Isolation and characterization of sunflower associated bacterial strain with broad spectrum plant growth promoting traits

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Isolation and characterization of sunflower associated bacterial strain with broad spectrum plant growth promoting traits

Afshan Majeed, M. Kaleem Abbasi, Sohail Hameed, Asma Imran, Tahir Naqqash, Muhammad Kashif Hanif
Int. J. Biosci.13( 2), 111-125, August 2018.
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Abstract

Plant growth promoting rhizobacteria (PGPR) based biofertilizers act as a natural driving force, allowing crops to deliver their full potential by providing a promising alternative to chemical fertilizers and pesticides. Despite its economic importance a little is known about the response of sunflower towards inoculation with PGPR. A potential PGPR was isolated from Chamyati, Azad Jammu and Kashmir, an unexplored area towards PGPR and the bacterial mechanisms related to plant growth promotion were evaluated and characterized. The bacterium was identified as Arthrobacter sp. AF-163 through 16S rRNA gene sequence analysis. This bacterium was found catalase and cytochrome oxidase positive, metabolically diverse by utilizing 54 out of 93 carbon sources in Biolog microplate analysis and resistant to a number of antibiotics in intrinsic antibiotic resistance assay. AF-163 showed nitrogenase activity (107.2 nmoles mg-1 protein h-1) in gas chromatographic analysis; produced 23.7 µgmL-1 indole-3-acetic acid (HPLC analysis) and solubilized 40.5 μgmL−1 insoluble phosphorus (spectrophotometric analysis) displaying significant decrease in pH (up to 2.3) due to the production of ascorbic acid, malic acid and gluconic acid and oxalic acid. Moreover AF-163 showed antagonistic activity against Fusarium oxysporum in in vitro dual culture assay. Inoculation with this bacterium to sunflower grown in soil-free culture showed a significant increase in sunflower growth parameters.  This study concludes that Arthrobacter sp. strain AF-163 contains multiple plant growth promoting traits, recommended to be evaluated further under field conditions before using them as commercial bio-inoculant.

VIEWS 7

Adesemoye AO, Egamberdieva D. 2013. Beneficial effects of plant prowth-promoting phizobacteria on improved crop production. Journal of Developmental Economics 22, 45-63.

Ahemad M, Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University. Science 26, 1‒20.

Ahmad F, Ahmad I, Khan M. 2008. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbioogical Research 163(2), 173-181.

Ali S, Hameed S, Imran A, Iqbal M, Lazarovits G. 2014. Genetic, physiological and biochemical characterization of Bacillus sp. strain RMB7 exhibiting plant growth promoting and broad spectrum antifungal activities. Microbial Cell Factories 13(1), 144.

Ambrosini A, Beneduzi A, Stefanski T, Pinheiro FG, Vargas LK, Passaglia LMP. 2012. Screening of plant growth promoting rhizobacteria isolated from sunflower (Helianthus annuus L.). Plant and Soil 356, 245-264.

Antoun H, Prévost D. 2005. Ecology of Plant Growth Promoting Rhizobacteria.  PGPR: Biocontrol and Biofertilization. Springer. p 1-38.

Babalola OO. 2010. Beneficial bacteria of agricultural importance. Biotechnology Letters 32(11), 1559-1570.

Balasubramaniyan P, Palaniappan SP. 2004. Principles and practices of agronomy. Agrobios, India.

Bashan Y, De-Bashan LE. 2010. How the plant growth promoting bacterium Azospirillum promotes plant growth-A critical assessment. Advances in Agronomy 108, 77-136.

Berg G, Smalla K. 2009. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68(1), 1-13.

Bianco C, Defez R. 2010. Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appllied and Environmental Microbiology 76, 4626–4632. http://dx.doi.org/10.1128/AEM.02756-09

Buchan A, Crombie B, Alexandre GM. 2010. Temporal dynamics and genetic diversity of chemotactic-competent microbial populations in the rhizosphere. Environmental Microbiology 12(12), 3171-3184.

de Weert S, Dekkers LC, Bitter W, Tuinman S, Wijfjes AHM, Van Boxtel R, Lugtenberg BJJ. 2006. The two component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane. FEMS Microbiology Ecolpgy 58(2), 205-213.

de Werra P, Péchy-Tarr M, Keel C, Maurhofer M. 2009. Role of gluconic acid production in the regulation of biocontrol traits of Pseudomonas fluorescens CHA0. Appllied and Environmental Microbiology 75(12), 4162-4174.

Dimkpa C, Weinand T, Asch F. 2009. Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant, Cell and Environment 32(12), 1682-1694.

Dobbelaere S, Vanderleyden J, Okon Y. 2003. Plant growth-promoting effects of diazotrophs in the rhizosphere. Critical Reviews in Plant Sciences 22(2), 107-149.

Edi–Premono M, Moawad A,Vleck PLG. 1996. Effect of phosphate solubilizing Pseudmonas putida on the growth of maize and its survival in the rhizosphere. Indonasian Journal of Crop Sciences 11, 13–23.

Ehsanullah KJ, Ismail M, Hussain M, Zafar M, Zaman U. 2011. Hydroprimed sunflower achenes perform better than the salicylic acid primed achenes. Journal of Agricultural Science and Technololgy 7(6), 1561-1569.

Fernando WGD, Nakkeeran S, Zhang Y. 2006. Biosynthesis of antibiotics by PGPR and its relation in biocontrol of plant diseases. In PGPR: Biocontrol and Biofertilization. Edited by Siddiqui ZA. Netherlands: Springer 67–109.

Fuentes-Ramirez, LE. Caballero-Mellado J. 2006. Bacterial biofertilizers.  PGPR: Biocontrol and Biofertilization. Springer. p 143-172.

Ghyselinck J, Velivelli SL, Heylen K, O’Herlihy E, Franco J, Rojas M. 2013. Bioprospecting in potato fields in the central andean highlands: screening of rhizobacteria for plant growth-promoting properties. Systematic and Appllied Microbiology 36, 116–127. http://dx.doi.org/10.1016/j.syapm.2012.11.007

GOP. 2012. Economic Survey of Pakistan, 2011-2012. Finance Division, Economic Advisor’s Wing, Islamabad, Pakistan.

Gordon SA, Weber RP. 1951. Colorimetric estimation of indoleacetic acid. Plant Physiology 26(1), 192-195.

Haas D,  Défago G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 3(4), 307-319.

Hanif K, Hameed S, Imran A, Naqqash T, Shahid M, Van Elsas JD. 2015. Isolation and characterization of a β-propeller gene containing phosphobacterium Bacillussubtilis strain KPS-11 for growth promotion of potato (Solanum tuberosum L.). Frontiers in Microbiology 6, 583.

Hariprasad P, Niranjana S. 2009. Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant and Soil 316(1-2), 13-24.

Hussain K, Hameed Shahid SM, Ali A, Iqbal J, Hahn D. 2015. First report of Providencia vermicola strains characterized for enhanced rapeseed growth attributing parameters. Internatinal Journal Agriculture and Biology 17, 1110‒1116.

Hussain M, Farooq M, Jabran K, Wahid A. 2010. Foliar application of glycinebetaine and salicylic acid improves growth, yield and water productivity of hybrid sunflower planted by different sowing methods. Journal of Agronomy and Crop Science 196(2), 136-145.

Imran A, Mirza MS, Shah TM, Malik KA, Hafeez FY. 2015. Differential esponse of kabuli and desi chickpea genotypes toward inoculation with PGPR in different soils. Frontiers in Microbiology 6,  859. http://dx.doi.org/10.3389/fmicb.2015.00859

Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, Zhou W. 2016. Plant growth promoting bacteria confer salt tolerance in Vignaradiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regulation 80(1), 23-36.

Jorquera MA, Crowley DE, Marschner P, Greiner R, Fernández MT, Romero D. 2011. Identification of β-propeller phytase-encoding genes in culturable Paenibacillus and Bacillus spp. from the rhizosphere of pasture plants on volcanic soils. FEMS Microbiology Ecology 75, 163–172. http://dx.doi.org/10.1111/j.1574-6941.2010.00995.x

Kaymak HC. 2011. Potential of PGPR in agricultural innovations, in: Maheshwari, D.K. (Eds.), Plant Growth and Health Promoting Bacteria. Springer, Berlin, p 45–79.

Khan AG. 2005. Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. Journal of Trace Elements in Medicine and Biology 18, 355–364.

Kumar A, Guleria S, Mehta P, Walia A, Chauhan A, Shirkot CK. 2015. Plant growth-promoting traits of phosphate solubilizing bacteria isolated from Hippophae rhamnoides L. (Sea-buckthorn) growing in cold desert Trans-Himalayan Lahul and Spiti regions of India. Acta Physiologiae Plantarum 37(3), 47-59.

Lavania M, Nautiyal C. 2013. Solubilization of tricalcium phosphate by temperature and salt tolerant Serratia marcescens NBRI1213 isolated from alkaline soils. African Journal of Microbiology Research 7, 4403–4413. http://dx.doi.org/10.5897/AJMR2013.5773

Lawlor DW. 2002. Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. Journal of Experimental Botany 53(370), 773-787.

Line J, Hiett K, Guard J, Seal B. 2011. Temperature affects sole carbon utilization patterns of Campylobactercoli 49941. Current Microbiology 62(3), 821-825.

Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63, 541-556.

Majeed A, Abbasi MK, Hameed S, Imran A. Rahim N. 2015. Isolation and characterization of plant growth-promoting rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Frontiers in Microbiology 6, 198.

Maniatis T, Fritsch EF, Sambrook J. 1982. Molecular Cloning: A Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory.

Medeiros FH, Souza RM, Medeiros FC, Zhang H, Wheeler T, Payton P, Ferro HM, Paré PW. 2011. Transcriptional profiling in cotton associated with Bacillus subtilis (UFLA285) induced biotic-stress tolerance. Plant and Soil 347(1-2) 327-337.

Müller EE, Ehlers MM. 2007. Biolog identification of non-sorbitol fermenting bacteria isolated on E. coliO157 selective CT-SMAC agar. Water SA 31, 247–252.

Naqqash T, Hameed S, Imran A, Hanif MK, Majeed A, van Elsas JD. 2016. Differential response of potato toward inoculation with taxonomically diverse plant growth promoting rhizobacteria. Frontiers in Plant Sciences 7.

Nayidu N, Bollina V, Kagale S. 2013.  Oilseed crop productivity under salt stress. In: Ahmad, P., Azooz, M. M., Prasad, M. N. V.  (eds.), Ecophysiology and Responses of Plants Under Salt Stress. Springer International Publishing, New York, USA, p 252–253.

Palaniappan P, Chauhan PS, Saravanan VS, Anandham R, Sa T. 2010. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biology and Fertility of Soils 46(8), 807-816.

Park M, Kim C, Yang J, Lee H, Shin W, Kim S. 2005. Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiological Research 160, 127–133. http://dx.doi.org/10.1016/j.micres.2004.10.003

Patel DK, Archana G, Kumar GN. 2008. Variation in the nature of organic acid secretion and mineral phosphate solubilization by Citrobacter sp. DHRSS in the presence of different sugars. Current Microbiolgy 56(2), 168-174.

Pérez-Montaño F, Alías-Villegas C, Bellogín RA,Cerro PD, Espuny MR, Jiménez-Guerrero I. 2013. Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiological Research 169, 325–336. http://dx.doi.org/10.1016/j.micres.2013. 09.011

Pikovskaya RI. 1948. Metabolism of phosphorous in soil in connection with vital activity of some microbial species. Microbiologia 17, 362-370.

Radzki W, Mañero FG, Algar E, García JL, García-Villaraco A, Solano BR. 2013. Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Antonie Van Leeuwenhoek 104(3), 321-330.

Richardson AE, Barea JM, McNeill AM,  Prigent-Combaret C. 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil 321(1-2), 305-339.

Saharan B, Nehra V. 2011. Plant growth promoting rhizobacteria: a critical review. Life Sciences and Medicine Research 21, 1-30.

Sahin F, Çakmakçi R, Kantar F. 2004. Sugar beet and barley yields in relation to inoculation with N2-fixing and phosphate solubilizing bacteria. Plant and Soil 265(1), 123-129.

Sakthivel N, Gnanamanickam S. 1987. Evaluation of Pseudomonas fluorescens for suppression of sheath rot disease and for enhancement of grain yields in rice (Oryza sativa L.). Appllied and Environmental Microbiology 53(9), 2056-2059.

Shahid M, Hameed S, Tariq M, Zafar M, Ali A, Ahmad N. 2014. Characterization of mineral phosphate-solubilizing bacteria for enhanced sunflower growth and yield-attributing traits. Annals of Microbiology 65(3), 1525-1536.

Shen H, He X, Liu Y, Chen Y, Tang J, Guo T. 2016. A Complex Inoculant of N2-Fixing, P-and K-Solubilizing Bacteria from a Purple Soil Improves the Growth of Kiwifruit (Actinidia chinensis) Plantlets. Frontiers in Microbiology 7, 84.

Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá JA. 2009. Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biology and Biochemistry 41(9), 1768-1774.

Singh H, Reddy MS. 2011. Effect of inoculation with phosphate solubilizing fungus on growth and nutrient uptake of wheat and maize plants fertilized with rock phosphate in alkaline soils. European Journal of Soil Biology 47(1), 30-34.

Škorić D, Jocić S, Sakač Z, Lečić N. 2008. Genetic possibilities for altering sunflower oil quality to obtain novel oils. Canadian Journal of Physiology and Pharmacology 86(4), 215–221.

Somasegaran P, Hoben HJ. 1994. Handbook for rhizobia: methods in legume-Rhizobium technology Springer-Verlag New York Inc.

Souza R, Ambrosini A, Passaglia LM. 2015. Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecuar Biology 38(4), 401-419.

Spaepen S, Vanderleyden J, Remans R. 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews 31(4), 425-448.

Steel RGD, Torrie JH, Dickey DA. 1997. Principles and Procedures of Statistics, A biometrical approach. (3rd  Ed.). McGraw Hill Book Int. Co., New York. p 172-177.

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.), Appllied and Environmental Microbiology 37, 1016-1024.

Tilman D, Fargione J, Wolff B, Antonio CD’, Dobson A, Howarth R, Schindler D, Schlesinger W, Simberloff D, Swackhamer D. 2001. Forecasting agriculturally driven global environmental change. Science 292(5515), 281-284.

Valverde A, Velazquez E, Fernandez-Santos F, Vizcaino N, Rivas R, Mateos PF, Martinez-Molina E, Igual JM,  Willems A. 2005. Phyllobacterium trifolii sp. nov., nodulating Trifolium and Lupinus in Spanish soils. International Journal of Systematic and Evolutionary Microbiology 55, 1985-1989.

Van Loon L. 2007. Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology 119(3), 243-254.

Vincent JM, Humphrey B. 1970. Taxonomically significant group antigens in Rhizobium. Journal of Genenal Microbiology 63, 379–382. http://dx.doi.org/10.1099/00221 287-63-3-379

Waver RW, Frederick LR. 1982. Rhizobium, in: Page A. L., Miller, R. H., Keeney D. R.(Eds.), Methods of Soil Analysis, Part 2. Chemical and Microbiological Properties.Madison, WI: SSSA, p. 1043–1067.

Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173(2), 697-703.

Wielbo J, Marek-Kozaczuk M, Kubik-Komar A, Skorupska A. 2007. Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Canadian Journal of Microbiology 53(8), 957-967.