2019 ; Vol.29-1: 66~78
|Author||Setu Bazie Tagele, Hyun Gu Lee, Sang Woo Kim, Youn Su Lee|
|Title||Phenazine and 1-Undecene Producing Pseudomonas chlororaphis subsp. aurantiaca Strain KNU17Pc1 for Growth Promotion and Disease Suppression in Korean Maize Cultivars|
J. Microbiol. Biotechnol.2019 ;
|Abstract||In this study, strain KNU17Pc1 was tested for its antifungal activity against Rhizoctonia solani
AG-1(IA), which causes banded leaf and sheath blight (BLSB) of maize. KNU17Pc1 was tested
further for its broad-spectrum antifungal activity and in vitro plant growth promoting (PGP)
traits. In addition, the in vivo effects of KNU17Pc1 on reduction of BLSB severity and seedling
growth promotion of two maize cultivars under greenhouse conditions were investigated. On
the basis of multilocus sequence analysis (MLSA), KNU17Pc1 was confirmed as P. chlororaphis
subsp. aurantiaca. The study revealed that KNU17Pc1 had strong in vitro antifungal activity
and was effective toward all in vitro PGP traits except phosphate solubilization. In this study,
for the first time, a strain of P. chlororaphis against Colletotrichum dematium, Colletotrichum
gloeosporioides, Fusarium oxysporum f.sp. melonis, Fusarium subglutinans and Stemphylium
lycopersici has been reported. Further biochemical studies showed that KNU17Pc1 was able to
produce both types of phenazine derivatives, PCA and 2-OH-PCA. In addition, solid phase
microextraction-gas chromatography–mass spectrometry (SPME-GC-MS) analysis identified
13 volatile organic compounds (VOCs) in the TSB culture of KNU17Pc1, 1-undecene being the
most abundant volatile. Moreover, for the first time, Octamethylcyclotetrasiloxan (D4),
dimethyl disulfide, 2-methyl-1,3-butadiene and 1-undecene were detected in P. chlororaphis.
Furthermore, this study reported for the first time the effectiveness of P. chlororaphis to control
BLSB of maize. Hence, further studies are necessary to test the effectiveness of KNU17Pc1
under different environmental conditions so that it can be exploited further for biocontrol and
plant growth promotion.|
|Key_word||Biocontrol, SPME-GC-MS, PGPR, Zea mays, Pseudomonas chlororaphis|
Shiferaw B, Prasanna BM, Hellin J, Bänziger M. 2011. Crops that feed the world 6. Past successes and future challenges to the role played by maize in global food security. Food Security 3: 307.
Castiglioni P, Warner D, Bensen RJ, Anstrom DC, Harrison J, Stoecker M, et al. 2008. Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol. 147: 446-455.
Ramachandiran K, Pazhanivelan S. 2016. Abiotic factors (nitrogen and water) in maize: a review. Agric. Rev. 37: 317-324.
Hooda KS, Khokhar MK, Parmar H, Gogoi R, Joshi D, Sharma SS, et al. 2017. Banded leaf and sheath blight of maize: historical perspectives, current status and future directions. Proc. N atl. A cad. S ci., India S ect. B B iol. S ci. 87: 1041-1052.
Groth DE, Bond JA. 2006. Initiation of rice sheath blight epidemics and effect of application timing of azoxystrobin on disease incidence, severity, yield, and milling quality. Plant Dis. 90: 1073-1076.
Compant S, Duffy B, Nowak J, Clement C, Barka, E. 2005. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action and future prospects. Appl. Environ. Microbiol. 71: 4951-4959.
Duke KA, Becker MG, Girard IJ, Millar JL, Fernando WD, Belmonte MF, et al. 2017. The biocontrol agent Pseudomonas chlororaphis PA23 primes Brassica napus defenses through distinct gene networks. BMC Genomics 18: 467.
Jain R, Pandey AA. 2016. phenazine-1-carboxylic acid producing polyextremophilic Pseudomonas chlororaphis (MCC2693) strain, isolated from mountain ecosystem, possesses biocontrol and plant growth promotion abilities. Microbiol. Res. 190: 63-71.
Egamberdieva D, Jabborova D, Hashem A. 2015. Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi J. Boil. Sci. 22: 773-779.
Shrestha BK, Karki HS, Groth DE, Jungkhun N, Ham JH. 2016. Biological control activities of rice-associated Bacillus sp. strains against sheath blight and bacterial panicle blight of rice. PLoS One 11: e0146764.
Schwyn B, Neilands JB. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160: 47-56.
Smibert RM, Krieg NR. 1994. Phenotypic Characterization. In Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds.), Methods for General and Molecular Bacteriology, pp. 607-654. American Society for Microbiology, Washington, D.C
Ghodsalavi B, Ahmadzadeh M, Soleimani M, Madloo PB, Taghizad-Farid R. 2013. Isolation and characterization of rhizobacteria and their effects on root extracts of Valeriana officinalis. Austr. J. Crop Sci. 7: 338-344.
Cappuccino JG, Sherman N. 1996. pp. 186. 4th Ed. Microbiology:A Laboratory Manual. The Benjamin/cummings Publishing Co., Inc., Menlo Park, California.
Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiol. 26: 192-195.
Pamp SJ, Tolker-Nielsen T. 2006. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 189: 2531-2539.
Pierson III LS, Thomashow LS. 1992. Cloning and heterologous expression of the phenazine biosynthetic. Mol. Plant-Microbe Interact. 5: 330-339.
Davis BD, Mingioli ES. 1950. Mutants of Escherichia coli requiring methionine or vitamin B12. J. Bacteriol. 60: 17-28.
Wood DW, Gong F, Daykin MM, Williams P, Pierson L. 1997. N-acyl-homoserine lactone-mediated regulation of phenazine gene expression by Pseudomonas aureofaciens 30-84 in the wheat rhizosphere. J. Bacteriol. 179: 7663-7670.
Maddula VSRK, Pierson E A, Pierson III LS. 2008. Altering the ratio of phenazines in Pseudomonas chlororaphis (aureofaciens) strain 30-84: effects on biofilm formation and pathogen inhibition. J. Bacteriol. 190: 2759-2766.
Ohkura M, Abawi GS, Smart CD, Hodge KT. 2009. Diversity and aggressiveness of Rhizoctonia solani and Rhizoctonia-like fungi on vegetables in New York. Plant Dis. 93: 615-624.
Ahuja SC, Payak MM. 1986. A rating scale for banded leaf and sheath blight of maize. Indian Phytopath. Indian Phytopathologyrecd 36: 338-340
Wheeler BEJ. 1969. An Introduction to Plant Diseases. The English language Book Socity And Wiley and Sons Ltd, London.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
Culbertson JE, Toney MD. 2013. Expression and characterization of PhzE from P. aeruginosa PAO1: aminodeoxyisochorismate synthase involved in pyocyanin and phenazine-1-carboxylate production. Biochim. Biophys. Acta Proteins Proteomics 1834:240-246.
Schneemann I, Wiese J, Kunz AL, Imhoff JF. 2011. Genetic approach for the fast discovery of phenazine producing bacteria. Mar. Drugs 9: 772-789.
SAS Institute Inc. 2008. SAS/STAT 9.2 User’s Guide. Cary, NC: Institute Inc.
Andreani NA, Martino ME, Fasolato L, Carraro L, Montemurro F, Mioni R, et al. 2015. Tracking the blue: a MLST approach to characterise the Pseudomonas fluorescens group. Food Microbiol. 45: 148-158.
Devi TV, Vizhi RM, Sakthivel N, Gnanamanickam SS. 1989. Biological control of sheath-blight of rice in India with antagonistic bacteria. Plant Soil 119: 325-330.
Nejad MS, Bonjar GHS, Khatami M, Amini A, Aghighi S. 2016. In vitro and in vivo antifungal properties of silver nanoparticles against Rhizoctonia solani, a common agent of rice sheath blight disease. IET. Nanobiotechnol. 11: 236-240.
Thrane C, Nielsen MN, Sørensen J, Olsson S. 2001. Pseudomonas fluorescens DR54 reduces sclerotia formation, biomass development, and disease incidence of Rhizoctonia solani causing damping-off in sugar beet. Microb. Ecol. 42:438-445.
Tariq M, Yasmin S, Hafeez FY. 2010. Biological control of potato black scurf by rhizosphere associated bacteria. Braz. J. Microbiol. 41: 439-451.
Hu QP, Xu JG, Song P, Song JN, Chen WL. 2008. Isolation and identification of a potential biocontrol agent Bacillus subtilis QM3 from Qinghai yak dung in China. World J. Microbiol. Biotechnol. 24: 2451-2458.
Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B. 2009. Bacterial volatiles and their action potential. Appl. Microbial. Biotechnol. 81: 1001-1012.
Wang JH, Zhang JB, Li HP, Gong AD, Xue S, Agboola RS, et al. 2014. Molecular identification, mycotoxin production and comparative pathogenicity of Fusarium temperatum isolated from maize in China. J. Phytopathol. 162: 147-157.
Varela CP, Casal OA, Padin MC, Martinez VF, Oses MS, Scauflaire J, et al. 2013. First report of Fusarium temperatum causing seedling blight and stalk rot on maize in Spain. Plant Dis. 97: 1252-1253.
Park HK, Kim BS, Lee WS. 1990. Inheritance of resistance to anthracnose (Colletotrichum spp.) in pepper (Capsicum annuum L.). II. Genetic analysis of resistance to Colletotrichum dematium. J. Kor. Soc. Hort. Sci. 31: 207-212.
Du Toit LJ, Derie ML. 2003. Inoculum sources of Stemphylium botryosum and Cladosporium variabile in spinach seed crops. Phytopathology 93: S22.
Suárez-Estrella F, Vargas-Garcia C, Lopez MJ, Capel C, Moreno J. 2007. Antagonistic activity of bacteria and fungi from horticultural compost against Fusarium oxysporum f. sp. melonis. Crop Prot. 26: 46-53.
Huang CJ, Tsay JF, Chang SY, Yang HP, Wu WS, Chen CY. 2012. Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag. Sci. 68:1306-1310.
Whistler CA, Pierson III LS. 2003. Repression of phenazine antibiotic production in Pseudomonas aureofaciens strain 30-84 by RpeA. J. Bacteriol. 185: 3718-3725.
Haas D, Défago G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3: 307-319.
Mavrodi DV, Blankenfeldt W, Thomashow LS. 2006. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 44: 417-445.
He L, Xu YQ, Zhang XH. 2008. Medium factor optimization and fermentation kinetics for phenazine-1-carboxylic acid production by Pseudomonas sp. M18G. Biotechnol. Bioeng. 100:250-259.
Chin-A-Woeng TF, Thomas-Oates JE, Lugtenberg BJ, Bloemberg GV. 2001. Introduction of the phzH gene of Pseudomonas chlororaphis PCL1391 extends the range of biocontrol ability of phenazine-1-carboxylic acid-producing Pseudomonas spp. strains. Mol.Plant-Microbe Interact. 14:1006-1015.
Yuan M, Yu Y, Li HR, Dong N, Zhang XH. 2014. Phylogenetic diversity and biological activity of actinobacteria isolated from the Chukchi Shelf marine sediments in the Arctic Ocean. Mar. Drug. 12: 1281-1297.
Passari AK, Chandra P, Leo VV, Mishra VK, Kumar B, Singh BP. 2017. Production of potent antimicrobial compounds from Streptomyces cyaneofuscatus associated with fresh water sediment. Front. Microbiol. 8: 68.
Cordero P, Príncipe A, Jofré E, Mori G, Fischer S. 2014. Inhibition of the phytopathogenic fungus Fusarium proliferatum by volatile compounds produced by Pseudomonas. Arch. Microbiol. 196: 803-809.
Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L. 2015. Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl. Environ. Microbiol. 81: 821-830.
Velivelli SL, Kromann P, Lojan P, Rojas M, Franco J, Suarez JP, et al. 2015. Identification of mVOCs from Andean rhizobacteria and field evaluation of bacterial and mycorrhizal inoculants on growth of potato in its center of origin. Microb. Ecol. 69:652-667.
Lin Y, Liu Q, Cheng L, Lei Y, Zhang A. 2014. Synthesis and antimicrobial activities of polysiloxane-containing quaternary ammonium salts on bacteria and phytopathogenic fungi. React. Funct. Polym. 85: 36-44.
Schöller C, Molin S, Wilkins K. 1997. Volatile metabolites from some gram-negative bacteria. Chemosphere 35: 1487-1495.
Holopainen JK. 2004. Multiple functions of inducible plant volatiles. Trends Plant Sci. 9: 529-533.
Meldau DG, Meldau S, Hoang LH, Underberg S, Wünsche H, Baldwin IT. 2013. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell 25: 2731-2747.
Hernández-León R, Rojas-Solís D, Contreras-Pérez M, del Carmen Orozco-Mosqueda M, Macías-Rodríguez LI, Reyesde la Cruz H, et al. 2015. Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biol. Control 81: 83-92.
Jiao Z, Wu N, Hale L, Wu W, Wu D, Guo Y. 2013. Characterisation of Pseudomonas chlororaphis subsp. aurantiaca strain Pa40 with the ability to control wheat sharp eyespot disease Ann. Appl. Biol. 163: 444-453.
Shahid I, Rizwan M, Baig DN, Saleem RS, Malik KA, Mehnaz S. 2017. Secondary metabolites production and plant growth promotion by Pseudomonas chlororaphis and P. aurantiaca strains isolated from cactus, cotton, and para grass. J. Microbiol. Biotechnol. 27: 480-491.
Alemu F, Alemu T. 2015. Pseudomonas fluorescens isolates used as a plant growth promoter of Faba Bean (Vicia faba) in vitro as well as in vivo study in Ethiopia. Am. J. Life Sc. 3: 100-108.
Jha CK, Patel B, Saraf M. 2012. Stimulation of the growth of Jatropha curcas by the plant growth promoting bacterium Enterobacter cancerogenus MSA2. World J. Microbiol. Biotechnol. 28: 891-899.
Bhattacharyya PN, Jha DK. 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28: 1327-1350.
Hrynkiewicz K, Baum C, Leinweber P. 2010. Density, metabolic activity, and identity of cultivable rhizosphere bacteria on Salix viminalis in disturbed arable and landfill soils. J. Plant Nutr. Soil Sci. 173: 747-756.
Sivakumar G, Sharma RC, Rai SN. 2000. Biocontrol of banded leaf and sheath blight of maize by peat based Pseudomonas fluorescens formulation. Indian Phytopathol. 53: 190-192.
Kozdrój J, Trevors JT, Van Elsas JD. 2004. Influence of introduced potential biocontrol agents on maize seedling growth and bacterial community structure in the rhizosphere. Soil Biol. Biochem. 36: 1775-1784.
Sandhya VS, Ali SZ, Grover M, Reddy G, Venkateswarlu B. 2010. Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul. 62: 21-30.
Glick BR, Cheng Z, Czarny J, Duan J. 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur. J. Plant Pathol. 119: 329-339.
Dimkpa CO, Merten D, Svatoš A, Büchel G, Kothe E. 2009. Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J. Appl. Microbiol. 107: 1687-1696.
Anees M, Edel-Hermann V, Steinberg C. 2010. Build up of patches caused by Rhizoctonia solani. Soil Biol. Biochem. 42:1661-1672.