DOI QR코드

DOI QR Code

Secondary Metabolites Production and Plant Growth Promotion by Pseudomonas chlororaphis and P. aurantiaca Strains Isolated from Cactus, Cotton, and Para Grass

  • Shahid, Izzah (Department of Biological Sciences, Forman Christian College (A Chartered University)) ;
  • Rizwan, Muhammad (Applied Chemistry Research Center, Pakistan Council of Scientific and Industrial Research) ;
  • Baig, Deeba Noreen (Department of Biological Sciences, Forman Christian College (A Chartered University)) ;
  • Saleem, Rahman Shahzaib (Department of Chemistry, School of Science and Engineering, Lahore University of Management Sciences) ;
  • Malik, Kauser A. (Department of Biological Sciences, Forman Christian College (A Chartered University)) ;
  • Mehnaz, Samina (Department of Biological Sciences, Forman Christian College (A Chartered University))
  • Received : 2016.01.12
  • Accepted : 2016.12.09
  • Published : 2017.03.28

Abstract

Fluorescent pseudomonads have been isolated from halophytes, mesophytes, and xerophytes of Pakistan. Among these, eight isolates, GS-1, GS-3, GS-4, GS-6, GS-7, FS-2 (cactus), ARS-38 (cotton), and RP-4 (para grass), showed antifungal activity and were selected for detailed study. Based on biochemical tests and 16S rRNA gene sequences, these were identified as strains of P. chlororaphis subsp. chlororaphis and aurantiaca. Secondary metabolites of these strains were analyzed by LC-MS. Phenazine-1-carboxylic acid (PCA), 2-hydroxy-phenazine, Cyclic Lipopeptide (white line-inducing principle (WLIP)), and lahorenoic acid A were detected in variable amounts in these strains. P. aurantiaca PB-St2 was used as a reference as it is known for the production of these compounds. The phzO and PCA genes were amplified to assure that production of these compounds is not an artifact. Indole acetic acid production was confirmed and quantified by HPLC. HCN and siderophore production by all strains was observed by plate assays. These strains did not solubilize phosphate, but five strains were positive for zinc solubilization. Wheat seedlings were inoculated with these strains to observe their effect on plant growth. P. aurantiaca strains PB-St2 and GS-6 and P. chlororaphis RP-4 significantly increased both root and shoot dry weights, as compared with uninoculated plants. However, P. aurantiaca strains FS-2 and ARS-38 significantly increased root and shoot dry weights, respectively. All strains except PB-St2 and ARS-38 significantly increased the root length. This is the first report of the isolation of P. aurantiaca from cotton and cactus, P. chlororaphis from para grass, WLIP and lahorenoic acid A production by P. chlororaphis, and zinc solubilization by P. chlororaphis and P. aurantiaca.

Keywords

References

  1. Hayat R, Ali S, Amara U, Khalid R, Ahmed I. 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann. Microbiol. 60: 579-598. https://doi.org/10.1007/s13213-010-0117-1
  2. Saharan B. 2011. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res.
  3. Welbaum GE, Sturz AV, Dong Z, Nowak J. 2004. Managing soil microorganisms to improve productivity of agroecosystems. Crit. Rev. Plant Sci. 23: 175-193. https://doi.org/10.1080/07352680490433295
  4. Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Barka EA. 2005. Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl. Environ. Microbiol. 71: 1685-1693. https://doi.org/10.1128/AEM.71.4.1685-1693.2005
  5. Gray E, Smith D. 2005. Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol. Biochem. 37: 395-412. https://doi.org/10.1016/j.soilbio.2004.08.030
  6. Bloemberg GV, Lugtenberg BJ. 2001. Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr. Opin. Plant Biol. 4: 343-350. https://doi.org/10.1016/S1369-5266(00)00183-7
  7. Lodewyckx C, Vangronsveld J, Porteous F, Moore ER, Taghavi S, Mezgeay M, van der Lelie D. 2002. Endophytic bacteria and their potential applications. Crit. Rev. Plant Sci. 21: 583-606. https://doi.org/10.1080/0735-260291044377
  8. Mayak S, Tirosh T, Glick BR. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 42: 565-572. https://doi.org/10.1016/j.plaphy.2004.05.009
  9. de Weger LA, van der Bij AJ, Dekkers LC, Simons M, Wijffelman CA, Lugtenberg BJ. 1995. Colonization of the rhizosphere of crop plants by plant-beneficial pseudomonads. FEMS Microbiol. Ecol. 17: 221-227. https://doi.org/10.1111/j.1574-6976.1995.tb00205.x
  10. Liu H, He Y, Jiang H, Peng H, Huang X, Zhang X, et al. 2007. Characterization of a phenazine-producing strain Pseudomonas chlororaphis GP72 with broad-spectrum antifungal activity from green pepper rhizosphere. Curr. Microbiol. 54: 302-306. https://doi.org/10.1007/s00284-006-0444-4
  11. Raaijmakers JM, de Bruijn I, de Kock MJ. 2006. Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol. Plant Microbe Interact. 19: 699-710. https://doi.org/10.1094/MPMI-19-0699
  12. Loper JE, Henkels MD, Shaffer BT, Valeriote FA, Gross H. 2008. Isolation and identification of rhizoxin analogs from Pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl. Environ. Microbiol. 74: 3085-3093. https://doi.org/10.1128/AEM.02848-07
  13. Omel’yanets T, Mel’nik G. 1987. Toxicological evaluation of the microbial preparation mycolytin. Zdravookhranenie Turkmenistana 6: 8.
  14. Tien T, Gaskins M, Hubbell D. 1979. Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl. Environ. Microbiol. 37: 1016-1024.
  15. Mehnaz S. 2013. Secondary metabolites of Pseudomonas aurantiaca and their role in plant growth promotion, pp. 373-393. In Arora NK (ed.). Plant Microbe Symbiosis: Fundamentals and Advances. Springer, Berlin-Heidelberg. Germany.
  16. Mehnaz S, Baig DN, Jamil F, Weselowski B, Lazarovits G. 2009. Characterization of a phenazine and hexanoyl homoserine lactone producing Pseudomonas aurantiaca strain PB-St2, isolated from sugarcane stem. J. Microbiol. Biotechnol. 19: 1688-1694. https://doi.org/10.4014/jmb.0904.04022
  17. Mehnaz S, Bauer JS, Gross H. 2014. Complete genome sequence of the sugar cane endophyte Pseudomonas aurantiaca PB-St2, a disease-suppressive bacterium with antifungal activity toward the plant pathogen Colletotrichum falcatum. Genome Announc. 2: e01108-e01113.
  18. Mehnaz S, Saleem RSZ, Yameen B, Pianet I, Schnakenburg G, Pietraszkiewicz H, et al. 2013. Lahorenoic acids A-C, ortho-dialkyl-substituted aromatic acids from the biocontrol strain Pseudomonas aurantiaca PB-St2. J. Nat. Prod. 76: 135-141. https://doi.org/10.1021/np3005166
  19. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44: 301-307.
  20. Winnepenninckx B, Backeljau T, De Wachter R. 1995. Phylogeny of protostome worms derived from 18S rRNA sequences. Mol. Biol. Evol. 12: 641-649.
  21. Normand P. 1995. Utilisation des sequences 16S pour le positionnement phyletique d’un organisme inconnu. Oceanis 21: 31-56.
  22. Tan Z-Y, Xu X-D, Wang E-T, Gao J-L, Martinez-Romero E, Chen W-X. 1997. Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int. J. Syst. Evol. Microbiol. 47: 874-879.
  23. Zhang Y, Fernando WG, Kievit TRd, Berry C, Daayf F, Paulitz T. 2006. Detection of antibiotic-related genes from bacterial biocontrol agents with polymerase chain reaction. Can. J. Microbiol. 52: 476-481. https://doi.org/10.1139/w05-152
  24. Rasul G, Mirza MS, Latif F, Malik KA. 1998. Identification of plant growth hormones produced by bacterial isolates from rice, wheat and kallar grass, pp. 25-37. In Malik KA, Sajjad Mirza M, Ladha JK (eds.). Nitrogen Fixation with Non-Legumes. Springer, Berlin-Heidelberg. Germany.
  25. Millar R, Higgins VJ. 1970. Association of cyanide with infection of birdsfoot trefoil by Stemphylium loti. Phytopathology 60: 104-110. https://doi.org/10.1094/Phyto-60-104
  26. Perez-Miranda S, Cabirol N, George-Tellez R, Zamudio-Rivera L, Fernandez F. 2007. O-CAS, a fast and universal method for siderophore detection. J. Microbiol. Methods 70: 127-131. https://doi.org/10.1016/j.mimet.2007.03.023
  27. Schwyn B, Neilands J. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56. https://doi.org/10.1016/0003-2697(87)90612-9
  28. Nautiyal CS. 1999. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol. Lett. 170: 265-270. https://doi.org/10.1111/j.1574-6968.1999.tb13383.x
  29. Pikovskaya R. 1948. Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17: e370.
  30. Sharma SK, Sharma MP, Ramesh A, Joshi OP. 2012. Characterization of zinc-solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds. J. Microbiol. Biotechnol. 22: 352-359. https://doi.org/10.4014/jmb.1106.05063
  31. Hoagland DR, Arnon DI. 1950. The Water-Culture Method for Growing Plants without Soil. California Agricultural Experimental Station Publications. College of Agriculture, University of California, Berkley, CA. USA.
  32. Andres JA, Rovera M, Guinazu LB, Pastor NA, Rosas SB. 2011. Role of Pseudomonas aurantiaca in crop improvement, pp. 107-122. Maheshwari DK (ed.). Bacteria in Agrobiology: Plant Growth Responses. Springer, Berlin-Heidelberg. Germany.
  33. Chin-A-Woeng TF, van den Broek D, de Voer G, van der Drift KM, Tuinman S, Thomas-Oates JE, et al. 2001. Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Mol. Plant Microbe Interact. 14: 969-979. https://doi.org/10.1094/MPMI.2001.14.8.969
  34. Hu W, Gao Q, Hamada MS, Dawood DH, Zheng J, Chen Y, Ma Z. 2014. Potential of Pseudomonas chlororaphis subsp. aurantiaca strain Pcho10 as a biocontrol agent against Fusarium graminearum. Phytopathology 104: 1289-1297. https://doi.org/10.1094/PHYTO-02-14-0049-R
  35. Rovera M, Pastor N, Niederhauser M, Rosas SB. 2014. Evaluation of Pseudomonas chlororaphis subsp. aurantiaca SR1 for growth promotion of soybean and for control of Macrophomina phaseolina. Biocontrol Sci. Technol. 24: 1012-1025. https://doi.org/10.1080/09583157.2014.910293
  36. Cezairliyan B, Vinayavekhin N, Grenfell-Lee D, Yuen GJ, Saghatelian A, Ausubel FM. 2013. Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog. 9: e1003101. https://doi.org/10.1371/journal.ppat.1003101
  37. Pierson III LS, Thomashow LS. 1992. Cloning and heterologous expression of the phenazine biosynthetic locus from Pseudomonas aureofaciens 30-84. Mol. Plant Microbe Interact. 5: 330-339. https://doi.org/10.1094/MPMI-5-330
  38. Cantore PL, Lazzaroni S, Coraiola M, Serra MD, Cafarchia C, Evidente A, Iacobellis NS. 2006. Biological characterization of white line-inducing principle (WLIP) produced by Pseudomonas reactans NCPPB1311. Mol. Plant Microbe Interact. 19: 1113-1120. https://doi.org/10.1094/MPMI-19-1113
  39. Meng J, Fan Y, Su M, Chen C, Ren T, Wang J, Zhao Q. 2014. WLIP derived from Lasiosphaera fenzlii Reich exhibits antitumor activity and induces cell cycle arrest through PPAR-${\gamma}$ associated pathways. Int. Immunopharmacol. 19: 37-44. https://doi.org/10.1016/j.intimp.2013.12.026
  40. Rokni-Zadeh H, Li W, Yilma E, Sanchez-Rodriguez A, De Mot R. 2013. Distinct lipopeptide production systems for WLIP (white line-inducing principle) in Pseudomonas fluorescens and Pseudomonas putida. Environ. Microbiol. Rep. 5: 160-169. https://doi.org/10.1111/1758-2229.12015
  41. Gaffney TD, Lam ST, Ligon J, Gates K, Frazelle A, Maio JD, et al. 1994. Global regulation of expression of antifungal factors by a Pseudomonas fluorescens biological control strain. Mol. Plant Microbe Interact. 7: 455-463. https://doi.org/10.1094/MPMI-7-0455
  42. Rovera M, Carlier E, Pasluosta C, Avanzini G, Andres J, Rosas S. 2008. Pseudomonas aurantiaca SR1: plant growth promoting traits, secondary metabolites and crop inoculation response, pp. 155-163. In Ahmad I, Pichtel J, Hayat S (eds.). Plant-Bacteria Interactions: Strategies and Techniques to Promote Plant Growth. John Wiley & Sons, NY. USA.
  43. Bapiri A, Asgharzadeh A, Mujallali H, Khavazi K, Pazira E. 2012. Evaluation of zinc solubilization potential by different strains of fluorescent pseudomonads. J. Appl. Sci. Environ. Manag. 16: 295-298.
  44. Di Simine C, Sayer J, Gadd G. 1998.Solubilization of zinc phosphate by a strain of Pseudomonas fluorescens isolated from a forest soil. Biol. Fertil. Soils 28: 87-94. https://doi.org/10.1007/s003740050467
  45. Rosas SB, Carlier E, Andres JA, Bergesse J, Guinazu LB, Rovera M, et al. 2012. Efficacy of Pseudomonas chlororaphis subsp. aurantiaca SR1 for improving productivity of several crops. In Sharma P, Abrol V (eds.). Crop Production Technologies, Ch. 8. InTech, Croatia.
  46. Rosas S, Rovera M, Andres J, Pastor N, Guinazu L, Carlier E, et al. 2005. Proceeding prospects and applications for plant associated microbes, pp. 91-99. In Sorvari S, Toldo O (eds.). Proceedings of the 1st International Conference on Plant-Microbe Interactions: Endophytes and Biocontrol Agents. Lapland, Finland.
  47. Mandryk MN, Kolomiets E, Dey ES. 2007. Characterization of antimicrobial compounds produced by Pseudomonas aurantiaca S-1. Polish J. Microbiol. 56: 245-250.

Cited by

  1. Identification and Quantification of Secondary Metabolites by LC-MS from Plant-associated Pseudomonas aurantiaca and Pseudomonas chlororaphis vol.8, pp.2, 2017, https://doi.org/10.21769/bioprotoc.2702
  2. A decade of understanding secondary metabolism in Pseudomonas spp. for sustainable agriculture and pharmaceutical applications vol.1, pp.1, 2017, https://doi.org/10.1007/s42398-018-0006-2
  3. Phenazine and 1-Undecene Producing Pseudomonas chlororaphis subsp. aurantiaca Strain KNU17Pc1 for Growth Promotion and Disease Suppression in Korean Maize Cultivars vol.29, pp.1, 2017, https://doi.org/10.4014/jmb.1808.08026
  4. Exploitation of new endophytic bacteria and their ability to promote sugarcane growth and nitrogen nutrition vol.112, pp.2, 2017, https://doi.org/10.1007/s10482-018-1157-y
  5. Volatile Organic Compounds Produced by Pseudomonas chlororaphis subsp. aureofaciens SPS-41 as Biological Fumigants To Control Ceratocystis fimbriata in Postharvest Sweet Potatoes vol.67, pp.13, 2019, https://doi.org/10.1021/acs.jafc.9b00289
  6. Impact of Soil Salinity on the Cowpea Nodule-Microbiome and the Isolation of Halotolerant PGPR Strains to Promote Plant Growth under Salinity Stress vol.4, pp.4, 2017, https://doi.org/10.1094/pbiomes-09-19-0057-r
  7. Full Issue PDF vol.4, pp.4, 2020, https://doi.org/10.1094/pbiomes-4-4
  8. Draft Genome Sequence of Pseudomonas chlororaphis subsp. aurantiaca ARS-38, a Bacterial Strain with Plant Growth Promotion Potential, Isolated from the Rhizosphere of Cotton in Pakistan vol.9, pp.3, 2017, https://doi.org/10.1128/mra.01398-19
  9. Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides vol.104, pp.3, 2017, https://doi.org/10.1007/s00253-019-10300-8
  10. Insights into plant-beneficial traits of probiotic Pseudomonas chlororaphis isolates vol.69, pp.3, 2017, https://doi.org/10.1099/jmm.0.001157
  11. High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of upland rice vol.203, pp.2, 2017, https://doi.org/10.1007/s00203-020-02058-9
  12. Pseudomonas mediated nutritional and growth promotional activities for sustainable food security vol.2, pp.None, 2021, https://doi.org/10.1016/j.crmicr.2021.100084