Abstract
There is increasing interest in the use of plant growth-promoting rhizobacteria (PGPR) as environmental-friendly and healthy biofertilizers. Strawberries (Fragraria x ananassa) are mainly consumed fresh and hence any PGPRs used for biofertilization must be safe for humans, which is the case for members of the genus Rhizobium. In this study, the effects of inoculation of strawberry plants with Rhizobium sp. strain PEPV16, which belongs to the phylogenetic group of R. leguminosarum, and whose plant growth promotion ability has been reported previously for lettuce (Lactuca sativa) and carrots (Daucus carota), was examined. The results demonstrated that PEPV16 promotes strawberry growth through significant increases in the number of stolons, flowers and fruits as compared with uninoculated controls. Compared to uninoculated controls, the fruits of the inoculated plants had higher concentrations of Fe, Zn, Mn and Mo, and they also had higher concentrations of organic acids, such as citric and malic acid, and lower amounts of ascorbic acid than fruits. Although decreases in ascorbic acid have previously been described after the inoculation of strawberry with strains from different PGPR genera, this is the first study to report increases in organic acids after PGPR inoculation.
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References
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Basu A, Nguyen A, Betts NM, Lyons TJ (2014) Strawberry as a functional food: an evidence-based review. Crit Rev Food Sci Nutr 54:790–806
Berlec A (2012) Novel techniques and findings in the study of plant microbiota: search for plant probiotics. Plant Sci 193–194:96–102
Bona E, Lingua G, Manassero P et al (2015) AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels. Mycorrhiza 25:181–193
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
Dopico-García MS, Valentão P, Guerra L et al (2007) Experimental design for extraction and quantification of phenolic compounds and organic acids in white “Vinho Verde” grapes. Anal Chim Acta 583:15–22
Erturk Y, Ercisli S, Cakmakci R (2012) Yield and growth response of strawberry to plant growth-promoting rhizobacteria inoculation. J Plant Nutr 35:817–826
Esitken A, Yildiz HE, Ercisli S et al (2010) Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic (Amsterdam) 124:62–66
Ferreira L, Sánchez-Juanes F, García-Fraile P et al (2011) MALDI-TOF mass spectrometry is a fast and reliable platform for identification and ecological studies of species from family Rhizobiaceae. PLoS One 6, e20223
Flores-Félix JD, Menéndez E, Rivera LP et al (2013) Use of Rhizobium leguminosarum as a potential biofertilizer for Lactuca sativa and Daucus carota crops. J Plant Nutr Soil Sci 176:876–882
Flores-Félix JD, Menéndez E, Marcos-García M et al (2015a) Calcofluor white, an alternative to propidium iodide for plant tissues staining in studies of root colonization by fluorescent-tagged rhizobia. J Adv Biol Biotechonol 2:65–70
Flores-Félix JD, Silva LR, Rivera LP et al (2015b) Plants probiotics as a tool to produce highly functional fruits: the case of Phyllobacterium and vitamin C in strawberries. PLoS One 10, e0122281
García-Fraile P, Carro L, Robledo M et al (2012) Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One 7, e38122
García-Fraile P, Silva LR, Sánchez-Márquez S et al (2013) Plums (Prunus domestica L.) are a good source of yeasts producing organic acids of industrial interest from glycerol. Food Chem 139:31–34
Gaunt MW, Turner SL, Rigottier-Gois L et al (2001) Phylogenies of atpD and recA support the small sub- unit rRNA-based classification of rhizobia. Int J Syst Evol Microbiol 51:2037–2048.
Giampieri F, Tulipani S, Alvarez-Suarez JM et al (2012) The strawberry: composition, nutritional quality, and impact on human health. Nutrition 28:9–19
Giampieri F, Forbes-Hernandez TY, Gasparrini M et al (2015) Strawberry as a health promoter: an evidence based review. Food Funct 6:1386–1398
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:15
Heide OM, Stavang JA, Sønsteby A (2013) Physiology and genetics of flowering in cultivated and wild strawberries - A review. J Hortic Sci Biotechnol 88:1–8
Ipek M, Pirlak L, Esitken A et al (2014) Plant Growth-Promoting Rhizobacteria (PGPR) increase yield, growth and nutrition of strawberry under high-calcareous soil conditions. J Plant Nutr 37:990–1001
Jiao YS, Yan H, Ji ZJ et al (2015) Rhizobium sophorae sp. nov. and Rhizobium sophoriradicis sp. nov., nitrogen-fixing rhizobial symbionts of the medicinal legume Sophora flavescens. Int J Syst Evol Microbiol 65:497–503
Kaiser BN, Gridley KL, Ngaire Brady J et al (2005) The role of molybdenum in agricultural plant production. Ann Bot 96:745–754
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kumar N, Lad G, Giuntini E et al (2015) Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum. Open Biol 5:140133
López-Aranda JM, Soria C, Santos BM et al (2011) Strawberry production in mild climates of the world: a review of current cultivar use. Int J Fruit Sci 11:232–244
Lugtenberg BJJ, Dekkers LC, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490
Mendel RR, Schwarz G (2011) Molybdenum cofactor biosynthesis in plants and humans. Coord Chem Rev 255:1145–1158
Peix A, Ramírez-Bahena MH, Velázquez E, Bedmar EJ (2015) Bacterial associations with legumes. Crit Rev Plant Sci 34:17–42
Pirlak L, Köse M (2009) Effects of plant growth promoting rhizobacteria on yield and some fruit properties of strawberry. J Plant Nutr 32:1173–1184
Robledo M, Jiménez-Zurdo JI, Velázquez E et al (2008) Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. PNAS 105:7064–7069. doi:10.1073/pnas.0802547105
Robledo M, Rivera L, Jiménez-Zurdo JI et al (2012) Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces. Microb Cell Fact 11:125
Román-Ponce B, Zhang YJ, Vásquez-Murrieta MS et al (2015) Rhizobium acidisoli sp. nov., isolated from root nodules of Phaseolus vulgaris in acid soils in Mexico. Int J Syst Evol Microbiol. doi:10.1099/ijsem.0.000732
Saïdi S, Ramírez-Bahena MH, Santillana N et al (2014) Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int J Syst Evol Microbiol 64:242–247
Saitou N, Nei M (1987) A neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 44:406–425
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tulipani S, Armeni T, Giampieri F et al (2014) Strawberry intake increases blood fluid, erythrocyte and mononuclear cell defenses against oxidative challenge. Food Chem 156:87–93
Wei GH, Wang ET, Tan ZY et al (2002) Rhizobium indigoferae sp. nov. and Sinorhizobium kummerowiae sp. nov., respectively isolated from Indigofera spp. and Kummerowia stipulacea. Int J Syst Evol Microbiol 52:2231–2239
Zhang YJ, Zheng WT, Everall I et al (2015) Rhizobium anhuiense sp. nov., isolated from effective nodules of Vicia faba and Pisum sativum grown in Southern China. Int J Syst Evol Microbiol 65:2960–2967
Acknowledgments
This work was sponsored by the “Junta de Castilla y León” (Grant SA183A11-2), MINECO (Grant AGL2011-29227) and by the “Fundação para a Ciência e a Tecnologia”–FCT (PEst-C/SAU/UI0709/2014). Co-funded by the Fundo Europeu de Desenvolvimento Regional - FEDER via the Programa Operacional Factores de Competitividade-COMPETE/QREN. PGF is the recipient of a postdoctoral researcher contract from the Academy of Sciences of the Czech Republic. JDFF, MMG and EM were supported by PhD fellowships from the University of Salamanca, the “Miguel Casado San José” foundation, and MICINN, respectively. LRS acknowledges FCT for a Post-doc Grant (SFRH/BPD/105263/2014). The authors thank Nicholas Skinner for English corrections.
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Flores-Félix, JD., Marcos-García, M., Silva, L.R. et al. Rhizobium as plant probiotic for strawberry production under microcosm conditions. Symbiosis 67, 25–32 (2015). https://doi.org/10.1007/s13199-015-0373-8
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DOI: https://doi.org/10.1007/s13199-015-0373-8