Evaluation of Glucose Dehydrogenase and Pyrroloquinoline Quinine (pqq) Mutagenesis that Renders Functional Inadequacies in Host Plants

Muhammad  Naveed; Younas  Sohail; Nauman  Khalid; Iftikhar  Ahmed; Abdul Samad  Mumtaz

doi:10.4014/jmb.1501.01075

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Research article

Environmental Microbiology and Engineering

Evaluation of Glucose Dehydrogenase and Pyrroloquinoline Quinine (pqq) Mutagenesis that Renders Functional Inadequacies in Host Plants

Muhammad Naveed ¹, Younas Sohail ¹, Nauman Khalid ^2*, Iftikhar Ahmed ³ and Abdul Samad Mumtaz ¹

¹Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan, ²Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan, ³National Institute for Genomics and Advanced Biotechnology (NIGAB), National Agricultural Research Centre (NARC), Islamabad 45500, Pakistan

Received: January 26, 2015; Accepted: April 1, 2015

J. Microbiol. Biotechnol. 2015; 25(8): 1349-1360

Published August 28, 2015 https://doi.org/10.4014/jmb.1501.01075

Abstract

The rhizospheric zone abutting plant roots usually clutches a wealth of microbes. In the recent past, enormous genetic resources have been excavated with potential applications in host plant interaction and ancillary aspects. Two Pseudomonas strains were isolated and identified through 16S rRNA and rpoD sequence analyses as P. fluorescens QAU67 and P. putida QAU90. Initial biochemical characterization and their root-colonizing traits indicated their potential role in plant growth promotion. Such aerobic systems, involved in gluconic acid production and phosphate solubilization, essentially require the pyrroloquinoline quinine (PQQ)- dependent glucose dehydrogenase (GDH) in the genome. The PCR screening and amplification of GDH and PQQ and subsequent induction of mutagenesis characterized their possible role as antioxidants as well as in growth promotion, as probed in vitro in lettuce and in vivo in rice, bean, and tomato plants. The results showed significant differences (p ≤ 0.05) in parameters of plant height, fresh weight, and dry weight, etc., deciphering a clear and in fact complementary role of GDH and PQQ in plant growth promotion. Our study not only provides direct evidence of the in vivo role of GDH and PQQ in host plants but also reveals their functional inadequacy in the event of mutation at either of these loci.

Keywords

Glucose dehydrogenase, pyrroloquinoline quinine, rhizosphere, Pseudomonas, mutagenesis, phosphate solubilization

References

Ahmed I, Sin Y, Paek J, Ehsan M, Hayat R, Iqbal M, Chang YH. 2014. Description of Lysinibacillus pakistanensis. Int. J. Agric. Biol. 16: 447-450.
Ahmed I, Yokota A, Fujiwara T. 2007. A novel highly boron tolerant bacterium, Bacillus boroniphilus sp. nov., isolated from soil, that requires boron for its growth. Extremophile 11: 217-224.
Anthony C, Ghosh M. 1998. The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog. Biophys. Mol. Biol. 69: 1-21.
Bloemberg GV, Lugtenberg BJJ. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4: 343-350.
Choi O, Kim J, Kim JG, Jeong Y, Moon JS, Park CS, Hwang I. 2008. Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol. 146: 657-668.
Chuanwu X, Lambrecht M, Vanderleyden J, Michiels J. 1999. Bi-functional gfp- and gusA-containing mini-Tn5 transposon derivatives for combined gene expression and bacterial localization studies. J. Microbiol. Methods 35: 85-92.
Chung YC, Chen SJ, Hsu CK, Chang CT, Chou ST. 2005. Studies on the antioxidative activity of Graptopetalum paraguayense. Food Chem. 91: 419-424.
Cleton-Jansen AM, Goosen N, Wenzel TJ, van de Putte P. 1988. Cloning of the gene encoding quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus: evidence for the presence of a second enzyme. J. Bacteriol. 170: 2121-2125.
Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61: 1308-1321.
Diggle SP, Griffin AS, Campbell GS, West SA. 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450: 411-414.
Duine JA. 1991. Quinoproteins: enzymes containing the quinonoid cofactor pyrroloquinoline quinone, topaquinone or tryptophan-tryptophan quinone. Eur. J. Biochem. 200: 271-284.
Duine JA, Frank J, van Zeeland J. 1979. Glucose dehydrogenase from Acinetobacter calcoaceticus: a quinoprotein. FEBS Lett. 15.
Duine JA, Jongejan JA. 1989. Quinoproteins, enzymes with pyrroloquinoline quinone as cofactor. Annu. Rev. Biochem. 58: 403-426
Frapolli M, Defago G, Moenne-Loccoz Y. 2007. Multilocus sequence analysis of biocontrol fluorescent Pseudomonas spp. producing the antifungal compound 2,4-diacetylphloroglucinol. Environ. Microbiol. 9: 1939-1955.
Goldstein A, Lester T, Brown J. 2003. Research on the metabolic engineering of the direct oxidation pathway for extraction of phosphate from ore has generated preliminary evidence for PQQ biosynthesis in Escherichia coli as well as a possible role for the highly conserved region of quinoprotein dehydrogenases. Biochim. Biophys. Acta 1647: 266-271.
Gyamfi MA, Yonamine M, Aniya Y. 1999. Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. Gen. Pharmacol. 32: 661-667.
Hayat R, Ali S, Amara U, Khalid R, Ahmed I. 2010. Soil beneficial bacteria and their role in plant growth promotion. Ann. Microbiol. 60: 579-598.
Herman MAB, Nault BA, Smart CD. 2008. Effects of plant growth-promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York. Crop Protect. 27: 996-1002.
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: 303-308.
Kloepper JW, Ryu C-M, Zhang S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94: 1259-1266.
Kumazawa T, Sato K, Seno H, Ishii A, Suzuki O. 1995. Levels of pyrroloquinoline quinone in various foods. J. Biochem. 307: 331-333.
Latif S, Khan SU, Naveed M, Mustafa G, Bashir T, Mumtaz AS. 2013. The diversity of Rhizobia, Sinorhizobia and novel non-Rhizobial Paenibacillus nodulating wild herbaceous legumes. Arch. Microbiol. 195: 647-653.
Matsushita K, Ohno Y, Shinagawa E, Adachi O, Ameyama M. 1980. Membrane-bound D-glucose dehydrogenase from Pseudomonas sp. solubilization, purification and characterization. Agric. Biol. Chem. 44: 1505-1512.
Matsushita K, Shinagawa E, Inoue T, Adachi O, Ameyama M. 1986. Immunological evidence for 2 types of PQQ-dependent D-glucose dehydrogenase in bacterial membranes and the location of the enzyme in Escherichia coli. FEMS Microbiol. Lett. 37: 141-144.
McIntire WS. 1998. Newly discovered redox cofactors:possible nutritional, medical, and pharmacological relevance to higher animals. Annu. Rev. Nutr. 18: 145-177.
Meyer JB, Frapolli M, Keel C, Maurhofer M. 2011. Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads. Appl. Environ. Microbiol. 77: 7345-7354
Midgley M, Dawes EA. 1973. The regulation of glucose and methyl glucose uptake in Pseudomonas aeruginosa. Biochem. J. 132: 141-154.
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: 26-30.
Naveed M, Ahmed I, Khalid N, Mumtaz AS. 2014. Bioinformatics based structural characterization of glucose dehydrogenase (gdh) gene and growth promoting activity of Leclercia sp. QAU-66. Braz. J. Microbiol. 45: 603-611.
Naveed M, Mubeen S, Ahmed I, Khalid N, Suleria HAR, Bano A, Mumtaz AS. 2014. Identification and characterization of rhizospheric microbial diversity by 16S ribosomal RNA gene sequencing. Braz. J. Microbiol. 45: 985-993.
Pikovskaya RI. 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiologiya 17: 362-370.
Rodríguez H, Gonzalez T, Selman G. 2000. Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J. Biotechnol. 84: 155-161.
Sashidhar B, Podile AR. 2009. Transgenic expression of glucose dehydrogenase in Azotobacter vinelandii enhances mineral phosphate solubilization and growth of sorghum seedlings. Microbiol. Biotechnol. 2: 521-529.
Schäfer M, Schmitz C, Facius R, Horneck G, Milow B, Funken KH, Ortner J. 2000. Systematic study of parameters influencing the action of rose bengal with visible light on bacterial cells: comparison between the biological effect and singlet-oxygen production. Photochem. Photobiol. 71: 514-523.
Shanks OC, Santo Domingo JW, Lamendella R, Kelty CA, Graham JE. 2006. Competitive metagenomic DNA hybridization identifies host-specific microbial genetic markers in cow fecal samples. Appl. Environ. Microbiol. 72: 4054-4060.
Xiong LB, Sekity J, Shimose N. 1988. Stimulation of Lillium pollen germination by pyrroloquinoline quinine. Agric. Biol. Chem. 52: 1065-1066.
Xiong LB, Sekity J, Shimose N. 1990. Occurrence of pyrroloquinoline quinone (PQQ) pistils and pollen grains of higher plants. Agric. Biol. Chem. 54: 249-250.
Yamada M, Sumi K, Matsushita K, Adachi O, Yamada Y. 1993. Topological analysis of quinoprotein glucose dehydrogenase in Escherichia coli and its ubiquinone-binding site. J. Biol. Chem. 268: 12812-12817.

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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(8): 1349-1360

Published online August 28, 2015 https://doi.org/10.4014/jmb.1501.01075

Evaluation of Glucose Dehydrogenase and Pyrroloquinoline Quinine (pqq) Mutagenesis that Renders Functional Inadequacies in Host Plants

Muhammad Naveed ¹, Younas Sohail ¹, Nauman Khalid ^2*, Iftikhar Ahmed ³ and Abdul Samad Mumtaz ¹

¹Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan, ²Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan, ³National Institute for Genomics and Advanced Biotechnology (NIGAB), National Agricultural Research Centre (NARC), Islamabad 45500, Pakistan

Received: January 26, 2015; Accepted: April 1, 2015

Abstract

The rhizospheric zone abutting plant roots usually clutches a wealth of microbes. In the recent
past, enormous genetic resources have been excavated with potential applications in host
plant interaction and ancillary aspects. Two Pseudomonas strains were isolated and identified
through 16S rRNA and rpoD sequence analyses as P. fluorescens QAU67 and P. putida QAU90.
Initial biochemical characterization and their root-colonizing traits indicated their potential
role in plant growth promotion. Such aerobic systems, involved in gluconic acid production
and phosphate solubilization, essentially require the pyrroloquinoline quinine (PQQ)-
dependent glucose dehydrogenase (GDH) in the genome. The PCR screening and
amplification of GDH and PQQ and subsequent induction of mutagenesis characterized their
possible role as antioxidants as well as in growth promotion, as probed in vitro in lettuce and
in vivo in rice, bean, and tomato plants. The results showed significant differences (p ≤ 0.05) in
parameters of plant height, fresh weight, and dry weight, etc., deciphering a clear and in fact
complementary role of GDH and PQQ in plant growth promotion. Our study not only
provides direct evidence of the in vivo role of GDH and PQQ in host plants but also reveals
their functional inadequacy in the event of mutation at either of these loci.

Keywords: Glucose dehydrogenase, pyrroloquinoline quinine, rhizosphere, Pseudomonas, mutagenesis, phosphate solubilization

Abstract

References

Ahmed I, Sin Y, Paek J, Ehsan M, Hayat R, Iqbal M, Chang YH. 2014. Description of Lysinibacillus pakistanensis. Int. J. Agric. Biol. 16: 447-450.
Ahmed I, Yokota A, Fujiwara T. 2007. A novel highly boron tolerant bacterium, Bacillus boroniphilus sp. nov., isolated from soil, that requires boron for its growth. Extremophile 11: 217-224.
Anthony C, Ghosh M. 1998. The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog. Biophys. Mol. Biol. 69: 1-21.
Bloemberg GV, Lugtenberg BJJ. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4: 343-350.
Choi O, Kim J, Kim JG, Jeong Y, Moon JS, Park CS, Hwang I. 2008. Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol. 146: 657-668.
Chuanwu X, Lambrecht M, Vanderleyden J, Michiels J. 1999. Bi-functional gfp- and gusA-containing mini-Tn5 transposon derivatives for combined gene expression and bacterial localization studies. J. Microbiol. Methods 35: 85-92.
Chung YC, Chen SJ, Hsu CK, Chang CT, Chou ST. 2005. Studies on the antioxidative activity of Graptopetalum paraguayense. Food Chem. 91: 419-424.
Cleton-Jansen AM, Goosen N, Wenzel TJ, van de Putte P. 1988. Cloning of the gene encoding quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus: evidence for the presence of a second enzyme. J. Bacteriol. 170: 2121-2125.
Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK. 2006. The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol. Microbiol. 61: 1308-1321.
Diggle SP, Griffin AS, Campbell GS, West SA. 2007. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450: 411-414.
Duine JA. 1991. Quinoproteins: enzymes containing the quinonoid cofactor pyrroloquinoline quinone, topaquinone or tryptophan-tryptophan quinone. Eur. J. Biochem. 200: 271-284.
Duine JA, Frank J, van Zeeland J. 1979. Glucose dehydrogenase from Acinetobacter calcoaceticus: a quinoprotein. FEBS Lett. 15.
Duine JA, Jongejan JA. 1989. Quinoproteins, enzymes with pyrroloquinoline quinone as cofactor. Annu. Rev. Biochem. 58: 403-426
Frapolli M, Defago G, Moenne-Loccoz Y. 2007. Multilocus sequence analysis of biocontrol fluorescent Pseudomonas spp. producing the antifungal compound 2,4-diacetylphloroglucinol. Environ. Microbiol. 9: 1939-1955.
Goldstein A, Lester T, Brown J. 2003. Research on the metabolic engineering of the direct oxidation pathway for extraction of phosphate from ore has generated preliminary evidence for PQQ biosynthesis in Escherichia coli as well as a possible role for the highly conserved region of quinoprotein dehydrogenases. Biochim. Biophys. Acta 1647: 266-271.
Gyamfi MA, Yonamine M, Aniya Y. 1999. Free-radical scavenging action of medicinal herbs from Ghana: Thonningia sanguinea on experimentally-induced liver injuries. Gen. Pharmacol. 32: 661-667.
Hayat R, Ali S, Amara U, Khalid R, Ahmed I. 2010. Soil beneficial bacteria and their role in plant growth promotion. Ann. Microbiol. 60: 579-598.
Herman MAB, Nault BA, Smart CD. 2008. Effects of plant growth-promoting rhizobacteria on bell pepper production and green peach aphid infestations in New York. Crop Protect. 27: 996-1002.
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: 303-308.
Kloepper JW, Ryu C-M, Zhang S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94: 1259-1266.
Kumazawa T, Sato K, Seno H, Ishii A, Suzuki O. 1995. Levels of pyrroloquinoline quinone in various foods. J. Biochem. 307: 331-333.
Latif S, Khan SU, Naveed M, Mustafa G, Bashir T, Mumtaz AS. 2013. The diversity of Rhizobia, Sinorhizobia and novel non-Rhizobial Paenibacillus nodulating wild herbaceous legumes. Arch. Microbiol. 195: 647-653.
Matsushita K, Ohno Y, Shinagawa E, Adachi O, Ameyama M. 1980. Membrane-bound D-glucose dehydrogenase from Pseudomonas sp. solubilization, purification and characterization. Agric. Biol. Chem. 44: 1505-1512.
Matsushita K, Shinagawa E, Inoue T, Adachi O, Ameyama M. 1986. Immunological evidence for 2 types of PQQ-dependent D-glucose dehydrogenase in bacterial membranes and the location of the enzyme in Escherichia coli. FEMS Microbiol. Lett. 37: 141-144.
McIntire WS. 1998. Newly discovered redox cofactors:possible nutritional, medical, and pharmacological relevance to higher animals. Annu. Rev. Nutr. 18: 145-177.
Meyer JB, Frapolli M, Keel C, Maurhofer M. 2011. Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads. Appl. Environ. Microbiol. 77: 7345-7354
Midgley M, Dawes EA. 1973. The regulation of glucose and methyl glucose uptake in Pseudomonas aeruginosa. Biochem. J. 132: 141-154.
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: 26-30.
Naveed M, Ahmed I, Khalid N, Mumtaz AS. 2014. Bioinformatics based structural characterization of glucose dehydrogenase (gdh) gene and growth promoting activity of Leclercia sp. QAU-66. Braz. J. Microbiol. 45: 603-611.
Naveed M, Mubeen S, Ahmed I, Khalid N, Suleria HAR, Bano A, Mumtaz AS. 2014. Identification and characterization of rhizospheric microbial diversity by 16S ribosomal RNA gene sequencing. Braz. J. Microbiol. 45: 985-993.
Pikovskaya RI. 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Microbiologiya 17: 362-370.
Rodríguez H, Gonzalez T, Selman G. 2000. Expression of a mineral phosphate solubilizing gene from Erwinia herbicola in two rhizobacterial strains. J. Biotechnol. 84: 155-161.
Sashidhar B, Podile AR. 2009. Transgenic expression of glucose dehydrogenase in Azotobacter vinelandii enhances mineral phosphate solubilization and growth of sorghum seedlings. Microbiol. Biotechnol. 2: 521-529.
Schäfer M, Schmitz C, Facius R, Horneck G, Milow B, Funken KH, Ortner J. 2000. Systematic study of parameters influencing the action of rose bengal with visible light on bacterial cells: comparison between the biological effect and singlet-oxygen production. Photochem. Photobiol. 71: 514-523.
Shanks OC, Santo Domingo JW, Lamendella R, Kelty CA, Graham JE. 2006. Competitive metagenomic DNA hybridization identifies host-specific microbial genetic markers in cow fecal samples. Appl. Environ. Microbiol. 72: 4054-4060.
Xiong LB, Sekity J, Shimose N. 1988. Stimulation of Lillium pollen germination by pyrroloquinoline quinine. Agric. Biol. Chem. 52: 1065-1066.
Xiong LB, Sekity J, Shimose N. 1990. Occurrence of pyrroloquinoline quinone (PQQ) pistils and pollen grains of higher plants. Agric. Biol. Chem. 54: 249-250.
Yamada M, Sumi K, Matsushita K, Adachi O, Yamada Y. 1993. Topological analysis of quinoprotein glucose dehydrogenase in Escherichia coli and its ubiquinone-binding site. J. Biol. Chem. 268: 12812-12817.