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Pyrroloquinoline quinone (PQQ): Role in Plant-Microbe Interactions

  • R. Carreño-López
  • J. M. Alatorre-Cruz
  • V. Marín-Cevada
Chapter

Abstract

Pyrroloquinoline quinone (PQQ) is synthesized by only some bacteria, but it has an impact on many organisms, including plant growth-promoting bacteria. This molecule can modify some microbial process such as gene expression, metabolism, among others, which have potential advantageous effects on plants. We describe the conditions and factors that influence the synthesis of PQQ, its functions as an enzymatic cofactor in many reactions, and how it promotes plant growth by phosphate solubilization in soils. We also describe its actions in the synthesis of antimicrobials and its influence on the biocontrol of fungi and bacteria that are pathogenic to plants. PQQ also has a role in the induction of systemic resistance in plants and the molecule may help in the metabolism of other bacteria, promoting a kind of bacterial mutualism. PQQ can also modify gene expression through signal transduction systems and combat stress induced by ultraviolet and gamma radiation, as well as serving as a powerful agent against oxidative stress and perhaps influencing bacterial motility.

Keywords

PGPB Pyrroloquinoline quinone Plant-microbe interactions Biological control 

References

  1. Ahmed N, Shahab S (2010) Involvement of bacterial pyrroloquinoline quinone in plant growth promotion: a novel discovery. World Appl Scienc J 8:57–61Google Scholar
  2. Akagawa M, Minematsu K, Shibata T, Kondo T, Ishii T, Uchida K (2016) Identification of lactate dehydrogenase as a mammalian pyrroloquinoline quinone (PQQ)-binding protein. Sci Rep 6:26723.  https://doi.org/10.1038/srep26723 PubMedPubMedCentralGoogle Scholar
  3. Alquéres S, Meneses C, Rouws L, Rothballer M, Baldani I, Schmid M, Hartmann A (2013) The bacterial superoxide dismutase and glutathione reductase are crucial for endophytic colonization of rice roots by Gluconacetobacter diazotrophicus PAL5. Mol Plant-Microbe Interact 26(8):937–945.  https://doi.org/10.1094/MPMI-12-12-0286-R PubMedGoogle Scholar
  4. Ameyama M, Sidnagawa E, Matsusidta K, Adachi O (1984) Growth stimulation of microorganisms by pyrroloquinoline quinone. Agric Biol Chem 48(11):2909–2911Google Scholar
  5. An R, Moe LA, Nojiri H (2016) Regulation of pyrroloquinoline quinone-dependent glucose dehydrogenase activity in the model rhizosphere-dwelling bacterium Pseudomonas putida KT2440. Appl Environ Microbiol 82(16):4955–4964PubMedPubMedCentralGoogle Scholar
  6. Anthony C, Gosh M (1998) The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog Biophys Mol Biol 69(1):1–21PubMedGoogle Scholar
  7. Anzuay MS, Ciancio MGR, Ludueña LM, Angelini JG, Barros G, Pastor N, Taurian T (2017) Growth promotion of peanut (Arachis hypogaea L.) and maize (Zea mays L.) plants by single and mixed cultures of efficient phosphate solubilizing bacteria that are tolerant to abiotic stress and pesticides. Microbiol Res 199:98–109.  https://doi.org/10.1016/j.micres.2017.03.006 PubMedGoogle Scholar
  8. Arakawa K, Sugino F, Kodama K, Ishii T, Kinashi H (2005) Cyclization mechanism for the synthesis of macrocyclic antibiotic lankacidin in Streptomyces rochei. Chem Biol 12(2):249–256PubMedGoogle Scholar
  9. Asteriani RD, Duine JA (1998) Reconstitution of membrane-integrated quinoprotein glucose dehydrogenase apoenzyme with PQQ and the holoenzyme’s mechanism of action. Biochemistry 37(19):6810–6818.  https://doi.org/10.1021/bi9722610 Google Scholar
  10. Barr I, Latham JA, Iavarone AT, Chantarojsiri T, Hwang JD, Klinman JP (2016) Demonstration that the radical S-adenosylmethionine (SAM) enzyme PqqE catalyzes de novo carbon-carbon cross-linking within a peptide substrate PqqA in the presence of the peptide chaperone PqqD. J Biol Chem 291(17):8877–8884.  https://doi.org/10.1074/jbc.C115.699918 PubMedPubMedCentralGoogle Scholar
  11. Bauerly K, Harris C, Chowanadisai W, Graham J, Havel PJ, Tchaparian E, Satre M, Karliner JS, Rucker RB (2011) Altering pyrroloquinoline quinone nutritional status modulates mitochondrial, lipid, and energy metabolism in rats. PLoS One 6(7):e21779PubMedPubMedCentralGoogle Scholar
  12. Cho YS, Park RD, Kim YW, Hwangbo H, Jung WJ, Shu JS, Koo BS, Krishnan HB, Kim KY (2003) PQQ-dependent organic acid production and effect on common bean growth by Rhizobium tropici CIAT 899. J Microbiol Biotechnol 13(6):955–959Google Scholar
  13. Choi O, Kim J, Kim J-G, Jeong Y, Moon JS, Park CS, Hwang I (2008) Pyrroloquinoline quinone is a plant growth factor produced by Pseudomonas fluorescens B16. Plant Physiol 146:657–668PubMedPubMedCentralGoogle Scholar
  14. De Biase D, Maras B, John RA (1991) A chromophore in glutamate decarboxylase has been wrongly identified as PQQ. FEBS Lett 278(1):120–122PubMedGoogle Scholar
  15. De Jonge R, De Mattos TMJ, Stock JB, Neijssel OM (1996) Pyrroloquinoline quinone, a chemotactic attractant for Escherichia coli. J Bacteriol 178(4):1224–1226PubMedPubMedCentralGoogle Scholar
  16. Duine JA (1999) The PQQ history. J Biosci Bioeng 88(3):231–236PubMedGoogle Scholar
  17. Evans RL III, Latham JA, Klinman JP, Wilmot CM Xia Y (2016) 1H, 13C, and 15N resonance assignments and secondary structure information for Methylobacterium extorquens PqqD and the complex of PqqD with PqqA. Biomol NMR Assign 10(2):385–389.  https://doi.org/10.1007/s12104-016-9705-8 PubMedPubMedCentralGoogle Scholar
  18. Farhat MB, Fourati A, Chouayekh H (2013) Coexpression of the pyrroloquinoline quinone and glucose dehydrogenase genes from Serratia marcescens CTM 50650 conferred high mineral phosphate-solubilizing ability to Escherichia coli. Appl Biochem Biotechnol 170:1738–1750PubMedGoogle Scholar
  19. Ge X, Wang W, Du B, Wang J, Xiong X, Zhang W (2013) Multiple pqqA genes respond differently to environment and one contributes dominantly to pyrroloquinoline quinone synthesis. J Basic Microbiol 55:312–323PubMedGoogle Scholar
  20. Gliese N, Khodaverdi V, Görisch H (2010) The PQQ biosynthetic operons and their transcriptional regulation in Pseudomonas aeruginosa. Arch Microbiol 192(1):1–14.  https://doi.org/10.1007/s00203-009-0523-6 PubMedGoogle Scholar
  21. Goldstein AH, Braverman K, Osorio N (1999) Evidence for mutualism between a plant growing in a phosphatelimited desert environment and a mineral phosphate solubilizing (MPS) rhizobacterium. FEMS Microbiol Ecol 30(4):295–300PubMedGoogle Scholar
  22. Groen BW, Van Kleef MAG, Duine JA (1986) Quinohaemoprotein alcohol dehydrogenase apoenzyme from Pseudomonas testosteroni. Biochem J 234:611–615PubMedPubMedCentralGoogle Scholar
  23. Guo YB, Li J, Li L, Chen F, Wu W, Wang J, Wang H (2009) Mutations that disrupt either the pqq or the gdh gene of Rahnella aquatilis abolish the production of an antibacterial substance and result in reduced biological control of grapevine crown gall. Appl Environ Microbiol 75(21):6792–6803.  https://doi.org/10.1128/AEM.00902-09 PubMedPubMedCentralGoogle Scholar
  24. He K, Nukada H, Urakami T, Murphy MP (2003) Antioxidant and pro-oxidant properties of pyrroloquinoline quinone (PQQ): implications for its function in biological systems. Biochem Pharmacol 65(1):67–74PubMedGoogle Scholar
  25. Hommes RWJ, Postma PW, Neijssel OM, Tempest DW, Dokter P, Duine JA (1984) Evidence of a quinoprotein glucose dehydrogenase apoenzyme in several strains of Escherichia coli. FEMS Microbiol Lett 24:329–333Google Scholar
  26. Ikemoto K, Sakamoto H, Nakano M (2012) Crystal structure and characterization of pyrroloquinoline quinone disodium trihydrate. Chem Cent J 6(57).  https://doi.org/10.1186/1752-153X-6-57.
  27. Kang Y, Shen M, Wang H, Zhao Q (2013) A possible mechanism of action of plant growth-promoting rhizobacteria (PGPR) strain Bacillus pumilus WP8 via regulation of soil bacterial community structure. J Gen Appl Microbiol 59(4):267–277PubMedGoogle Scholar
  28. Kerr B, Riley MA, Feldman MW, Bohannan BJM (2002) Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418:171–174PubMedGoogle Scholar
  29. Khairnar NP, Misra HS, Apte SK (2003) Pyrroloquinoline-quinone synthesized in Escherichia coli by pyrroloquinoline-quinone synthase of Deinococcus radiodurans plays a role beyond mineral phosphate solubilization. Biochem Biophys Res Commun 312(2):303–308PubMedGoogle Scholar
  30. Khairnar NP, Kamble VA, Mangoli SH, Apte SK, Misra HS (2007) Involvement of a periplasmic protein kinase in DNA strand break repair and homologous recombination in Escherichia coli. Mol Microbiol 65:294–304PubMedGoogle Scholar
  31. Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi–current perspective. Arch Agron Soil Sci 56:73–98Google Scholar
  32. Kim YC, Kim HJ, Park KH, Cho JY, Kim KY, Cho BH (2003) 3-Methylthiopropanoic acid produced by Enterobacter intermedium 60-2G inhibits fungal growth and weed seedling development. J Antibiot 56:177–180PubMedGoogle Scholar
  33. Kim KY, Diann J, Hari BK (1997) Rahnella aquatilis, a bacterium isolated from soybean rhizosphere, can solubilize hydroxyapatite. FEMS Microbiol Lett 53(2):273–277Google Scholar
  34. Kirkup BC, Riley MA (2004) Antibiotic-mediated antagonism leads to a bacterial game of rock–paper–scissors in vivo. Nature 428:412–414PubMedGoogle Scholar
  35. Klinman JP, Bonnot F (2014) The intrigues and intricacies of the biosynthetic pathways for enzymatic quinocofactors: PQQ, TTQ, CTQ, TPQ and LTQ. Chem Rev 114(8):4343–4365PubMedGoogle Scholar
  36. Knowles PF, Pandeya KB, Rius FX, Spencer CM, Moog RS, McGuirl MA, Dooley DM (1987) The organic cofactor in plasma amine oxidase: evidence for pyrroloquinoline quinone and against pyridoxal phosphate. Biochem J 241(2):603–608PubMedPubMedCentralGoogle Scholar
  37. Kremmydas GF, Tampakaki AP, Georgakopoulos DG (2013) Characterization of the biocontrol activity of Pseudomonas fluorescens strain X reveals novel genes regulated by glucose. PLoS One 8(4):e61808.  https://doi.org/10.1371/journal.pone.0061808 PubMedPubMedCentralGoogle Scholar
  38. Kumazawa T, Sato K, Seno H, Ishii A, Suzuki O (1995) Levels of pyrroloquinoline quinone in various foods. Biochem J 307:331–333PubMedPubMedCentralGoogle Scholar
  39. Kumazawa T, Seno H, Urakami T, Matsumoto T, Suzuki O (1992) Trace levels of pyrroloquinoline quinone in human and rat samples detected by gas chromatography/mass spectrometry. Biochim Biophys Acta 1156:62–66PubMedGoogle Scholar
  40. Li L, Jiao Z, Hale L, Wu W, Guo Y (2014) Disruption of gene pqqA or pqqB reduces plant growth promotion actitvity and biocontrol of crown gall disease by Rahnella aquatilis HX2. PLoS One 9(12):e115010.  https://doi.org/10.1371/journal.pone.0115010 PubMedPubMedCentralGoogle Scholar
  41. Magnusson OT, Toyama H, Saeki M, Rojas A, Reed JC, Liddington JC, Klinman JP, Schwarzenbacher R (2004) Quinone biogenesis: structure and mechanism of PqqC, the final catalyst in the production of pyrroloquinoline quinone. PNAS 101(21):7913–7918PubMedGoogle Scholar
  42. Matsumura H, Umezawa K, Takeda K, Sugimoto N, Ishida T, Samejima M, Ohno H, Yoshida M, Igarashi K, Nakamura N (2014) Discovery of a eukaryotic pyrroloquinoline quinone-dependent oxidoreductase belonging to a new auxiliary activity family in the database of carbohydrate-active enzymes. PLoS One 9(8):e104851PubMedPubMedCentralGoogle Scholar
  43. Matsushita K, Arents JC, Bader R, Yamada M, Adachi O, Postma PW (1997) Escherichia coli is unable to produce pyrroloquinoline quinone (PQQ). Micro 143:3149–3156Google Scholar
  44. Matsushita K, Toyama H, Yamada M, Adachi O (2002) Quinoproteins: structure, function and biotechnological applications. Appl Microbiol Biotechnol 50:13–22Google Scholar
  45. Meyer JB, Frapolli M, Keel C, Maurhofer M (2011) Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the philogeny and diversity of phosphate-solubilizing Pseudomonas. Appl Environ Microbiol 77(20):7345–7354PubMedPubMedCentralGoogle Scholar
  46. Mhlongo MI, Piater LA, Madala NE, Labuschagne N, Dubery IA (2018) The chemistry of plant-microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci 9(112).  https://doi.org/10.3389/fpls.2018.00112
  47. Mills MM, Moore CM, Langlois R, Milne A, Achterberg E, Nachtigall K, Lochte K, Geider RJ, La Roche J (2008) Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol Oceanogr 53(2):824–834Google Scholar
  48. Misra HS, Rajpurohit YS, Khairnar NP (2012) Pyrroloquinoline-quinone and its versatile roles in biological processes. J Biosci 37:313–325PubMedGoogle Scholar
  49. Misra HS, Khairnar NP, Barik A, Indira Priyadarsini K, Mohan H, Apte SK (2004) Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Lett 578(1–2):26–30PubMedGoogle Scholar
  50. Miyasaki T, Sugisawa T, Hoshino T (2006) Pyrroloquinoline quinone-dependent dehydrogenases from Ketogulonicigenium vulgare catalyze the direct conversion of L-sorbosone to L-ascorbic acid. Appl Environ Microbiol 72(2):1487–1495Google Scholar
  51. Naveed M, Sohail Y, Khalid N, Ahmed I, Mumtaz AS (2015) Evaluation of glucose dehydrogenase and pyrroloquinoline quinine (pqq) mutagenesis that renders functional inadequacies in host plants. J Microbiol Biotechnol 25(8):1349–1360.  https://doi.org/10.4014/jmb.1501.01075 PubMedGoogle Scholar
  52. Noji N, Nakamura T, Kitahata N, Taguchi K, Kudo T, Yoshida S, Tsujimoto M, Sugiyama T, Asami T (2007) Simple and sensitive method for pyrroloquinoline quinone (PQQ) analysis in various foods using liquid chromatography/electrospray-ionization tandem mass spectrometry. J Agric Food Chem 55:7258–7263PubMedGoogle Scholar
  53. Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilization endophytic Pseudomonas isolates. Front Microbiol 6:745.  https://doi.org/10.3389/fmicb.2015.00745 PubMedPubMedCentralGoogle Scholar
  54. Ouchi A, Nakano M, Nagaoka S, Mukai K (2009) Kinetic study of the antioxidant activity of pyrroloquinoline quinol (PQQH(2), a reduced form of pyrroloquinoline quinone) in micellar solution. J Agric Food Chem 57(2):450–456.  https://doi.org/10.1021/jf802197d PubMedGoogle Scholar
  55. Patel AH, Chovatia V, Shah S (2015) Expression of pyrroloquinoline quinone in Rhizobium leguminosarum for phosphate solubilization. Environ Ecol 33(2):621–624Google Scholar
  56. Paul ND, Moore JP, McPherson M, Lambourne C, Croft P, Heaton JC, Wargent JJ (2012) Ecological responses to UV radiation: interactions between the biological effects of UV on plants and on associated organisms. Physiol Plant 145(4):565–581.  https://doi.org/10.1111/j.1399-3054.2011.01553.x PubMedGoogle Scholar
  57. Paz A, Flückiger R, Gallop PM (1990) Comment: redox-cycling is a property of PQQ but not of ascorbate. FEBS Lett 264(2):283–284PubMedGoogle Scholar
  58. Puehringer S, Metlitzky M, Schwarzenbacher R (2008) The pyrroloquinoline quinone biosynthesis pathway revisited: a structural approach. BMC Biochem 9:8PubMedPubMedCentralGoogle Scholar
  59. Rahman M, Sabir AA, Mukta JA, Khan MMA, Mohi-Ud-Din M, Miah MG, Rahman M, Islam MT (2018) Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Sci Rep 8(1):2504.  https://doi.org/10.1038/s41598-018-20235-1 PubMedPubMedCentralGoogle Scholar
  60. Rajpurohit YS, Desai SS, Misra HS (2013) Pyrroloquinoline quinone and a quinoprotein kinase support γ-radiation resistance in Deinococcus radiodurans and regulate gene expression. J Basic Microbiol 53(6):518–531.  https://doi.org/10.1002/jobm.201100650 PubMedGoogle Scholar
  61. Rodríguez H, Fraga R, González T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21Google Scholar
  62. Rodríguez H, González T, Selman G (2000) Expresion of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J Biotechnol 84:155–161Google Scholar
  63. Rucker R, Chowanadisai W, Nakano M (2009) Potential physiological importance of pyrroloquinoline quinone. Altern Med 14(3):268–277Google Scholar
  64. Salisbury SA, Forrest HS, Cruse WB, Kennard O (1979) A novel coenzyme from bacterial primary alcohol dehydrogenases. Nature 280:843–844PubMedGoogle Scholar
  65. Sánchez-Contreras M, Martin M, Villacieros M, O’Gara F, Bonilla I, Rivilla R (2002) Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 184(6):1587–1596.  https://doi.org/10.1128/JB.184.6.1587-1596.2002 PubMedPubMedCentralGoogle Scholar
  66. Scharf BE, Hynes MF, Alexandre GM (2016) Chemotaxis signaling systems in model beneficial plant-bacteria associations. Plant Mol Biol 90(6):549–559.  https://doi.org/10.1007/s11103-016-0432-4 PubMedGoogle Scholar
  67. Schnider U, Keel C, Voisard C, Défago G, Haas D (1995) Tn5-directed cloning of pqq genes from Pseudomonas fluorescens CHA0: mutational inactivation of the genes results in overproduction of the antibiotic pyoluteorin. Appl Environ Microbiol 61(11):3856–3864PubMedPubMedCentralGoogle Scholar
  68. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphtae solubilizing microbes: sustainable approach for managing phosphorus deficiency agricultural soils. Springer Plus 2:587PubMedGoogle Scholar
  69. Shen YQ, Bonnot F, Imsand EM, RoseFigura JM, Sjölander K, Klinman JP (2012) Distribution and properties of the genes encoding the biosynthesis of bacterial cofactor, pyrroloquinoline quinone. Biochemistry 51(11):2265–2275PubMedPubMedCentralGoogle Scholar
  70. Shimao M, Yamamoto H, Ninomiya K, Kato N, Adachi O, Ameyama M, Sakazawa C (1984) Pyrroloquinoline quinone as an essential growth factor for a polyvinyl alcohol-degrading symbiont, Pseudomonas sp. VM15C. Agric Biol Chem 48(11):2873–2876Google Scholar
  71. Song Hee Han, Chul Hong Kim, Jang Hoon Lee, Ju Yeon Park, Song Mi Cho, Seur Kee Park, Kil Yong Kim, Krishnan HB, Young Cheol Kim (2008) Inactivation of genes of 60-2G reduces antifungal activity and induction of systemic resistance. FEMS Microbiol Lett 282(1):140–146PubMedGoogle Scholar
  72. Stella M, Halimi MS (2015) Gluconic acid production by bacteria to liberate phosphorus from insoluble phosphate complexes. J Trop Agric Food Sci 43(1):41–53Google Scholar
  73. Stites TE, Mitchell AE, Rucker RB (1999) Physiological importance of quinoenzymes and the o-quinone family of cofactors. J Nutr 130(4):719–727Google Scholar
  74. Toyama H, Lidstrom ME (1998) pqqA is not required for biosynthesis of pyrroloquinoline quinone in Methylobacterium extorquens AM1. Microbiology 114:183–191Google Scholar
  75. Trcek J, Toyama H, Czuba J, Misiewicz A, Matsushita K (2006) Correlation between acetic acid resistance and characteristics of PQQ-dependent ADH in acetic acid bacteria. Appl Microbiol Biotechnol 70(3):366–373PubMedGoogle Scholar
  76. Trček J, Jernejc K, Matsushita K (2007) The highly tolerant acetic acid bacterium Gluconacetobacter europaeus adapts to the presence of acetic acid by changes in lipid composition, morphological properties and PQQ-dependent ADH expression. Extremophiles 11(4):627–635.  https://doi.org/10.1007/s00792-007-0077-y PubMedGoogle Scholar
  77. Tremblay J, Déziel E (2010) Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 11:587.  https://doi.org/10.1186/1471-2164-11-587 PubMedPubMedCentralGoogle Scholar
  78. Tsai TY, Yang CY, Shih HL, Wang AHJ, Chou SH (2009) Xanthomonas campestris PqqD in the pyrroloquinoline quinone biosynthesis adopts a novel saddle like fold that possibly serves as a PQQ carrier. Proteins 76(4):1042–1048.  https://doi.org/10.1002/prot.22461 PubMedGoogle Scholar
  79. Urakami T, Yashima K, Kobayashi H, Yoshida A, Ito-Yoshida C (1992) Production of pyrroloquinoline quinone by using methanol-utilizing bacteria. Appl Environ Microbiol 58(12):3970–3976PubMedPubMedCentralGoogle Scholar
  80. Van Kleef MAG, Duine JA (1989) Factor relevant in bacterial pyrroloquinoline quinone production. Appl Environ Microbiol 55(5):1209–1213PubMedPubMedCentralGoogle Scholar
  81. Van Schie BJ, Hellingwerf KJ, Van Dikjen JP, Elferink MGL, Van Dijl JM, Kuenen JG, Konings WN (1985) Energy transduction by electron transfer via pyrroloquinoline-quinone-dependent glucose dehydrogenase in Escherichia coli, Pseudomonas aeruginosa and Acinetobacter calcoaceticus (var. lwoffi). J Bacteriol 163(2):493–499PubMedPubMedCentralGoogle Scholar
  82. Van Schie BJ, Van Dijken JP, Kuenen JG (1984) Non-coordinated synthesis of glucose dehydrogenase and its prosthetic group PQQ in Acinetobacter and Pseudomonas species. FEMS Microbiol Lett 24:133–138Google Scholar
  83. Wagh J, Shah S, Bhandhari P, Archana G, Kumar GN (2014) Heterologous expression of pyrroloquinoline quinone (pqq) gene cluster confers mineral phosphate solubilization ability to Herbaspirillum seropedicae Z67. Appl Microbiol Technol 98:5117–5129Google Scholar
  84. Wecksler SR, Stoll S, Iavarone AT, Imsand EM, Tran H, Britt RD, Klinman JP (2010) Interaction of PqqE and PqqD in the pyrroloquinoline quinone (PQQ) biosynthetic pathway links PqqD to the radical SAM superfamily. Chem Commun 46:7031–7033Google Scholar
  85. Wei Q, Ran T, Ma C, He J, Xu D, Wang W (2016) Crystal structure and function of PqqF protein in the pyrroloquinoline quinone biosynthetic pathway. J Biol Chem 291(30):15575–15587.  https://doi.org/10.1074/jbc.M115.711226 PubMedPubMedCentralGoogle Scholar
  86. Xiong XH, Zhao Y, Ge X, Yuan SJ, Wang JH, Zhi JJ, Yang YX, Du BH, Guo WJ, Wang SS, Yang DX, Zhang WC (2011) Production and radioprotective effects of pyrroloquinoline quinone. Int J Mol Sci 12(12):8913–8923PubMedPubMedCentralGoogle Scholar
  87. Xu J, Deng P, Showmaker KC, Wang H, Baird SM, Lu SE (2014) The pqqC gene is essential for antifungal activity of Pseudomonas kilonensis JX22 against Fusarium oxysporum f. sp. lycopersici. FEMS Microbiol Lett 353(2):98–105.  https://doi.org/10.1111/1574-6968.12411 PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • R. Carreño-López
    • 1
  • J. M. Alatorre-Cruz
    • 2
  • V. Marín-Cevada
    • 1
  1. 1.Benemérita Universidad Autónoma de PueblaPueblaMexico
  2. 2.Universidad Autónoma de QuerétaroQuerétaroMexico

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