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First published online August 26, 2005; 10.1104/pp.105.062372 Plant Physiology 139:341-352 (2005) © 2005 American Society of Plant Biologists
NpPDR1, a Pleiotropic Drug Resistance-Type ATP-Binding Cassette Transporter from Nicotiana plumbaginifolia, Plays a Major Role in Plant Pathogen Defense1Unité de Biochimie Physiologique, Institut des Sciences de la Vie, Université Catholique de Louvain, B–1348 Louvain-la-Neuve, Belgium (Y.S., S.G., T.T., D.V., M.B.); and Département Biotechnologie, Centre Wallon de Recherches Agronomiques, B–5030 Gembloux, Belgium (A.B.)
Nicotiana plumbaginifolia NpPDR1, a plasma membrane pleiotropic drug resistance-type ATP-binding cassette transporter formerly named NpABC1, has been suggested to transport the diterpene sclareol, an antifungal compound. However, direct evidence for a role of pleiotropic drug resistance transporters in the plant defense is still lacking. In situ immunolocalization and histochemical analysis using the gusA reporter gene showed that NpPDR1 was constitutively expressed in the whole root, in the leaf glandular trichomes, and in the flower petals. However, NpPDR1 expression was induced in the whole leaf following infection with the fungus Botrytis cinerea, and the bacteria Pseudomonas syringae pv tabaci, Pseudomonas fluorescens, and Pseudomonas marginalis pv marginalis, which do not induce a hypersensitive response in N. plumbaginifolia, whereas a weaker response was observed using P. syringae pv syringae, which does induce a hypersensitive response. Induced NpPDR1 expression was more associated with the jasmonic acid than the salicylic acid signaling pathway. These data suggest that NpPDR1 is involved in both constitutive and jasmonic acid-dependent induced defense. Transgenic plants in which NpPDR1 expression was prevented by RNA interference showed increased sensitivity to sclareol and reduced resistance to B. cinerea. These data show that NpPDR1 is involved in pathogen resistance and thus demonstrate a new role for the ATP-binding cassette transporter family.
ATP-binding cassette (ABC) transporters, which belong to a protein superfamily found in all living organisms, mediate the translocation of a wide range of structurally unrelated molecules across biological membranes (Higgins, 1992  ; Holland et al., 2002). All functional ABC proteins have a basic structural organization consisting of a hydrophobic transmembrane domain (TMD), usually made up of six transmembrane spans, and a hydrophilic nucleotide binding fold (NBF). The latter contains a conserved 200 amino acid region with three motifs, the Walker A and Walker B boxes (Walker et al., 1982), which are separated by approximately 120 amino acids that contain the ABC signature motif (Bairoch, 1992). The TMD and NBF are usually arranged in a duplicated forward (TMD-NBD-TMD-NBD) or reverse (NBD-TMD-NBD-TMD) configuration, and these proteins are known as full-size ABCs. However, half-size transporters, which can act as dimers, have also been reported (see Pighin et al., 2004 for a recent example in plants). In some cases, especially in prokaryotes, the different structural domains can be encoded as separate subunits, referred to as quarter molecules (Higgins, 1992).
The complete sequencing of the Arabidopsis (Arabidopsis thaliana) genome allowed the identification of 131 ABC transporter coding sequences (Sanchez-Fernandez et al., 2001
The MRP subfamily contains the best-characterized plant ABC transporters. Some of these are responsible for the vacuolar import of chlorophyll catabolites and xenobiotics or endogenous metabolites conjugated to glutathione, glucoside, or glucuronate (for review, see Rea, 1999
The MDR subfamily contains Arabidopsis AtPGP1 (P-glycoprotein 1), the first plant ABC transporter to be cloned (Dudler and Hertig, 1992
The plant PDR subfamily has been poorly investigated. For some of its members, a link between the ABC transporter and a physiological substrate has been demonstrated. The plasma membrane transporter NpABC1 (from now on, NpABC1 will be called NpPDR1 to specify the subfamily it belongs to) was identified in Nicotiana plumbaginifolia culture cells treated with sclareol, an antifungal diterpene, and was indirectly shown to transport a sclareol analogue, suggesting, but not demonstrating, the involvement of this transporter in plant defense (Jasinski et al., 2001
Plant defense mechanisms are varied, depending on the plant and pathogen involved. In most cases, the plant response is complex, including both constitutive and pathogen-induced defense mechanisms. The latter generally involves either the salicylic acid (SA)- or jasmonic acid (JA)-controlled pathway. In addition to defense proteins, such as various lytic enzymes, secondary metabolites participate in constitutive or induced defense (Feys and Parker, 2000
The involvement of PDR-type transporters in plant defense is supported by the observations that a pathogen-produced elicitor induces NtPDR1 expression in an Nicotiana tabacum suspension culture (Sasabe et al., 2002
NpPDR1 Expression in N. plumbaginifolia
NpPDR1 has been previously immunodetected in N. plumbaginifolia peeled leaf epidermis (Jasinski et al., 2001
In situ immunolocalization studies on N. plumbaginifolia peeled leaf epidermis localized NpPDR1 to the glandular trichomes (Fig. 1B), whereas plasma membrane H+-ATPase was mainly found in the stomatal guard cells (Fig. 1C). To confirm this, we introduced a DNA construct containing the gusA reporter gene under the control of the NpPDR1 transcription promoter region into N. tabacum; this construct has been shown to function in N. tabacum BY2 cells but has not been tested in plants (Grec et al., 2003 ).  -Glucuronidase (GUS) histochemical analysis of the epidermis of the transgenic plants confirmed that NpPDR1 was expressed in the leaf trichomes (Fig. 1D). NpPDR1 expression analysis was extended to other organs. Western blotting of the root of a plant grown in soil showed that NpPDR1 was expressed throughout the entire length of this organ and that expression was also observed in hydroponic culture and in sterile in vitro culture (Fig. 1E). In situ immunolocalization failed to detect NpPDR1 in the root, probably because the antigenic determinants were lost during the harsh embedding conditions. However, in transgenic plants expressing NpPDR1-gusA, GUS expression was seen in the whole root, except for the tip (Fig. 1F). Cross section showed expression in most of the root cells. Western blotting with flower organs showed that NpPDR1 expression was exclusively found in the upper part of the petal (Fig. 1G).
The antimicrobial properties of sclareol and other terpenes (Bailey et al., 1975
The difference in the responses seen using P. syringae pv syringae, which induces HR, and the other strains, which do not, prompted us to examine markers of the SA and JA signaling pathways involved in plant defense. Using reverse transcription (RT)-PCR (Fig. 2C), we found that the PR1a gene, an SA pathway-dependent marker, was only induced following infection with P. syringae pv syringae PsP2, while the PR2b gene, a JA pathway-dependent marker, was up-regulated to a greater extent following infection with P. syringae pv tabaci LMG 5393, P. fluorescens LMG 1794, or P. marginalis pv marginalis LMG 5177, all of which induced strong NpPDR1 expression. Examination of the effect of JA, SA, and ethylene infiltration confirmed these data; NpPDR1 expression was more induced by JA than by the other two chemicals (Fig. 2D), in agreement with previous data obtained with N. tabacum suspension cells (Grec et al., 2003 ). All together, these data suggest that NpPDR1 is predominantly involved in an induced defense pathway distinct from the SA-dependent HR.
In order to decipher the physiological function of NpPDR1 and investigate its possible involvement in the plant-pathogen response, we prevented its expression by RNA interference. We thus obtained transgenic plants expressing a double-stranded RNA corresponding to a region encompassing nucleotides 12 to 434 of the NpPDR1 cDNA. Several transgenic plants showed no NpPDR1 expression (western blotting) in the leaf epidermis or in the whole leaf upon induction by sclareol infiltration (four independent lines are shown in Figure 3A). Induction of NpPDR1 expression in the whole leaf by P. syringae pv tabaci was prevented as found by northern (Fig. 3B) and western blotting (Fig. 3C). In order to investigate in more detail the involvement of NpPDR1 in sclareol transport, we took advantage of the toxic properties of this diterpene (Cutler et al., 1977
The NpPDR1-silenced plants did not show any particular modification of growth and development compared to the wild type. Since the antimicrobial properties of sclareol and the response of NpPDR1 to biotic stress suggest the involvement of NpPDR1 in the plant-pathogen response, the resistance of wild-type and NpPDR1-silenced plants to P. syringae pv tabaci was tested by leaf infiltration. Although, in some experiments we observed that the transgenic plants were more susceptible to the pathogen and showed a faster burnishing of the infiltrated zone (data not shown), these data were not systematically observed and were not investigated further. On the other hand, increased pathogen susceptibility of NpPDR1-silenced plants was evidenced by their frequent spontaneous infection by a fungus identified as B. cinerea (Fig. 5), which never occurred in wild-type plants. B. cinerea infection led to rotting at the root-stem junction and, eventually, plant death sometimes before the flowering stage. This was observed for the four lines tested but not for the wild-type plants (Fig. 5D). Fungal growth was frequently observed along the stem and on the lower stalk leaves. Western blotting showed that NpPDR1 expression was induced in wild-type leaf disks infected by B. cinerea (Fig. 6A). We then challenged the resistance of leaf disks of wild-type and four silenced plants to B. cinerea and found that silenced plants were clearly more susceptible to the pathogen; for 38 out of 48 leaf disks (divided in three independent experiments) of silenced plants, clear signs of pathogen development (Fig. 6B) were observed, while none was detected for the wild-type plant. B. cinerea susceptibility was also challenged on 14 plantlets in soil. All of the NpPDR1-silenced plantlets clearly showed severe infection development, while this was not the case for the wild-type (Fig. 6C).
The previous characterization of NpPDR1, performed on a N. plumbaginifolia suspension cell culture (Jasinski et al., 2001 ), suggested that it is involved in sclareol transport, and the antimicrobial properties of this diterpenoid (Bailey et al., 1975) led to the conclusion that NpPDR1 might be involved in plant defense. However, this hypothesis is not yet supported by any experimental data and is even questioned by the observation that Arabidopsis plants knocked out for AtPDR12, the closest homolog of NpPDR1, do not show increased susceptibility to the pathogens tested (Campbell et al., 2003). As the expression profile at the cellular level of NpPDR1 or its S. polyrrhiza and Arabidopsis homologs had not been reported, we first determined NpPDR1 expression using the gusA reporter gene. We showed that NpPDR1 was detected in the leaf glandular trichomes, consistent with its involvement in the secretion of the sclareol-related diterpenes found in the leaf exudates of Nicotiana species (Colledge and Reid, 1975; Severson et al., 1984). In the root, expression was found in most cell types. We could eliminate the possible up-regulation of NpPDR1 expression in response to soil microorganisms since the protein was also immunodetected in roots of plants grown under sterile conditions. This is in agreement with the constitutive presence of antimicrobial terpenes and other metabolites in this organ (Oberlies et al., 2001; Ulubelen et al., 2001; Chen et al., 2002; Tan et al., 2002).
NpPDR1 expression in the upper part of the petal might also be related to plant defense like in other organs. However, petals are involved in the biosynthesis of flower volatile metabolites (Dudareva and Pichersky, 2000
The strong up-regulation of NpPDR1 in the whole leaf after infection by the bacteria P. syringae pv tabaci, P. fluorescens, and P. marginalis pv marginalis and the fungus B. cinerea, suggests its involvement in induced plant defense resulting in the secretion of secondary metabolites, such as sclareol and other diterpenes, which inhibit the growth of the invading organism. The lower induction of NpPDR1 expression seen after P. syringae pv syringae infection might be explained by the inhibitory effect of SA on the JA-dependent defense pathway (Doares et al., 1995
A recent analysis of the response of NtPDR1, a N. tabacum gene related to, but not an ortholog of, NpPDR1, to microbial elicitors in tobacco suspension cells showed that its expression is induced by JA, but not SA, and that NtPDR1 expression is up-regulated by elicitors, some of which induce HR, linked in many instances to the SA pathway (Sasabe et al., 2002
These data contrast with those reported in a study on the pathogen response of AtPDR12, the closest NpPDR1 homolog in Arabidopsis (69.6% amino acid sequence identity). Campbell et al. (2003) As P. syringae pv tabaci was shown to induce NpPDR1 expression, it could be hypothesized that preventing NpPDR1 expression would make the plant more sensitive to this bacteria. Actually we did not observe reproducible higher sensitivity of NpPDR1-silenced plants to this strain. This suggests that the substrates transported by NpPDR1 are not the only defense mechanism that protects the plant against this pathogen. On the contrary, preventing NpPDR1 expression clearly increased the plant's susceptibility to the fungus B. cinerea to such an extent that spontaneous infection was observed that eventually led to plant death. This observation demonstrates the major role of NpPDR1 in the plant defense.
The question of the substrates transported by NpPDR1 is still puzzling, like for many ABC transporters. Sclareol has been used as a model substrate for NpPDR1 (Jasinski et al., 2001 In conclusion, the localization of NpPDR1 expression to the leaf trichomes and the roots and its response to biotic stress support its involvement in the secretion of defense-related metabolites, both as a constitutive defense barrier and as part of an inducible defense mechanism. The finding that NpPDR1 silencing resulted in increased susceptibility to sclareol and spontaneous infection by B. cinerea provides direct evidence for a role of NpPDR1 in plant defense and defines a new function for the ABC transporter family.
Plant Material Nicotiana plumbaginifolia seeds were treated with 500 µg/mL of gibberellic acid and germinated on humidified compost. After germination, the plants were grown in compost in a growth chamber under conditions of 16 h light (200 µmol photons s–1 m–2 at soil level) at 25°C and 8 h dark at 19°C. For in vitro culture, seeds of transgenic Nicotiana tabacum L. cv SRI and N. plumbaginifolia were sterilized for 1 min in 70% (v/v) ethanol and 3 min in 50% (v/v) commercial bleach, then washed five times in sterile water. N. plumbaginifolia seeds were further treated with 500 µg/mL of 0.22 µm-filtered gibberelic acid. Transformants were selected on solid Murashige and Skoog medium (4.4 g/L of Murashige and Skoog salts [ICN Biomedicals], pH 5.6, 3% Suc, 1% agar) supplemented with 100 mg/L of kanamycin, and grown at 25°C under conditions of 16 h light (50 µmol photons s–1 m–2) and 8 h dark. When rooted, the plants were transferred to soil and grown in growth chambers as described above.
The NpPDR1 cDNA 5' region encompassing nucleotides 12 to 434 was amplified using two sets of oligonucleotides containing additional restriction sites (5'-ATAGGTCTCGAGTTTTCAGTTCATTTGATC-3' and 5'-TGTGTGAATTCTTCTATTCTTGAGTTTCAG-3' for the sense fragment, and 5'-ATTCGTGGATCCTTTTCAGTTCATTTGATC-3' and 5'-TGTGTAAGCTTTTCTATTCTTGAGTTTCAG-3' for the antisense fragment) and cloned in the sense and antisense orientation into the polylinkers flanking a pyruvate orthophosphate dikinase intron in the pKANNIBAL plasmid (Wesley et al., 2001
The 1,282-bp sequence upstream of the NpPDR1 transcription initiation site was fused to the gusA reporter gene and the construct inserted into the pBi 101.1 binary vector (Jefferson et al., 1987
Pseudomonas syringae pv tabaci LMG 5393 (Laboratorium voor Microbiologie van Gent, collection no. 5393 [Belgian Coordinated Collections of Microorganisms, BCCM]), Pseudomonas fluorescens LMG 1794, Pseudomonas marginalis pv marginalis LMG 5177, and P. syringae pv syringae PsP2 were grown overnight at 28°C in King B medium (King et al., 1954
The fungal strain isolated from two independent spontaneous infection events of NpPDR1-silenced plants was identified by the BCCM section of the Université catholique de Louvain (http://bccm.belspo.be/index.html) as Botrytis cinerea according to morphological properties of the mycelium and spores. The strain was indexed as Mycothèque Université catholique de Louvain 46725.
Monospore cultures of B. cinerea were grown in petri dishes on solid yeast dextrose medium (2% [w/v] Glc, 2% [w/v] yeast extract, 2% [w/v] agar). Spores were collected in 1 mL of sterile 0.1% (w/v) Tween 80, filtered on Miracloth paper (Calbiochem), and diluted in water to the appropriate concentration after counting (Thomas cell). For in vitro leaf-disk infection assays, 1 cm2 leaf disks were cut from 2-month-old in vitro-grown plants and laid on two blotting papers (MN 218B, Macherey-NagelO) wetted with sterile water and were then spotted with 5 µL of the B. cinerea suspension (104 or 105 spores/mL). For in vitro root-infection assays, 2-month-old in vitro plants were transferred to sterile peat pellets (Jiffy Products International AS) in a closed box and infected 2 weeks later by addition of 1 mL of B. cinerea spores (103/mL) to the soil next to the stem-root junction.
Leaves of growth-chamber-grown plants were soaked in tap water containing two drops of commercial detergent (3 min), rinsed under tap water, and dipped for 30 s in 70% (v/v) ethanol. After a 3-min sterilization in 50% (v/v) bleach, the leaves were rinsed for 5 x 30 s in sterile water, then 1 cm2 pieces were hand cut and incubated on regeneration medium (Murashige and Skoog solid medium supplemented with 0.2 mg/L of 3-indol-acetic acid and 2.2 mg/L of 6-benzylaminopurin) containing different concentrations of sclareol (0, 75, 100, 150, and 200 µM). Adventitious bud regeneration was then observed for 3 to 4 weeks, with renewal of the medium each week.
Protoplasts were isolated as described previously (Lukaszewicz et al., 1998
Two hundred milligrams of plant material was ground in 1 mL of homogenization buffer (250 mM sorbitol, 50 mM Tris-HCl, pH 8.0, 2 mM EDTA, 7g/L of polyvinylpyrrolidone, 5 mM dithiothreitol, 1 mM phenylmethylsulfonyl fluoride, and 2 µg/mL each of leupeptin, pepstatin, aprotinin, antipain, and chymostatin) in a glass tissue grinder (Kontes) in ice. The homogenate was centrifuged for 5 min at 10,000g at 4°C and the supernatant centrifuged again under the same conditions, then the resulting supernatant was centrifuged for 1 h at 22,000g at 4°C, and the final pellet suspended in 30 µL of 5 mM KH2PO4, pH 7.8, 330 mM Suc, 3 mM KCl, and 2 µg/mL each of leupeptin, pepstatin, aprotinin, antipain, and chymostatin.
Rabbit polyclonal antibodies were raised against a peptide corresponding to Ala-212-Arg-335 of NpPDR1 using a previously described method (Jasinski et al., 2001
For immunoblotting, 5 µg of each protein sample solubilized for 15 min at 37°C in an SDS cocktail (2% [w/v] SDS, 10% [w/v] glycerol, 1% [w/v] dithiothreitol, 0.005% [w/v] bromophenol blue, and 80 mM Tris-HCl, pH 6.8, containing the protease inhibitors mentioned above) was subjected to SDS-PAGE (7% polyacrylamide) and transferred electrophoretically to a polyvinylidene difluoride membrane (Millipore), which was then blocked with 3% (w/v) nonfat milk powder in 20 mM Tris-HCl, pH 7.6, 137 mM NaCl, and 0.5% (w/v) Tween 80. The membrane was then incubated for 1 h at 20°C with a 1:500 dilution of one of two rabbit anti-NpPDR1 antisera raised, respectively, against a C-terminal peptide (Jasinski et al., 2001
The leaf abaxial epidermis was pealed off and fixed for 20 min on ice in 100 mM sodium phosphate (SP), pH 7.2 (SP buffer), containing 4% (w/v) paraformaldehyde. After two washes in SP buffer containing 0.2% (v/v) Nonidet and one wash in SP buffer, the cell walls were digested by incubation for 30 min at 20°C in 5 mM CaCl2, 500 mM Suc, 0.6% (w/v) cellulase, 0.2% (w/v) macerozyme (Yakult Pharmaceuticals), and 0.1% (w/v) bovine serum albumin, pH 5.2. The tissue was then blocked for 1 h in blocking buffer (phosphate-buffered saline [136 mM NaCl, 2.7 mM KCl, 10 mM NaHPO4, 1.76 mM KH2PO4, pH 7.4] containing 0.4% [w/v] nonfat milk, 0.04% [w/v] Tween 80), then incubated for 1 h at 20°C in blocking buffer containing antibodies against NpPDR1 (1:150 dilution) or H+-ATPase (1:80 dilution). After four washes in blocking buffer, the samples were incubated for 1 h at 37°C with fluorescein isothiocyanate-coupled goat anti-rabbit IgG antibodies (Molecular Probes), washed 4 x 10 min in blocking buffer and once in phosphate-buffered saline, and examined using a Leica DMR fluorescence microscope.
GUS activity in the leaf epidermis of N. tabacum plants was measured as described previously (Moriau et al., 1999
Twenty micrograms of total RNA was reverse transcribed using dT-18 and M-MLV reverse transcriptase (Promega), following the manufacturer's instructions. Using 1 µL of different dilutions (1:10, 1:50, and 1:100) of the sample, a 294-bp fragment of NpPDR1 cDNA, and, as a control, a 650-bp fragment of the atp2-1 cDNA (Boutry and Chua, 1985
We thank A.M. Faber and P. Gosselin (Université catholique de Louvain) for their excellent technical assistance and C. Decock (Belgian Coordinated Collections of Microorganisms) for the B. cinerea identification. Received March 18, 2005; returned for revision April 22, 2005; accepted July 13, 2005.
1 This work was supported by grants from the Belgian National Fund for Scientific Research, the Interuniversity Attraction Poles Program-Belgian Science Policy, and the European Community (IHP-RTN). Y.S. was a recipient of a fellowship from the Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture, and A.B. is funded by the Ministère de la Région Wallonne.  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.062372. * Corresponding author; e-mail boutry{at}fysa.ucl.ac.be; fax (32)–10–47–38–72.
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