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First published online September 7, 2007; 10.1104/pp.107.104851 Plant Physiology 145:853-862 (2007) © 2007 American Society of Plant Biologists
A Central Role of Abscisic Acid in Drought Stress Protection of Agrobacterium-Induced Tumors on Arabidopsis1,[W]Department of Molecular Plant Physiology and Biophysics (M.E., C.-W.L., W.H., R.H., R.D.), Department of Botany II (J.Z., M.R.), and Department of Pharmaceutical Biology (N.S., M.M.), Biocenter, Julius-von-Sachs-Institute, University of Wuerzburg, D–97082 Wuerzburg, Germany
Crown gall tumors induced by Agrobacterium tumefaciens represent a sink that has to be provided with nutrients and water by the host plant. The lack of an intact epidermis or cuticle results in uncontrolled loss of water. However, neither the tumor nor the host plant displays wilting. This phenomenon points to drought adaptation in both tumors and the crown gall host plant. To understand the underlying molecular mechanisms of protection against desiccation the gene expression pattern of Arabidopsis (Arabidopsis thaliana) tumors was integrated with the profile of stress metabolites: Arabidopsis tumors accumulated high amounts of abscisic acid (ABA), the ethylene precursor aminocyclopropyl carboxylic acid, osmoprotectants, and form a suberized periderm-like protective layer. Suberization of the outer tumor cell layers most likely is mediated by ABA since external application of ABA induced suberization of Arabidopsis roots. However, the expression level of the classical marker genes, known to respond to drought stress and/or ABA, was lower in tumors. Instead another set of drought and/or ABA-inducible genes was more highly transcribed. Elevated transcription of several ABA-dependent aquaporin genes might indicate that ABA controls the water balance of the tumor. The retarded tumor growth on abi and aba mutant plants underlined the importance of a tumor-specific ABA signaling pathway. Taken together, we propose that ABA is an important signal for protection of tumors against desiccation and thus supports tumor development.
Infection of plants by Agrobacterium tumefaciens can induce plant tumors, also referred to as crown galls, which develop upon integration of an Agrobacterium-derived T-DNA into the host plant genome (pMP90; Thomashow et al., 1980  ). Expression of the T-DNA-encoded oncogenes in turn promote biosynthesis of auxin and cytokinin, resulting in non-plant-controlled production of these phytohormones. This initiates cell proliferation as well as differentiation of a vascular network, which will connect the tumor to vascular bundles of the host plant and thus support the tumor with nutrients and water (Kado, 1984; Aloni et al., 1995; Mistrik et al., 2000; Ullrich and Aloni, 2000).
Tumors display a ruptured surface that is devoid of a cuticle covered epidermal cell layer; as a result tumors exhibit an increased water loss (Schurr et al., 1996
Protection against drought can also be achieved by a decrease in cellular osmotic potential due to synthesis and/or accumulation of osmoprotective compounds (see Mahajan and Tuteja, 2005
Adaptation to water stress results from an alteration in gene expression by up-regulation of the major ABA- and/or stress-responsive genes, like RD (response to dehydration), COR (cold responsive), LEA (late embryogenesis abundant)/dehydrin-like, and aquaporin genes (Seki et al., 2001
Here we have investigated the role of drought protective mechanisms during tumor development of A. tumefaciens (strain C58) induced crown galls. In contrast to previous studies (e.g. Mistrik et al., 2000
ABA Accumulation in Tumors Is Not Reflected on the Level of Gene Expression
In the search for triggers that might promote drought resistance of tumors we analyzed contents of the stress hormones ABA and aminocyclopropyl carboxylic acid (ACC), the latter of which is a precursor of the gaseous ethylene and can induce ABA biosynthesis (Hansen and Grossmann, 2000
Tumors and inflorescence stalks above the tumor exhibited a significant increase in ABA content compared to reference stalks of uninfected plants (around a 10-fold increase in tumor and 4-fold in the stalk above the tumor, respectively; Fig. 1B). However, this increase in ABA content is not reflected by the expression level of genes encoding enzymes of ABA biosynthesis or degradation (for review, see Nambara and Marion-Poll, 2005 ): Zeaxanthin epoxidase (AtZEP) and 9-cis-epoxycarotenoid dioxygenases (AtNCED1 and AtNCED4) were either decreased or unchanged (see AtNCED2, AtNCED3, AtNCED5, and AtNCED6 in Supplemental Fig. S1B). ABA2 and AAO3, encoding enzymes catalyzing the conversion of xanthoxal to abscisic aldehyde, or abscisic aldehyde oxidase, respectively, were not up-regulated (Supplemental Fig. S1B). The reliability of the microarray expression data for genes of the ABA biosynthesis pathway has been confirmed by real-time reverse transcription PCR (data not shown).
We found no evidence for ABA accumulation as a consequence of impaired degradation or an increase in release from conjugated forms, since gene expression of members of the CYP70A7 gene family (CYP70A7-1 to CYP70A7-4; Supplemental Fig. S1B), key enzymes of ABA degradation, remained unchanged in the tumor. AtBG1, encoding a
These data suggest that the elevated content of ABA in tumors is not autonomously synthesized in this tissue but might rather be translocated into the tumor by the host plant. Therefore, the distribution of ABA in tumor cross sections (Fig. 2A
) was visualized using antibodies against ABA following the method of Schraut et al. (2004)
The Role of ABA in Agrobacterium-Mediated Crown Galls To investigate the role of ABA in Agrobacterium-Arabidopsis interactions we took advantage of Arabidopsis mutants impaired in ABA biosynthesis or signaling. Aba3-1, a mutant with strongly reduced ABA levels due to impairment in the final step of ABA biosynthesis, showed 6 times reduced tumor growth compared to appropriate wild-type controls, Columbia-0 (Col-0; Fig. 3A ). Mutants affecting ABA-dependent signaling pathways, like the ABA-insensitive abi1-1, abi2-1, and abi4-1, exhibited reduced tumor growth (Fig. 3B). The ABA-insensitive mutant abi3-1, which affects the ABI3 transcription factor, had no effect on tumor growth. This indicated that ABA signaling, mediated by the ABA-dependent phosphatases ABI1 and ABI2, as well as the transcription factor ABI4, are relevant for tumor growth.
The ABA mutant phenotype could either be rescued genetically or by external application of ABA to deficient Arabidopsis plants to confirm the role of ABA in tumor development. However, as tumor growth requires 30 d and most of the externally supplied ABA would be metabolized and accumulate as phaseic and dihydrophaseic acid, which might produce unspecific side effects, revertants of abi1-1 were used (Gosti et al., 1999 ). The reduced tumor growth phenotype of abi1-1 mutant plants was rescued by the genetic revertants abi1-1R4 and abi1-1R5 (Fig. 3C). These revertants constitute double mutants, in which the original abi1-1 mutation is antagonized by additional mutations, resulting in attenuation of the abi1-1 mutant phenotype. Interestingly, the abi1-1R5 mutant, which displays a strong ABA-hypersensitive phenotype in the original drought stress screen of Gosti et al. (1999), also supported increased tumor growth in our assay (Fig. 3C). Due to the complex phenotype of the genetic manipulations in these mutants we cannot distinguish between their potential effects on either efficiency of T-DNA transformation or the tumor growth following the successful T-DNA integration into the plant cell genome. To address this issue the efficiency of T-DNA integration of mutant and wild-type plants was compared by determining the transient expression of the reporter gene GUS driven by the 2x cauliflower mosaic virus 35S promoter. The staining of three representative Arabidopsis leaves (Supplemental Fig. S2A) or inflorescence stalk segments (Supplemental Fig. S2B) showed slight differences. These visual differences, however, were not significant when calculating the number of stained leaves (Supplemental Fig. S2C) or determining the activity of GUS, applying a fluorimetric assay (Supplemental Fig. S2D). In summary, the extensive transient expression experiments revealed no significant differences in transformation efficiency between wild-type and ABA mutant plants. Thus, these functional studies reveal a fundamental effect of ABA on tumor growth and not on efficiency of T-DNA integration.
ABA signaling is well established as a mediator of drought stress adaptation in several plant models (Koornneef et al., 1984
Analysis of gene expression in tumor tissue points to a distinct mechanism of drought acclimation in Agrobacterium-induced tumors, which differs from that of other well-investigated tissues, like leaves or roots. Several genes regulated by drought and/or ABA showed transcriptional activation in tumors: LEA (At2g46140), two ABA response-related genes (At5g23350, At5g08350), HVA22c, and the drought-inducible AtDI21 (Supplemental Table S1). The expression of AtDR4, a representative gene for those that are down-regulated by ABA and drought stress in Arabidopsis roots, was 6 times lower in the tumor than in reference tissues. Moreover, a strong induction of four out of 35 Arabidopsis aquaporin genes in tumor tissue was observed. Some of these water channel genes are known to be regulated by drought and/or ABA to protect cells from desiccation (Seki et al., 2001
Plants develop an epidermal cell layer that is covered by a cuticle to prevent substantial water loss. As the tumor is lacking an intact epidermis, modifications of the tumor surface that can inhibit desiccation were analyzed by use of specific staining and fluorescence techniques. The distribution of suberin in Arabidopsis tumors can be visualized by Sudan-III staining, a red dye commonly used to visualize aliphatic cell wall components. Cross sections of tumors revealed red staining in cell walls of the outer cell layers and a group of cells in the middle of the cross section representing the surface of an emarginated tumor area (Fig. 2, E and F). In addition, strong autofluorescence in response to blue light (488 nm, the typical spectrum of phenolic compounds) was also observed in these cell layers (Fig. 2, H and I). These results are in accordance with the chemical composition of suberin, which contains aliphatic as well as phenolic moieties, and suggest that cell walls of the tumors' outer surface incorporate suberin. In contrast, the cuticle of the inflorescence stalk revealed Sudan-III staining (Fig. 2, E [arrows] and G) but no blue light-induced autofluorescence (Fig. 2H, arrows), indicating the presence of aliphatic cutin. The autofluorescence of vascular tissue (Fig. 2H) that is not stained by Sudan-III (Fig. 2E) is most likely caused by lignin phenolics.
The aliphatic domain of suberin is essentially composed of monomeric units of long chain fatty acid derivatives (
Like lignin, the aromatic moiety of suberin is composed of phenolic monomers with three distinct aromatic rings that differ in their number of methoxyl groups: p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S; Whetten and Sederoff, 1995 ; Lapierre et al., 1996; Schreiber et al., 1999). Suberized cell walls are often characterized by a higher H content in comparison to lignified tissue, and the yield of chemically degradable monomers is generally lower than in lignin (Zeier et al., 1999b). Using gas chromatography, we detected a substantial amount of H units in the tumor tissue (Fig. 5A
). By comparison, isolates from inflorescence stalks that consisted to a major part of lignified vascular bundles were almost exclusively composed of G and S units and only contained traces of H. Moreover, the total content of degradable lignin monomers was lower in tumor than in the inflorescence stalk tissue (Fig. 5B). These findings indicate the presence of aromatic constituents of suberin in tumor tissue.
In line with these results we found that the expression of genes encoding enzymes presumed to be involved in suberin biosynthesis was increased in tumors. The gene encoding the root-specific fatty acid  -hydrolase CYP86A1 was 3 times higher expressed in tumors than in inflorescence stalk. In addition, the transcription of genes, encoding components of the biosynthesis of phenolic compounds such as PHE-AMMONIA LYASE1 and 4-COUMARATE-COA LIGASE2 as well as a peroxidase (At2g38390) and the LIPID TRANSFER PROTEIN2, putatively involved in lipid transport, were elevated in tumors (Supplemental Table S2; Kolattukudy, 1981; Bernards and Razem, 2001; Kunst et al., 2004; Duan and Schuler, 2005). The histological and chemical analyses together with gene expression studies provide evidence that the outer cell layers of Agrobacterium-induced tumors are protected by suberized cell walls.
To determine whether ABA is generally capable of inducing suberization in Arabidopsis, the impact of exogenous ABA on root suberization, a process readily feasible for experimental analysis, was investigated. Aliphatic suberin in Arabidopsis roots revealed structural similarity to tumor suberin (Fig. 6A
). However, certain differences exist, as C18(1)-derived hydroxy- and diacids, which represent main components of many suberin polymers (Kolattukudy, 1984
Agrobacterium-induced plant tumors show increased water loss, resulting in a redirection of water flow and nutrient transport necessary for tumor development (Schurr et al., 1996 ; Wächter et al., 2003). On the contrary, increased water loss causes tissue desiccation. Thus, successful tumor development requires a well-tuned balance between these opposing factors. Here we present evidence that the phytohormone ABA is able to regulate both of these processes. On the one hand, ABA has the potential to dampen water loss by inducing suberization of the tumor surface. On the other hand, ABA regulates stress genes to increase the osmotic potential in tumors and by that can direct water flow to the tumor. We propose a mechanism by which ABA maintains water potential in tumor tissue.
In Arabidopsis, like in other plant species, tumors lack an intact epidermis. As shown here, tumors seem to be protected against water loss by two to three suberized cell layers. Suberin of the tumor surface is structurally and chemically closely reminiscent of the periderm that constitutes the surface tissue of above-ground organs in the secondary growth stage of dicotyledonous plants and gymnosperms or of wound periderm (Schönherr and Ziegler, 1980
The studies show that ABA induces suberin biosynthesis in Arabidopsis roots and that genes involved in this process were up-regulated in tumors. The root-specific NADPH-dependent P450-cytochrome monooxygenase CYP86A1, which catalyzes the biosynthesis of suberin aliphatic moieties, was 3 times elevated (Schuler and Werck-Reichhart, 2003
Although water loss is minimized in tumors, the tissue is still endangered by desiccation. Like in other species, tumors of Arabidopsis accumulate high levels of the stress hormone ABA (Mistrik et al., 2000
Both Arabidopsis and Ricinus tumors accumulate high amounts of the osmoprotectant Pro. This amino acid is involved in elevation of the cell turgor and hence in maintaining the osmotic balance under drought stress conditions (Wächter et al., 2003
Taken together, we propose the following working model on how ABA might support tumor development (Fig. 7
). While the physiological effects of ABA have already been discussed in previous paragraphs and are well in line with the effects discussed in the literature, our microarray analysis did not reveal any evidence for key enzymes of ABA metabolism being up-regulated in tumor tissue. Rather, immunolocalization of ABA suggests that this stress phytohormone might be translocated via the transpiration stream of the host plant into the tumor. This observation corresponds to earlier findings on the distribution of nitrate reductase activity, which was also found to be repressed in tumors; hence, amino acids have to be imported from the leaves as well (Deeken et al., 2006
This external supply of ABA has the potential to maintain the fine-tuned water balance in tumors autonomously. On the one hand, ABA-induced suberization of the tumor surface counteracts water loss. On the other hand, ABA-induced drought stress mechanisms, among them the accumulation of osmoprotectants, increase the osmotic potential and thus redirect water flow from the host plant to tumor. As both of these opposing effects are ABA triggered, communication between the tumor and plant via the gaseous factor ethylene can form a feed-forward loop to supply ABA from the plant to tumor.
Plant Material and Tumor Induction
Plant cultivation and tumor induction were performed as previously described (Deeken et al., 2006
Surface-sterilized Col-0 seeds were transferred into an Erlenmeyer flask containing 100 mL of sterile Murashige and Skoog growth solution (Murashige and Skoog salts [Sigma] supplemented with Gamborg's B5 vitamins [Sigma] and 1% Suc) and shaken at 50 rpm. Seedlings that developed a sufficient amount of root material within 2 weeks were taken and ABA was added to a final concentration of 10 µM to induce suberization. Roots were harvested 4 d later. Control roots were treated with water.
Four-week-old Arabidopsis tumors were infiltrated under vacuum and fixed for at least 24 h and further on treated as described in Schraut et al. (2004)
Tumor cross sections as used for ABA immunolocalization were stained with a saturated solution of Sudan-III in 92% ethanol (w/v) for 10 min at 70°C, then washed with glycerol:water (1:1, v/v). Sections were examined using a Leica DMR microscope with bright-field illumination or fluorescence excitation of 488 nm using a two-dimensional blue filter (Leica).
Analytical determination of suberin and lignin in isolated plant tissue (1–2 mg dry weight) was performed according to Zeier et al. (1999b)
Free ABA and ABA released from its conjugates was analyzed by ELISA as described earlier (Jiang et al., 2004
Plant material (200 mg, stored at –80°C) was mixed with 990 µL of methanol and 10 µL of acetic acid, homogenized, and extracted using a vibrating ball mill MM 301 (Retsch) for 3 min. Samples were centrifuged and the supernatant was dried in a vacuum centrifuge. As internal standard 50 ng norvaline was added. Samples were derivatized with pentafluorobenzyl (PFB) bromide and purified by vapor phase extraction prior to gas chromatography-mass spectrometric analysis in the negative ion chemical ionization mode as described recently (Mueller et al., 2006
For transient transformation of Arabidopsis, Agrobacterium GV3101 (pMP90; Koncz and Schell, 1986
The following materials are available in the online version of this article.
We are grateful to B. Roeger and T. Latz for excellent technical support and Professor C.I. Ullrich-Eberius (Institut für Botanik, Technische Hochschule Darmstadt, Germany) for supplying us with the A. tumefaciens strain. Received July 3, 2007; accepted August 9, 2007; published September 7, 2007.
1 This work was supported by the Deutsch Forschungsgemeinschaft (grant no. SFB567, project B5, to R.D.).  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: Rosalia Deeken (deeken{at}botanik.uni-wuerzburg.de).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.104851 * Corresponding author; e-mail deeken{at}botanik.uni-wuerzburg.de.
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ABSTRACT
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-glucosidase, hydrolyzing Glc-conjugated inactive ABA to free ABA (Bindschedler et al., 2006
-aminoadipinic acid and Glu levels were 9 (1.3 ± 0.06 versus 0.14 ± 0.014 µmol g–1 FW) and 4 (4 ± 0.54 versus 1.3 ± 0.05 µmol g–1 FW) times higher, respectively (Deeken et al., 2006
