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First published online November 30, 2007; 10.1104/pp.107.112748 Plant Physiology 146:657-668 (2008) © 2008 American Society of Plant Biologists Pyrroloquinoline Quinone Is a Plant Growth Promotion Factor Produced by Pseudomonas fluorescens B161Department of Agricultural Biotechnology and Center for Agricultural Biomaterials, Seoul National University, Seoul 151–921, Korea (O.C., J.K., J.-G.K., Y.J., I.H.); Division of Plant Resources and Environment, Gyeongsang National University, Jinju 660–701, Korea (O.C., C.S.P.); and Plant Genome Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon 305–333, Korea (J.S.M.)
Pseudomonas fluorescens B16 is a plant growth-promoting rhizobacterium. To determine the factors involved in plant growth promotion by this organism, we mutagenized wild-type strain B16 using  Km elements and isolated one mutant, K818, which is defective in plant growth promotion, in a rockwool culture system. A cosmid clone, pOK40, which complements the mutant K818, was isolated from a genomic library of the parent strain. Tn3-gusA mutagenesis of pOK40 revealed that the genes responsible for plant growth promotion reside in a 13.3-kb BamHI fragment. Analysis of the DNA sequence of the fragment identified 11 putative open reading frames, consisting of seven known and four previously unidentified pyrroloquinoline quinone (PQQ) biosynthetic genes. All of the pqq genes showed expression only in nutrient-limiting conditions in a PqqH-dependent manner. Electrospray ionization-mass spectrometry analysis of culture filtrates confirmed that wild-type B16 produces PQQ, whereas mutants defective in plant growth promotion do not. Application of wild-type B16 on tomato (Solanum lycopersicum) plants cultivated in a hydroponic culture system significantly increased the height, flower number, fruit number, and total fruit weight, whereas none of the strains that did not produce PQQ promoted tomato growth. Furthermore, 5 to 1,000 nM of synthetic PQQ conferred a significant increase in the fresh weight of cucumber (Cucumis sativus) seedlings, confirming that PQQ is a plant growth promotion factor. Treatment of cucumber leaf discs with PQQ and wild-type B16 resulted in the scavenging of reactive oxygen species and hydrogen peroxide, suggesting that PQQ acts as an antioxidant in plants.
Bacteria that colonize plant roots and enhance plant growth by any mechanism are referred to as plant growth-promoting rhizobacteria (PGPR). PGPR have been applied on various crops to enhance growth, seed emergence, crop yield, and disease control, and some have been commercialized (Kloepper, 1992  ; Glick, 1995; Dey et al., 2004). The use of PGPR in sustainable agriculture is steadily increasing and offers an attractive way to replace chemical fertilizers, pesticides, and supplements.
PGPR can promote plant growth indirectly or directly. Indirect plant growth promotion is mediated by antibiotics or siderophores produced by PGPR that decrease or prevent the deleterious effects of plant-pathogenic microorganisms (Leong, 1986
In mammals, pyrroloquinoline quinone (PQQ) functions as a potent growth factor, although its biological functions are not fully understood (Smidt et al., 1991
The biochemical pathways of PQQ biosynthesis are not fully understood, but it is known that Glu and Tyr are precursors (Houck et al., 1991
We have studied the promotion of plant growth by P. fluorescens B16, which was isolated from the roots of graminaceous plants. The wild-type B16 colonizes the roots of various plants and produces an antibacterial compound that is effective against plant root pathogens, such as Agrobacterium tumefaciens and Ralstonia solanacearum (Kang and Park, 1997
Isolation of a Plant Growth Promotion-Defective Mutant
Following random mutagenesis of P. fluorescens B16 with
Identification of Genes Responsible for Plant Growth Promotion
To identify genes that confer plant growth promotion in wild-type B16, the DNA region flanking the
A restriction enzyme map of the 25-kb insert of pOK40 was constructed (Fig. 2). To further characterize the insert, we mutagenized pOK40 and pOK53, which carries a 13.4-kb BamHI fragment from pOK40 in pLAFR3, with Tn3-gusA, followed by marker exchange into wild-type B16. We identified 12 Tn3-gusA insertions that interfere with plant growth promotion, delineating the essential region for this function (Fig. 2). The 13.4-kb BamHI fragment from pOK40 was subcloned into pBluescriptII SK+, resulting in pOK51, for DNA sequencing. The sequence of the fragment contains 11 potential open reading frames (ORFs), which were named pqqA, B, C, D, E, F, H, I, J, K, and M, as the Tn3-gusA insertions in each ORF abolished PQQ production (Fig. 2). pqqA, B, C, D, E, F, and M genes exhibit strong similarity to those of the P. fluorescens strain Pf0-1 (Table II; Fig. 3 ). Proteins PqqH and I of P. fluorescens B16 are highly similar to a LysR-type transcriptional regulator and a class-III aminotransferase present upstream of the pqq gene cluster in P. fluorescens Pf0-1, respectively (Table II). pqqJ is predicted to encode a 13.6-kD protein exhibiting 53% identity and 68% similarity to a putative cytoplasmic protein from Salmonella enterica sp. enterica serovar Choleraesuis str. SC-B67 (Table II). PqqK is predicted to be a protein of 11.6 kD that is similar to a DNA-binding protein of Sinorhizobium meliloti 1021 (Table II).
Expression of pqq Genes in a PqqH-Dependent Manner in Nutrient-Limiting Conditions
To determine how the pqq genes of P. fluorescens B16 are expressed, we analyzed their expression levels using pqq::Tn3-gusA fusion mutants grown in Luria-Bertani (LB) medium or Agrobacterium minimal medium (AB). None of the pqq genes were expressed at high levels in LB medium, but each was expressed more strongly in AB medium (Table III
). This result indicates that pqq genes are expressed only under nutrient-limiting conditions. Because PqqH shows similarity to a transcriptional regulator, we evaluated whether PqqH influences expression of the other pqq genes by constructing Tn3-gusA fusions of each pqq gene in the pqqH::
Promotion of Tomato Plant Growth in a Hydroponic Culture System Because wild-type B16 promoted the growth of tomato plants in a rockwool system, we tested whether it could promote tomato plant growth in a hydroponic culture system. In this system, wild-type B16 increased plant height by 19.8% and flower number by 42%, as measured at 65 d after treatment (Fig. 4 ). In addition, treatment with B16 increased the fruit number and total fruit weight after the final harvest by 41% and 36%, respectively (Fig. 4). As expected, the mutant K818 failed to confer growth promotion and K818 carrying pOK40 did promote growth (Fig. 4). We repeated the growth study of tomato plants in the hydroponic culture system twice over 2 years and observed very similar results; therefore, only 1 year of data is presented in Figure 4. These results indicate that the growth promotion of tomato plants by wild-type B16 can be achieved in a hydroponic culture system.
PQQ Is a Key Element for Plant Growth Promotion Based on the fact that mutations in pqq genes abolished plant growth-promotion activity of wild-type B16, we examined whether the strain produces PQQ by analyzing culture supernatants using reverse-phase (RP)-HPLC. PQQ was detected as 5-acetonyl-PQQ by comparison with the elution times of synthetic PQQ and 5-acetonyl-PQQ from the RP-HPLC chromatograms (Fig. 5B ). Electrospray ionization (ESI)-mass spectrometry (MS) analysis of the peak fraction corresponding to 5-acetonyl-PQQ from B16 culture filtrates and a standard revealed [M-H]– ions at mass-to-charge ratio 387 (Fig. 5C). This result confirmed that wild-type B16 produces PQQ in vitro. None of the mutants defective in plant growth promotion produced PQQ, and pOK53, which carries all of the pqq genes, conferred PQQ production in the mutants (one example is shown in Fig. 5B).
To confirm that PQQ promotes plant growth, synthetic PQQ was applied to germinating seedlings of the cucumber cultivar ‘Eunsungbagdadagi’, because tomato seedlings did not grow well on Murashige and Skoog medium or in sand. Concentrations of synthetic PQQ ranging from 0 to 1,000 nM were used. Significant increases in the fresh weight were observed in cucumber seedlings growing on Murashige and Skoog medium that were treated with PQQ concentrations >100 nM (Fig. 6A ). Cucumber seedlings growing in sand treated with synthetic PQQ showed significantly greater fresh weight than seedlings growing in Murashige and Skoog medium (Fig. 6B). Treatment with 50, 100, or 1,000 nM PQQ increased the fresh weight of cucumber seedlings growing in sand by 18.4%, 17.1%, and 23.9%, respectively (Fig. 6). To determine whether PQQ promotes the growth of various plants, synthetic PQQ was applied to germinating seedlings of Arabidopsis ecotype Columbia and the hot pepper cultivar ‘Bukang’ on Murashige and Skoog medium. The fresh and dry weights of Arabidopsis and the size of the cotyledons of hot pepper treated with 25 nM PQQ were increased (data not shown).
PQQ Scavenges ROS and H2O2 in Cucumber Leaves To determine possible biochemical mechanisms involved in the promotion of plant growth by PQQ, we evaluated the ability of wild-type B16 and PQQ in planta to scavenge ROS and hydrogen peroxide (H2O2) using nitroblue tetrazolium (NBT) and diaminobenzidine (DAB) staining, respectively. Wounded leaf discs of the cucumber cultivar ‘Eunsungbagdadagi’ treated with the PQQ-deficient mutant strain BK433 or water clearly showed higher ROS production than leaf discs from plants treated with wild-type B16 (Fig. 7A ). The deposition of blue formazan, an indication of ROS production in leaf discs, decreased as the PQQ concentration exceeded 100 nM (Fig. 7A). Wounded leaf discs were stained with DAB to locate H2O2, and less H2O2 accumulation was observed in leaf discs treated with wild-type B16 than with the PQQ-deficient mutant BK433 or water (Fig. 7B). Staining was much less intense after treatment with 100 or 1,000 nM synthetic PQQ than after water treatment, suggesting that PQQ effectively scavenged H2O2 in wounded cucumber leaves.
To determine whether PQQ affects the activity of antioxidant enzymes, such as superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase, cucumber leaf extracts treated with synthetic PQQ, wild-type strain B16, or the PQQ-deficient mutant strain BK433 were examined using active staining methods in native PAGE. There were no detectable differences in the SOD, APX, or catalase activities among the treatments (data not shown).
To determine the mineral phosphate solubilization (MPS) activities of wild-type B16 and pqq::Tn3-gusA mutants, we performed MPS assays on Glc minimal medium agar plates containing tricalcium phosphate (TCP). Both wild-type B16 and all pqq::Tn3-gusA mutants showed very low MPS activity, with no significant differences (data not shown).
Plant growth promotion by PGPR has received attention for academic and practical reasons because beneficial interactions between PGPR and plants offer tremendous potential for field applications. To be an effective PGPR, an organism must be able to colonize roots because the organism needs to establish itself in the rhizosphere at population densities sufficient to produce a beneficial effect. Thus, previous failures in plant growth promotion studies in the field have often been correlated with poor root colonization (Bloemberg and Lutenberg, 2001 ). We found that the plant growth promotion-deficient mutant K818 maintained the ability to colonize roots, which suggested that additional factors beyond root colonization are required for plant growth promotion. This result led us to identify a new plant growth promotion factor, PQQ, from P. fluorescens B16.
In this study, we identified four previously unidentified pqq genes. It is unclear how these genes are involved in the biochemical pathways of PQQ biosynthesis. Possible PQQ biosynthesis pathways starting with a Tyr and a Glu residue have been proposed because the small PqqA peptide contains a Glu and a Tyr residue at conserved positions (Houck et al., 1991
The fact that the expression of pqq genes is regulated by PqqH under nutrient-limiting conditions is consistent with other reports that PGPR are often effective under low-nutrient conditions and have little or no measurable effect on plant growth when the plants are grown in nutrient-rich soil under optimal conditions (Penrose and Glick, 2003
Some information on the biochemical functions of PQQ has been reported. It is known that PQQ is a cofactor of aminoadipic 6-semialdehyde-dehydrogenase (U26), which is involved in Lys degradation in mice. Numerous studies have reported that PGPR is able to solubilize inorganic and/or organic phosphates in soil following formation of the GDH-PQQ holoenzyme (Liu et al., 1992
In addition, PQQ acts as an antioxidant in animal cells, preventing cell injury (Smidt et al., 1991
PQQ is at least 100 times more efficient than ascorbic acid, isoflavonoids, and polyphenolic compounds in assays assessing redox cycling potentials (Stites et al., 2000
There have been few studies of the functional roles of PQQ in plants. It is known that PQQ stimulates pollen germination in vitro in the plant species Lilium, Tulipa, and Camellia (Xiong et al., 1988
Bacterial Strains and Growth Conditions Bacterial strains and plasmids used in this study are listed in Table I. Escherichia coli strains were cultured on LB medium at 37°C. Pseudomonas fluorescens strain B16 was routinely cultivated at 28°C on LB medium or AB minimal medium (0.3% K2HPO4, 0.1% NaH2PO4, 0.1% NH4Cl, 0.03% MgSO4·7H2O, 0.015% KCl, 0.01% CaCl2·2H2O, 0.00025% FeSO4·7H2O, pH 7.0) supplemented with 0.2% Glc. Antibiotics were used at the following concentrations: ampicillin, 100 µg mL–1; chloramphenicol, 34 µg mL–1; gentamycin, 50 µg mL–1; kanamycin, 50 µg mL–1; nalidixic acid, 20 µg mL–1; rifampicin, 50 µg mL–1; spectinomycin, 50 µg mL–1; and tetracycline, 50 µg mL–1.
Standard methods were used for DNA cloning, restriction mapping, and gel electrophoresis as described by Sambrook et al. (1989)
The 13.4-kb insert in pOK51, carrying all of the pqq genes, was digested with appropriate restriction enzymes and subcloned into the corresponding sites in pBluescriptII SK+. DNA fragments were sequenced using the BigDye terminator kit (Applied Biosystems) with the universal and reverse primers. Synthetic primers were designed for primer walking when necessary. DNA sequences were assembled and ORFs were identified using the SeqManII subroutine of DNASTAR. All potential ORFs larger than 249-bp were examined for possible ribosome-binding sites and annotated using the BLASTX and BLASTP protocols (Altschul et al., 1990
The GUS enzyme assay (Jefferson et al., 1987
Tomato (Solanum lycopersicum ‘Kwangsoo’) seeds were grown to the four- or five-leaf stage in rockwool plugs. Root systems of the seedlings were immersed for 1 h in bacterial suspensions (108 CFU mL–1) for bacterization and then transplanted into rockwool cubes (10 x 10 x 7 cm) and kept in a greenhouse at 25°C ± 3°C. One-half-strength hydroponic culture solution (COSEAL) was supplied twice per week. Rockwool cubes were arranged in a randomized design. Replicated field trials were conducted over 2 years in the hydroponic culture system (12.6 x 1.9 m). Trials were carried out under natural illumination at 25°C ± 3°C from December, 2002 to April, 2003 for the first year and from September, 2003 to January, 2004 for the second year. Tomato seedlings at the four- or five-leaf stage in rockwool plugs were treated with bacterial suspensions (108 CFU mL–1) and transferred into the hydroponic culture system. The bacterial suspension (108 CFU mL–1) was then applied to the plants seven times at 10-d intervals after transplanting to provide sufficient bacterial cells and to ensure that the size of the bacterial population was not a limiting factor. One-half-strength hydroponic culture solution was supplied five times per day for 2 min. Tomato plants were grown for 5 months. Plant growth promotion was evaluated under two different conditions. In rockwool cubes, the height of the tomato plants was measured 21 d after inoculation. Root samples collected from rockwool cubes at 21 d were macerated in a sterile mortar and pestle. The population density of the bacteria on the roots was determined by dilution plate counting. In the hydroponic culture system, the height, thickness, number of stems, and number of flowers were recorded at 7-d intervals and mature tomato fruits were harvested seven times.
To measure PQQ production, bacteria were grown for 48 h at 28°C in AB minimal medium containing 0.4% gluconic acid. One volume of cell culture was diluted with nine volumes of methanol and the precipitated materials were removed by centrifugation. After evaporation of the methanol, a Sep-Pak C18 cartridge (Waters) was washed with 10 mL of methanol and subsequently with 10 mL of water. The sample was acidified with HCl to pH 2.0 and loaded onto the cartridge. After washing with 10 mL of 2 mM HCl, PQQ was eluted with 70% methanol. To identify the peak of PQQ, 200 µL of the sample were mixed with 100 µL of 0.2 M Na2B4O7 buffer and adjusted to pH 8.0 with HCl and 90 µL of 0.5% (v/v) acetone. RP-HPLC was performed using a Shimadzu LC-6A HPLC system as described previously (Van der Meer et al., 1990
Arabidopsis (Arabidopsis thaliana ecotype Columbia), hot pepper (Capsicum annum ‘Bukang’), and cucumber (Cucumis sativus ‘Eunsungbagdadagi’) seeds were surface sterilized (70% ethanol for 5 min followed by 1% sodium hypochlorite for 15 min), rinsed 10 times with sterile, distilled water, placed on petri dishes containing medium consisting of one-half-strength Murashige and Skoog salts (Sigma), 0.4% agar, and 3% Suc, and allowed to germinate over 2 d at 28°C. Glass bottles (8.5 x 16 cm) were prepared with one-half-strength Murashige and Skoog medium containing 5, 50, 100, or 1,000 nM of synthetic PQQ (Sigma). Two-day-old cucumber seedlings were transferred into the glass bottles. Germinated Arabidopsis and hot pepper seedlings were transferred to the glass bottles with one-half-strength Murashige and Skoog medium containing 25 nM of synthetic PQQ. Water was used as a control. Glass bottles were arranged in a randomized design. Sand was rinsed in distilled water for 3 d and autoclaved twice. Cucumber seeds were surface sterilized and placed in petri dishes containing sterile water to germinate at 28°C. Two-day-old cucumber seedlings were immersed for 1 h in 10 mL of 5, 50, 100, or 1,000 nM synthetic PQQ, transferred into the sand, and the surplus synthetic PQQ solution that remained after treatment was poured into the sand. Water was used as a control. Glass bottles and plants transplanted in sand were placed in a growth chamber set to a 14-h-light/10-h-dark cycle at 24°C ± 1°C with a relative humidity of 60%. Fresh weight of the plants was recorded at 13 d after transplanting.
Cucumbers were grown until the three-leaf stage in rockwool plugs. Root systems of the seedlings were immersed for 1 h in a bacterial suspension (108 CFU mL–1) for bacterization. Eight leaf discs (7 mm in diameter) from the third leaves of cucumber seedlings were used for detection of ROS and H2O2 7 d after inoculation. For PQQ treatment, leaf discs were immersed for 14 h at 25°C in 0, 10, 100, or 1,000 nM synthetic PQQ. All leaf discs were vacuum infiltrated with 1 mg mL–1 NBT in 10 mM potassium phosphate buffer (pH 7.8) or DAB solution and incubated at 25°C under light for 2 h. Leaf discs were rinsed with 80% (v/v) ethanol for 10 min at 70°C, mounted on a glass slide in lactic acid:phenol:water (1:1:1 [v/v/v]), and photographed directly using a microscope (Carl Zeiss).
For determination of antioxidant enzyme activities, cucumber leaves (1 g) were frozen in liquid nitrogen, ground, and resuspended in 150 µL of 50 mM KH2PO4 (pH 7.8). The homogenate was centrifuged at 13,000g for 15 min and protein content of the supernatant was determined (Bradford protein assay; Bio-Rad). Samples of 30 µg of protein from each tissue homogenate were separated in 10% native polyacrylamide gels. SOD activity in the gels was determined using the modified staining method (McCord and Fridovich, 1969
MPS activity of bacteria was checked on Glc minimal medium agar plates containing TCP, as described previously (Krishnaraj and Goldstein, 2001
Experimental data were analyzed statistically using ANOVA (SAS Institute). Significance of the effect of treatment was determined by the magnitude of the F value (P = 0.05). When a significant F test was obtained for the treatments, separation of means was accomplished by Fisher's protected LSD. Sequence data from this article can be found in the GenBank data libraries under accession number AY780887. Received November 6, 2007; accepted November 20, 2007; published November 30, 2007.
1 This work was supported by the Crop Functional Genomics Center of the 21st Century Frontier R&D Program (grant no. CG2131), funded by the Ministry of Science and Technology of the Republic of Korea, and by a Korea Research Foundation Grant, funded by the Korean Government (Ministry of Education and Human Resources Development, Basic Research Promotion Fund; grant no. KRF–2006–005–J04701).  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: Ingyu Hwang (ingyu{at}snu.ac.kr). www.plantphysiol.org/cgi/doi/10.1104/pp.107.112748 * Corresponding author; e-mail ingyu{at}snu.ac.kr.
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, followed by selection on LB agar medium containing kanamycin, to rescue the region flanking the insertion. The flanking region was sequenced with the primer HR (5'-TGCTTCAATCAATCACCGG-3'). pOK40 and pOK53, which carry all of the PQQ biosynthetic genes, were mutagenized with Tn3-gusA as described by Bonas et al. (1989)
