Abstract
The effects of boron and plant growth promoting bacteria (Bio-B) on the some of physiological parameters with amino acid and organic acid of strawberry cv. Fern were investigated under field conditions. The study treatments were soil, foliar, and soil + foliar applications as main plot and two Bio-B (control and plant growth promoting rhizobacteria; Azospirillum brasilense 1 × 109 cfu ml−1 + 10% boron as Di-SodyumOktaboratTetraHidrat) fertilizer applications as subplot in complete randomized block design with four replicates. Bio-B fertilizer was applied in three methods such as soil, foliar and soil + foliar application methods on strawberry. Two years data from the present study reported that the use of Bio-B significantly increased chlorophyll, photosynthesis, stomatal and membrane permeability, amino acid and organic acid of strawberry leaf. Soil + foliar applications of Bio-B fertilizer increased to strawberry yield compared to the control by 65.9%. Foliar applications of Bio-B fertilizer increased chlorophyll and stomatal permeability in comparison to the control by 17.62 and 56.52%, respectively. However, soil + foliar application of Bio-B fertilizer increased membrane permeability and photosynthesis compare to those under the control 24.80 and 23.32%, respectively. Amino acid content of strawberry was increased (23.45%) and organic acid amount was increased (23.45%) under soil application of Bio-B fertilizer compare to those under the control. The results of this study concluded that Bio-B fertilizer application was positively associated with strawberry yield and increased the potential to chlorophyll, photosynthesis, stomatal and membrane permeability, amino acid, organic acid content under field conditions.
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Adesemoye AO, Obini M, Ugoji EO (2008) Comparison of plant growth promotion with Pseudomonas aeruginosa and Bacillus subtilis in three vegetables. Brazilian. J Microbiol 39:423–426
Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B (2007) Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol Lett 274:10–217
Antoine FR, Wei CI, Littell RC, Marshall MR (1999) HPLC method for analysis of free amino acids in fish using o‑phthaldialdehyde precolumn derivatization. J Agr Food Chem 47:5100–5107
Aristoy MC, Toldra F (1991) Deproteinization techniques for HPLC amino acid analysis in fresh pork muscle and dry-cured ham. J Agric Food Chem 39:1792–1795
Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16
Belitz HD, Grosch W, Schieberle P (2001) Lehrbuch der Lebensmittelchemie: 1.2 Aminosäuren, 5th edn. Springer, Berlin, pp 9–33
Borgen A (2004) Strategies for regulation of seed borne diseases in organic farming. Seed Test Int 127:19–21
Borgen A, Kristensen L (2001) Effect of seed treatment with acetic acid in control of seed borne diseases. In: Biddle AJ (ed) Proceedings from BCPC symposium no. 76: “seed treatment: challenges & opportunities”. BCPC, Farnham, pp 135–140
Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503
Bremner JM (1996) Nitrogen-total. In: Bartels JM, Bigham JM (eds) Chemical methods. Methods of soil analysis, vol 3. The Soil Science Society of America and the American Society of Agronomy, Madison, pp 1085–1121
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community com- position and diversity. Appl Environ Microbiol 74:738–744
Camacho-Cristóbal JJ, Lunar L, Lafont F, Baumert A, González-Fontes A (2004) Boron deficiency causes accumulation of chlorogenic acid and caffeoyl polyamine conjugates in tobacco leaves. J Plant Physiol 161:879–881
Chen FX, Liu XH, Chen LS (2005) Advances in research on organic acid metabolism in fruits. J Fruit Sci 22:526–531
Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo J, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85:418–430
Cordenunsi BR, Nascimento JRO, Lajolo FM (2003) Physico-chemical changes related to quality of five strawberry fruit cultivars during cool-storage. Food Chem 83:167–173
Cordenunsi BR, Genovese MI, Nascimiento JRO, Hassimoto NMA, Santos RJ, Lajolo FM (2005) Effects of temperature on the chemical composition and antioxidant capacity of three strawberry cultivars. Food Chem 91:113–121
El-Shintinawy F (1999) Structural and functional damage caused by boron deficiency in sunflower leaves. Photosynthetica 36:565–573
Esitken A, Karlidag H, Ercisli S, Sahin F (2002) Effects of foliar application of Bacillus substilis Osu-142 on the yield, growth and control of shot-hole disease Coryneum blight of apricot. Gartenbauwissenschaft 67:139–142
Esitken A, Karlidag H, Ercisli S, Turan M, Sahin F (2003) The effect of spraying a growth promoting bacterium on the yield, growth and nutrient element composition of leaves of apricot Prunus armeniaca L. cv. Hacihaliloglu. Aust J Agric Res 54:377–380
Esitken A, Yildiz HE, Ercisli S, Donmez MF, Turan M, Gunes A (2010) Effects of plant growth promoting bacteria PGPB on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic 124:62–66
Fattah GM, Mohamedin AH (2000) Interactions between a vesicular-arbuscular mycorrhizal fungus Glomus intraradices and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401–409
Galili G, Höfgen R (2002) Metabolic engineering of amino acids and storage proteins. Metab Eng 4:3–11
Gao ZQ, Zhao CX, Cheng JJ, Zhang XC (2012) Tree structure and 3‑D distribution of radiation in canopy of apple trees with different canopy structures in China. Chin J Eco Agric 201:63–68
Giridara KS, Matta RA (2003) NaCl effects on proline metabolism in two high yielding genotypes of mulberry Morus alba L. with contrasting salt tolerance. Plant Sci 165:1245–1251
Gunes A, Ataoglu N, Turan M, Esitken A, Ketterings QM (2009) Effects of phosphate-solubilizing microorganisms on strawberry yield and nutrient concentrations. J Plant Nutr Soil Sci 172:385–392
Han S, Chen L, Jiang H, Smith BR, Yang L, Xie C (2008) Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol 165:1331–1341
Henderson JW, Ricker RD, Bidlingmeyer BA, Woodward C (1999) Amino acid analysis using Zorbax Eclipse-AAA Columns and the Agilent 1200 HPLC. Rapid, Accurate, Sensitive, and Reproducible HPLC Analysis of Amino Acids. Agilent Technologies, Part No. 5980–1193E
Keutgen AJ, Pawelzik E (2008) Quality and nutritional value of strawberry fruit under long term salt stress. Food Chem 1074:1413–1420
Li H, Li TX, Fu G, Katulanda P (2013) Induced leaf intercellular CO2, photosynthesis, potassium and nitrate retention and strawberry early fruit formation under macronutrient limitation. Photosynth Res 115(2-3):101–114
Lindemann B (2001) Receptors and transduction in taste. Nature 413:219–225
Lindsay WL, Norvell WA (1978) Development of DTPA soil test for zinc, iron, manganese and copper. Soil Sci Soc Am J 42:421–428
Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizo- sphere. Eur J Soil Biol 47:374–379
Lizot JF, Griboval B, Guenard M (2002) Mise au point dune technique de disinfection des semences applicable en agriculture biologique—Alternaria dauci sur semences de carottes. In: 2ème Conference internationale sur les moyens alternatifs de lutte contre les organisms nuisibles aux vegetaux Lille. vol 4
Lopes da Silva SF, Escribano BMT, Perez AJJ, Rivas GJC, Santos BC (2007) Anthocyanin pigments in strawberry. LWT Food Sci Technol 40:374–382
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London
Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208
Massonnet C, Regnard JL, Lauri PÉ, Costes E, Sinoquet H (2008) Contributions of foliage distribution and leaf functions to light interception, transpiration and photosynthetic capacities in two apple cultivars at branch and tree scales. Tree Physiol 28:665–678
Matsubara Y, Ishigaki T, Koshikawa K (2009) Changes in free amino acid concentrations in mycorrhizal strawberry plants. Sci Hortic 119:392–396
McLean EO (1982) Soil pH and lime requirement. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, 2nd edn. Chemical and microbiological properties, vol 2. ASA SSSA Publisher, Madison, pp 199–224
Micallef SA, Channer S, Shiaris MP, Colon CA (2009) Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal Behav 4:777–780
Mukhopadhayay M, Ghosh P, Mondal TK (2013) Effect of boron deficiency on photosynthesis and antioxidant responses of young Tea Plantlets. Редколлегия 5:671–677
Nelson DW, Sommers LE (1982) Organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, 2nd edn. Chemical and microbiological properties, vol 2. ASA SSSA Publisher, Madison, pp 574–579
Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJP, Zucker CS (2002) An amino-acid taste receptor. Nature 416:199–202
Nezarat S, Gholami A (2009) Screening plant growth promoting rhizobacteria for improving seed germination, transplant growth and yield of maize. Pakistan. J Biol Sci 121:26–32
Návarová H, Bernsdorff F, Döring AC, Zeier J (2012) Pipecolic acid, an endogenous mediator of de-fense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA, Washington, DC (Circ 939)
Orhan E, Esitken A, Ercisli S, Turan M, Sahin F (2006) Effects of plant growth promoting rhizobacteria PGPR on yield, growth and nutrient contents in organically growing raspberry. Sci Hortic 111:38–43
Pandey DK, Pandey N (2008) Screening of wheat genotypes for their susceptibility to boron deficiency. Res Environ Life Sci 1:37–42
Rhoades JD (1996) Salinity: electrical conductivity and total dissolved solids. In: Bartels JM, Bigham JM (eds) Chemical methods, 2nd edn. Methods of soil analysis, vol 3. ASA SSSA Publisher Agronomy, Madison, pp 417–436
Ricke SC (2003) Perspectives on the use of organic acids and short chain fatty acids as microbials. Poult Sci 82:632–639
Rolin D, Pfeffer PE, Douds DD, Farrell HM, Shachar Y (2001) Arbuscular mycorrhizal symbiosis and phosphorus nutrition: effects on amino acid production and turnover in leek. Symbiosis 30:1–14
Saia S, Ruisi P, Fileccia V, DiMiceli G, Amato G, Martinelli F (2015) Metabolomics suggests that soil inoculation with arbuscular mycorrhizal fungi decreased free amino acid content in roots of durum wheat grown under N‑limited, P‑rich field conditions. PLoS ONE. https://doi.org/10.1371/journal.pone.0129591
Sawicka B, Michałek W (2008) Photosynthetic activity of Helianthus tuberosus L. depending on a soil and mineral fertilization. Pol J Soil Sci 41:209–222
Sharma RR, Patel VB, Krishna H (2006) Relationship between light, fruit and leaf mineral content with albinism incidence in strawberry Fragaria x ananassa Duch. Sci Hortic 1091:66–70
Shaukat K, Affrasayab S, Hasnain S (2006a) Growth responses of Heliantus annus to plant growth promoting rhizobacteria used as a biofertilizer. J Agric Res 1:573–581
Shaukat K, Affrasayab S, Hasnain S (2006b) Growth responses of Triticum aestivum to plant growth promoting rhizobacteria used as a biofertilizer. Res J Microbiol 1:330–338
Shi L, Chen B, Wang Z, Elias DA, Mayer MU, Gorby YA (2006) Isolation of high-affinity functional protein complex between OmcA and MtrC two outer membrane decaheme c‑type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 188:4705–4714
Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. Microbiol Ecol 45:219–227
Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190
Sudhakar P, Chattopadhyay GN, Gangwar SK, Ghosh JK (2000) Effect of foliar application of Azotobacter, Azospirillum and Beijerinckia on leaf yield and quality of mulberry Morus alba. J Agric Sci 134:227–234
Sumner ME, Miller WP (1996) Cation exchange capacity and ex-change coefficients. In: Chemical methods, 2nd edn. Methods of Soil Analysis, vol 3. ASA SSSA Publisher, Madison, pp 1201–1230
Thomas GW (1982) Exchangeable cations. In: Page AL, Miller RH, Keeney DR (eds) Methods of Soil Analysis, 2nd edn. Chemical and microbiological properties, vol 2. ASA SSSA Publisher, Madison, pp 159–164
Thomson VP, Cunningham SA, Ball MC, Nicotra AB (2003) Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia 134:167–175
Turan M, Gulluce M, Von Wiren N, Sahin F (2012) Yield promotion and phosphorus solubilization by plant promoting rhizobacteria in extensive wheat production. J Plant Nutr Soil Sci 175:818–826
Turan M, Ekinci M, Yildirim E, Gunes A, Karagoz K, Kotan R, Dursun A (2014) Plant growth-promoting rhizobacteria improved growth, nutrient, and hormone content of cabbage Brassica oleracea seedlings. Turk J Agric For 38:327–333
Vranova V, Rejsek K, Skene KR, Formanek P (2011) Nonprotein amino acids: plant, soil and ecosystem interactions. Plant Soil 342:31–48
White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105(7):1073–1080
Wojcik P, Lewandowski M (2003) Effect of spray of calcium and boron on yield and quality of “Elsanta” strawberry. J Plant Nutr 3:671–682
Wolf B (1974) Improvements in the azomethine-H method for the determining of boron. Commun Soil Sci Plant Anal 5:39–44
Yamaya T, Matsumoto H (1989) Accumulation of asparagines in NaCl-stressed barley seedlings. Reports of the Ohara Institute for Agricultural Biology, Okayama University 19, pp 181–188
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We are grateful to the Research and Development project of Turkish Ministry of Industry (Project number: 01194.STZ.2012-1) for their generous financial support of this study.
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N. Kitir, A. Gunes, M. Turan, E. Yildirim, B. Topcuoglu, M. Turker, E. Ozlu, M.R. Karaman and G. Fırıldak declare that they have no competing interests.
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Kitir, N., Gunes, A., Turan, M. et al. Bio-Boron Fertilizer Applications Affect Amino Acid and Organic Acid Content and Physiological Properties of Strawberry Plant. Erwerbs-Obstbau 61, 129–137 (2019). https://doi.org/10.1007/s10341-018-0409-3
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DOI: https://doi.org/10.1007/s10341-018-0409-3