Abstract
Study of endophytic bacteria within plant seeds is very essential and meaningful on account of their heritability and versatility. This study investigated Bacillus bacterial communities within the seeds of four commercial tomato varieties, by 16S rRNA gene PCR-RFLP (restriction fragment length polymorphism). Phylogenetic analysis of 16S rRNA gene sequences indicated that the 22 representative isolates belonged to five species of genus Bacillus and the bacterial compositions showed remarkable differences among tomato varieties. Isolates exhibited multiple plant growth promoting (PGP) traits: 37 % of indole-3-acetic acid production; 37 % of phosphate solubilization; 24 % of siderophores production; 85 % of potential nitrogen fixation and 6 % of 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity. Isolate HYT-12-1 was shown to have highest ACC deaminase activity (112.02 nmol α-ketobutyrate mg−1 protein h−1) among the five ACC deamiase producing strains. 16S rRNA gene sequencing indicated that the isolate HYT-12-1 shared the highest sequence similarity (100 %) with B. subtilis. PGP experiments under gnotobiotic and greenhouse conditions revealed the ability of strain HYT-12-1 to enhance the growth of tomato seedlings. This is the first study to describe endophytic Bacillus communities within tomato seeds, and the results suggest that B. subtilis strain HYT-12-1 would have a great potential for industrial application as biofertilizer in the future.
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Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929
Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
Ali S, Charles TC, Glick BR (2012) Delay of flower senescence by bacterial endophytes expressing 1-aminocyclopropane-1-carboxylate deaminase. J Appl Microbiol 113:1139–1144
Barnawal D, Bharti N, Maji D, Chanotiya CS, Kalra A (2012) 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol Bioch 58:227–235
Bashan Y, Holguin G, Lifshitz R (1993) Isolation and characterization of plant growth-promoting rhizobacteria. In: Glick BR, Thompson JE (eds) Methods in plant molecular biology and biotechnology. CRC Press, USA, pp 331–345
Beneduzi A, Peres D, Vargas LK, Bodanese-Zanettini MH, Passaglia LMP (2008) Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing bacilli isolated from rice fields in South Brazil. Appl Soil Ecol 39:311–320
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cankar K, Kraigher H, Ravnikar M, Rupnik M (2005) Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett 244:341–345
Cavaglieri L, Orlando J, Etcheverry M (2009) Rhizosphere microbial community structure at different maize plant growth stages and root locations. Microbiol Res 164:391–399
Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Yong CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
de Santi Ferrara FI, Oliveira ZM, Gonzales HHS, Floh EIS, Barbosa HR (2012) Endophytic and rhizospheric enterobacteria isolated from sugar cane have different potentials for producing plant growth-promoting substances. Plant Soil 353:409–417
Deepa CK, Dastager SG, Pandey A (2010) Isolation and characterization of plant growth promoting bacteria from non-rhizospheric soil and their effect on cowpea (Vigna unguiculata (L.) Walp.) seedling growth. World J Microbiol Biotech 26:1233–1240
Enya J, Shinohara H, Yoshida S, Tsukiboshi T, Negishi H, Suyama K, Tsushima S (2007) Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents. Microb Ecol 53:524–536
Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Micobiol Lett 251:1–7
Glick BR, Karaturovic DM, Newell PC (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41:533–536
Hardoim PR, van Overbeek LS, van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471
Hardoim PR, Hardoim CC, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One 7:e30438
Jalili F, Khavazi K, Pazira E, Nejati A, Rahmani HA, Sadaghiani HR, Miransari M (2009) Isolation and characterization of ACC deaminase-producing fluorescent pseudomonads, to alleviate salinity stress on canola (Brassica napus L.) growth. J Plant Physiol 166:667–674
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 Biotech 28:891–899
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257
Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8:298–300
Li Z, Chang S, Lin L, Li Y, An Q (2011) A colorimetric assay of 1-aminocyclopropane-1-carboxylate (ACC) based on ninhydrin reaction for rapid screening of bacteria containing ACC deaminase. Lett Appl Microbiol 53:178–185
Logan NA, Berkeley RCW (1984) Identification of Bacillus strains using the API system. J Gen Microbiol 130:1871–1882
Mano H, Tanaka F, Nakamura C, Kaga H, Morisaki H (2007) Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes Environ 22:175–185
Montañez A, Blanco AR, Barlocco C, Beracochea M, Sicardi M (2012) Characterization of cultivable putative endophytic plant growth promoting bacteria associated with maize cultivars (Zea mays L.) and their inoculation effects in vitro. Appl Soil Ecol 58:21–28
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270
Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572
Okunishi S, Sako K, Mano H, Imamura A, Morisaki H (2005) Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ 20:168–177
Onofre-Lemus J, Hernández-Lucas I, Girard L, Caballero-Mellado J (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl Environ Microb 75:6581–6590
Ottesen AR, Peña AG, White JR, Pettengill JB, Li C, Allard S, Rideout S, Allard M, Hill T, Evans P, Strain P, Strain E, Musser S, Knight R, Brown E (2013) Baseline survey of the anatomical microbial ecology of an important food plants: Solanum lycopersicum (tomato). BMC Microbiol 13:114
Patel D, Jha CK, Tank N, Saraf M (2012) Growth enhancement of chickpea in saline soils using plant growth-promoting rhizobacteria. J Plant Growth Regul 31:53–62
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15
Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224
Ribeiro CM, Cardoso EJBN (2012) Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil Pine (Araucaria angustifolia). Microbiol Res 167:69–78
Rijavec T, Lapanje A, Dermastia M, Rupnik M (2007) Isolation of bacterial endophytes from germinated maize kernels. Can J Microbiol 53:802–808
Schallmey M, Singh A, Ward OP (2004) Developments in the use of Bacillus species for industrial production. Can J Microbiol 50:1–17
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Shen M, Kang YJ, Wang HL, Zhang XS, Zhao QX (2012) Effect of plant growth-promoting rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation. J Gen Appl Microbiol 58:253–262
Shi X, Wu Z, Namvar A, Kostrzynska M, Dunfield K, Warriner K (2009) Microbial population profiles of the microflora associated with pre- and postharvest tomatoes contaminated with Salmonella typhimurium or Salmonella montevideo. J Appl Microbiol 107:329–338
Singh MK, Singh DP, Mesapogu S, Babu BK, Bontemps C (2011) Concomitant colonization of nifH positive endophytic Burkholderia sp. in rice (Oryza sativa L.) promotes plant growth. World J Microbiol Biotech 27:2023–2031
Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Lett 296:131–136
Vauterin L, Vauterin P (1992) Computer-aided objective comparison of electrophoresis patterns for grouping and identification of microorganisms. Eur Microbiol 1:37–41
Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J Microbiol 48:559–565
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703
Zhang YF, He LY, Chen ZJ, Zhang WH, Wang QY, Qian M, Sheng XF (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725
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This work was supported by the National Basic Research Program of China (No. 2013CB127106) and the Special Fund for Agro-scientific Research in the Public Interest (No. 200803033).
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Xu, M., Sheng, J., Chen, L. et al. Bacterial community compositions of tomato (Lycopersicum esculentum Mill.) seeds and plant growth promoting activity of ACC deaminase producing Bacillus subtilis (HYT-12-1) on tomato seedlings. World J Microbiol Biotechnol 30, 835–845 (2014). https://doi.org/10.1007/s11274-013-1486-y
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DOI: https://doi.org/10.1007/s11274-013-1486-y