti- vated Rc, Rc-rolB and Rc-rolC calluses on the media lack- 4. The elimination of copper from the medium did not change growth and biosynthetic properties of all cultures tested (data not shown), suggesting that possible prooxida- tive effect of PG/Cu2+ combination could be excluded from PG and SHAM are used as lipoxygenase inhibitors possessing very similar pharmacological activity SHAM like PG did not inhibited AQ production either in Rc-rolC3
non-transgenic or transgenic R. cordifolia cultures ( The synergistic effect of PG/MeJA on AQ accumulation was confirmed in the experiment with SHAM. When grown in the presence of SHAM and MeJA, the Rc, Rc-rolC and Rc-rolB cultures accumulated 11, 84 and 70% more an- thraquinones, respectively, than the same cultures grown with MeJA (One can speculate that PG and SHAM changed their antioxidative properties to prooxidative ones, being combined with MeJa in our test system. It could lead to the generation of reactive oxygen intermediates, whichin concert with MeJA activated AQ production.
Rc-rolC3
3.3. Strong induction of AQs by piroxicam content
Q
A
Piroxicam, a member of non-steroidal anti-inflammatory drugs (NSAIDs), effectively inhibited lipoxygenase activ-ity in extracts from elicited tomato leaves Piroxicam not only did not inhibited AQ accumulation in the RC, Rc-rolC and Rc-rolB cultures, but caused 2.6-fold, 2.1-fold and 1.6-fold increase of AQs in these cultures, respectively Fig. 2. Effect of DIECA (A), PG (B) and SHAM (C) on AQ content (% (The stimulatory effect of piroxicam on AQ pro- DW) in R. cordifolia non-transformed (Rc) and transformed (Rc-rolC3 duction in R. cordifolia cultures was even more pronounced and Rc-rolB) callus cultures. Values are means from two experiments with ten replicates each. Vertical bars represent standard errors.
To our knowledge, the effect of piroxicam on produc- tion of secondary metabolites was first examined in this Rc-rolC3
Fig. 3. Effect of piroxicam on fresh biomass accumulation (g) after 4 weeks of culture and AQ content (% DW) in R. cordifolia non-transformed (Rc)and transformed (Rc-rolC3 and Rc-rolB) callus cultures. Values are means from two experiments with ten replicates each. Vertical bars represent standarderrors.
V.P. Bulgakov et al. / Plant Science 166 (2004) 1069–1075 study. It is intriguing that piroxicam caused the strong in- However, AQ production was not decreased by all in- duction of AQs. In previous years, most investigations with hibitors of octadecanoid pathway, which was used in the NSAIDs were carried out on animals, because NSAIDs present study (DIECA, PG, SHAM and piroxicam), either possess a strong inhibitor activity against mammalian cy- in non-transformed or transformed with the rolC and rolB clooxygenases and lipoxygenases and exert preventive effect genes calluses of R. cordifolia (Based on against carcinogenesis In human carcinoma cells, these results we concluded that (i) the production of AQs NSAIDs stimulated the three families of MAPK, extracel- in non-transformed cells of R. cordifolia does not proceed lular regulated kinases, c-Jun N-terminal kinases and p38 through the activation of the octadecanoid pathway and (ii) MAPK It is unknown whether or not similar mech- the octadecanoid pathway is not involved in the rolB and anism operates in plant cells. Protein kinases ultimately rolC gene-mediated increase of anthraquinone biosynthesis.
change the activity of plant transcription factors that regulate Several authors noted that the results obtained with in- the expression of defense genes through the recognition of hibitors of octadecanoid pathway must be interpreted with specific sequences in the promoter region (e.g. Down- caution, because most of them possessed additional ac- stream of the octadecanoid pathway, one or more protein ki- tivities, seemingly unrelated to their possibility to inhibit nases are involved in transducing the jasmonate signal the octadecanoid pathway Therefore, these results When piroxicam was used simultaneously with MeJA, no should be considered as preliminary results and additional additive effect on AQ accumulation was observed ( evidences supporting the inhibitory experiments should be suggesting that MeJA and piroxicam might compete for the We cannot exclude the possibility that, in natural con- ditions, both SA- and jasmonate-dependent pathways playa role in phytoalexin synthesis during the interaction of 4. Discussion
pathogenic microorganisms with R. cordifolia plants. How-ever, it seems unlikely that these effectors are involved in Because synthesis of phytoalexin-type secondary metabo- the increase of AQ production by the rol genes.
lites is a part of the defense reaction of plants, the question Summarizing the data of previously reported and present arises whether or not rol-gene signals interfere with gen- investigations, we suggest two scenarios of the rolB and rolC eral plant defense pathways. It is now generally accepted, genes action on secondary metabolism. According to the first that during plant-microbe interaction, the signal is amplified one, they act via known defense mechanisms downstream of via increased intracellular Ca2+ due to the opening of Ca2+ the Ca2+ signaling, H2O2-generating NADPH oxidase com- channels The increase of intracellular Ca2+ concen- plex, as well as downstream of SA- and jasmonate-mediated tration activates a Ca2+ dependent protein kinase(s) which, pathways. According to the second scenario, they perturb in turn, activates NADPH oxidase The involvement secondary metabolism by an unusual way, which is not ubiq- of the oxidative burst generated by NADPH oxidase in the process of phytoalexin stimulation is well known Although processes of ROS generation by mammalian The octadecanoid pathway intermediates, including jas- oncogenes, as well as the role of oxidative stress in many monic acid and methyl jasmonate, also play a crucial role aspects of oncology are a subject of unfailing interest of nu- in activation of synthesis of phytoalexin-type secondary merous investigations a theme for plant onco- metabolites derived from different biosynthetic pathways genes has never been considered. Vafa et al. is a general rule, although some data revealed demonstrated that in normal human fibroblasts, c-Myc ac- existence of jasmonate-independent signal transduction tivation could induce DNA damage that correlated with in- pathways, leading to activation of secondary metabolites duction of reactive oxygen species. The authors proposed SA- and ethylene-dependent pathways, in concert that the oncogene activation could override damage controls, with MeJA or independently, could also stimulate phy- thereby accelerating tumor progression via genetic instabil- toalexin production in affected by pathogens plants ity. It is unknown whether the rol genes act similarly, but According to previously obtained results, ethylene had no such a possibility cannot be excluded. Studying the effect effect on AQ production in the normal and transgenic R. of the rolC gene on ginseng cells, we have found that the cordifolia cultures SA increased AQ accumulation in gene caused chromosome instability in primary rolC-tumors the transgenic and non-transgenic calluses with very simi- and derived from them teratoma tissues It will be in- lar dynamics, indicating that the rol-gene-activator signals teresting to determine for future experiments whether the functioned independently from the SA signaling pathway rol genes change ROS generation in plant cells. Because the Ca2+ influx is not necessary for activator function of NADPH oxidase signaling pathway thought to be is not in- the rol genes. Likewise, the NADPH oxidase signaling path- volved in the rolB and C gene-mediated activation of AQ way is not involved in activator effect of these genes production other known pathways of ROS generation Therefore, if the rol genes activated secondary metabolism in rol-gene-transformed cells would be elucidated, such as via octadecanoid pathway, it would establish a link between ROS generation by cell wall-bound peroxidases and ROS the rol-gene effects and known defense pathways.
generation by apoplastic amine oxidase-type enzymes V.P. Bulgakov et al. / Plant Science 166 (2004) 1069–1075 Acknowledgements
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