Probiotic activities of Rhizobium laguerreae on growth and quality of spinach

. 2018 Jan 10 ; 8 (1) : 295. [epub] 20180110

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29321563
Odkazy

PubMed 29321563
PubMed Central PMC5762915
DOI 10.1038/s41598-017-18632-z
PII: 10.1038/s41598-017-18632-z
Knihovny.cz E-zdroje

The growing interest in a healthy lifestyle and in environmental protection is changing habits regarding food consumption and agricultural practices. Good agricultural practice is indispensable, particularly for raw vegetables, and can include the use of plant probiotic bacteria for the purpose of biofertilization. In this work we analysed the probiotic potential of the rhizobial strain PEPV40, identified as Rhizobium laguerreae through the analysis of the recA and atpD genes, on the growth of spinach plants. This strain presents several in vitro plant growth promotion mechanisms, such as phosphate solubilisation and the production of indole acetic acid and siderophores. The strain PEPV40 produces cellulose and forms biofilms on abiotic surfaces. GFP labelling of this strain showed that PEPV40 colonizes the roots of spinach plants, forming microcolonies typical of biofilm initiation. Inoculation with this strain significantly increases several vegetative parameters such as leaf number, size and weight, as well as chlorophyll and nitrogen contents. Therefore, our findings indicate, for the first time, that Rhizobium laguerreae is an excellent plant probiotic, which increases the yield and quality of spinach, a vegetable that is increasingly being consumed raw worldwide.

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Saini RK, Ko EY, Keum YS. Minimally processed ready-to-eat baby-leaf vegetables: Production, processing, storage, microbial safety, and nutritional potential. Food Rev. Intern. 2016;33:644–663. doi: 10.1080/87559129.2016.1204614. DOI

Castro-Ibáñez I, Gil MI, Allende A. Ready-to-eat vegetables: Current problems and potential solutions to reduce microbial risk in the production chain. Food Sci. Technol. 2016;85:284–292.

Wadamori Y, Gooneratne R, Hussain MA. Outbreaks and factors influencing microbiological contamination of fresh produce. J. Sci. Food Agric. 2016;97:1396–1403. doi: 10.1002/jsfa.8125. PubMed DOI

Oyinlola LA, Obadina AO, Omemu AM, Oyewole OB. Prevention of microbial hazard on fresh-cut lettuce through adoption of food safety and hygienic practices by lettuce farmers. Food Sci. Nutr. 2016;5:67–75. doi: 10.1002/fsn3.365. PubMed DOI PMC

Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb. Cell Fact. 2014;13:66. doi: 10.1186/1475-2859-13-66. PubMed DOI PMC

Mahanty T, et al. Biofertilizers: a potential approach for sustainable agriculture development. Environ. Sci. Pollut. Res. Int. 2016;24:3315–35. doi: 10.1007/s11356-016-8104-0. PubMed DOI

Berlec A. Novel techniques and findings in the study of plant microbiota: Search for plant probiotics. Plant Sci. 2012;193–194:96–102. doi: 10.1016/j.plantsci.2012.05.010. PubMed DOI

Compant S, Clément C, Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 2010;42:669–78. doi: 10.1016/j.soilbio.2009.11.024. DOI

Flores-Félix JD, et al. Rhizobium as plant probiotic for strawberry production under microcosm conditions. Symbiosis. 2016;67:25–32. doi: 10.1007/s13199-015-0373-8. DOI

Pii Y, et al. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol. Fert. Soils. 2015;51:403–15. doi: 10.1007/s00374-015-0996-1. DOI

Berg G, Eberl L, Hartmann A. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 2005;7:1673–1685. doi: 10.1111/j.1462-2920.2005.00891.x. PubMed DOI

Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 2013;37:634–63. doi: 10.1111/1574-6976.12028. PubMed DOI

García-Fraile P, et al. Rhizobium promotes non-legumes growth and quality in several production steps: Towards a biofertilization of edible raw vegetables healthy for humans. PLoS ONE. 2012;7:e38122. doi: 10.1371/journal.pone.0038122. PubMed DOI PMC

Olivares J, Bedmar EJ, Sanjuán J. Biological Nitrogen Fixation in the Context of Global Change. Mol. Plant Microbe. Interact. 2013;26:486–94. doi: 10.1094/MPMI-12-12-0293-CR. PubMed DOI

Chabot R, Antoun H, Cescas MP. Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil. 1996;184:311–21. doi: 10.1007/BF00010460. DOI

Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF. Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can. J. Microbiol. 1996;42:279–83. doi: 10.1139/m96-040. PubMed DOI

Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R. Potential of Rhizobium and Bradyrhizobium species as growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.) Plant Soil. 1998;204:57–67. doi: 10.1023/A:1004326910584. DOI

Peix A, et al. Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol. Biochem. 2001;33:103–10. doi: 10.1016/S0038-0717(00)00120-6. DOI

Yanni YG, et al. The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Australian J. Plant. Physiol. 2001;28:845–70.

Flores-Félix JD, et al. Use of Rhizobium leguminosarum as a potential biofertilizer for Lactuca sativa and Daucus carota crops. J. Plant Nutr. Soil Sci. 2013;176:876–82. doi: 10.1002/jpln.201300116. DOI

Granada CE, et al. Diversity of native rhizobia isolated in south Brazil and their growth promotion effect on white clover (Trifolium repens) and rice (Oryza sativa) plants. Biol. Fert. Soils. 2014;50:123–32. doi: 10.1007/s00374-013-0840-4. DOI

Karthik C, Oves M, Sathya K, Ramkumar VS, Arulselvi PI. Isolation and characterization of multi-potential Rhizobium strain ND2 and its plant growth-promoting activities under Cr(VI) stress. Arch. Agron. Soil Sci. 2017;63:1058–1069. doi: 10.1080/03650340.2016.1261116. DOI

Höflich G, Wiehe W, Kühn G. Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experientia. 1994;50:897–905. doi: 10.1007/BF01923476. DOI

Alami Y, Achouak W, Marol C, Heulin T. Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl. Environ. Microbiol. 2000;66:3393–3398. doi: 10.1128/AEM.66.8.3393-3398.2000. PubMed DOI PMC

Gutiérrez-Zamora ML, Martínez-Romero E. Natural endophytic association between Rhizobium etli and maize (Zea mays L.) J. Biotechnol. 2001;91:117–26. doi: 10.1016/S0168-1656(01)00332-7. PubMed DOI

Mishra RP, Singh RK, Jaiswal HK, Kumar V, Maurya S. Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.) Curr Microbiol. 2006;52:383–9. doi: 10.1007/s00284-005-0296-3. PubMed DOI

Schwedhelm C, Boeing H, Hoffmann G, Aleksandrova K, Schwingshackl L. Effect of diet on mortality and cancer recurrence among cancer survivors: a systematic review and meta-analysis of cohort studies. Nutr, Rev. 2016;74:737–48. doi: 10.1093/nutrit/nuw045. PubMed DOI PMC

Ndanuko RN, Tapsell LC, Charlton KE, Neale EP, Batterham MJ. Dietary Patterns and Blood Pressure in Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Adv. Nutr. 2016;7:76–89. doi: 10.3945/an.115.009753. PubMed DOI PMC

Medina-Remón A, Kirwan R, Lamuela-Raventós RM, Estruch R. Dietary Patterns and the Risk of Obesity, Type 2 Diabetes Mellitus, Cardiovascular Diseases, Asthma, and Mental Health Problems. Crit. Rev. Food Sci. Nutr. 2016;19:1–35. doi: 10.1080/10408398.2016.1158690. PubMed DOI

Martínez-González MA, Martín-Calvo N. Mediterranean diet and life expectancy; beyond olive oil, fruits, and vegetables. Curr. Opin. Clin. Nutr. Metab. Care. 2016;19:401–407. doi: 10.1097/MCO.0000000000000316. PubMed DOI PMC

Schwingshackl L, Hoffmann G. Does a Mediterranean-Type Diet Reduce Cancer Risk? Curr. Nutr. Rep. 2016;5:9–17. doi: 10.1007/s13668-015-0141-7. PubMed DOI PMC

Hariharan D, Vellanki K, Kramer H. The Western Diet and Chronic Kidney Disease. Curr. Hypertens Rep. 2015;17:3–16. doi: 10.1007/s11906-014-0529-6. PubMed DOI

Di Daniele N, et al. Impact of Mediterranean diet on metabolic syndrome, cancer and longevity. Oncotarget. 2017;8:8947–79. PubMed PMC

Petersson SD, Philippou E. Mediterranean diet, cognitive function, and dementia: A systematic review of the evidence. Adv. Nutr. 2016;7:889–904. doi: 10.3945/an.116.012138. PubMed DOI PMC

Yoon YE, et al. Influence of cold stress on contents of soluble sugars, vitamin C and free amino acids including gamma-aminobutyric acid (GABA) in spinach (Spinacia oleracea) Food Chem. 2017;215:185–192. doi: 10.1016/j.foodchem.2016.07.167. PubMed DOI

FAOSTAT. Crops data for 2011. Food and Agricultural Organization of the United Nations. http://faostat3.fao.org (2013).

Çakmakçı R, Erat M, Erdoğan Ü, Dönmez MF. The influence of plant growth–promoting rhizobacteria on growth and enzyme activities in wheat and spinach plants. J. Plant Nutr. Soil Sci. 2007;170:288–95. doi: 10.1002/jpln.200625105. DOI

Thilakarathna MS, Raizada MN. A meta-analysis of the effectiveness of diverse rhizobia inoculants on soybean traits under field conditions. Soil Biol. Biochem. 2017;105:177–196. doi: 10.1016/j.soilbio.2016.11.022. DOI

Bashan Y, de-Bashan LE, Prabhu SR, Hernández JP. Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013) Plant Soil. 2014;378:1–33. doi: 10.1007/s11104-013-1956-x. DOI

Kuykendall, L. D., Young, J. M., Martínez-Romero, E., Kerr, A. & Sawada, H. Rhizobium in Bergey’s Manual of Systematics ofArchaea and Bacteria (ed. John Wiley & Sons.) 1–36 (2015).

Saïdi S, et al. Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int. J. Syst. Evol. Microbiol. 2014;64:242–7. doi: 10.1099/ijs.0.052191-0. PubMed DOI

Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ. O-CAS, a fast and universal method for siderophore detection. J. Microbiol. Meth. 2007;70:127–131. doi: 10.1016/j.mimet.2007.03.023. PubMed DOI

Robledo M, et al. Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces. Microb Cell Fact. 2012;11:125. doi: 10.1186/1475-2859-11-125. PubMed DOI PMC

Jiménez-Gómez, A. et al. Effective Colonization of Spinach Root Surface by Rhizobium in Biological Nitrogen Fixation and Beneficial Plant-Microbe Interaction. (ed. González-Andrés, A. & James, E.) 109–122 (Germany, 2016).

Zhang YM, Tian CF, Sui XH, Chen WF, Chen WX. Robust markers reflecting phylogeny and taxonomy of rhizobia. PLoS One. 2012;7:e44936. doi: 10.1371/journal.pone.0044936. PubMed DOI PMC

Rouhrazi, K., Khodakaramian, G., & Velázquez, E. Phylogenetic diversity of rhizobial species and symbiovars nodulating Phaseolus vulgaris in Iran. FEMS microbiol letters. 363(5) (2016). PubMed

Lugtenberg B, Kamilova F. Plant-Growth-Promoting Rhizobacteria. Annu. Rev. Microbiol. 2009;63:541–556. doi: 10.1146/annurev.micro.62.081307.162918. PubMed DOI

Khalid A, Arshad M, Zahir ZA. Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 2004;96:473–80. doi: 10.1046/j.1365-2672.2003.02161.x. PubMed DOI

Crozier A, Arruda P, Jasmin JM, Monteiro AM, Sandberg G. Analysis of indole-3-acetic acid and related indoles in culture medium from Azospirillum lipoferum and Azospirillum brasilense. App. Environ. Microb. 1988;54:2833–2837. PubMed PMC

Fuentes-Ramírez L, Jiménez-Salgado T, Abarca-Ocampo IR, Caballero-Mellado J. Acetobacter diazotrophicus, an indoleacetic acid producing bacterium isolated from sugarcane cultivars of Mexico. Plant Soil. 1993;154:145–150. doi: 10.1007/BF00012519. DOI

Dernini S, et al. Med Diet 4.0: the Mediterranean diet with four sustainable benefits. Public Health Nutr. 2016;22:1–9. PubMed PMC

Flores-Félix J.D., et al. MALDI-TOFFMS, a tool for diversity analysis and detection of novel rhizobial species nodulating Phaseolus vulgaris. Microorganisms for future agriculture. Spain: Spanish Society of Nitrogen Fixation (SEFIN), Latin American Society Rhizobiology (ALAR) and University of Sevilla. 25–26 (2013).

Gaunt MW, Turner SL, Rigottier-Gois L, Lloyd-Macgilp SA, Young JWP. Phylogenies of atpD and recA support the small subunit rRNA-based classification of rhizobia. Int. J. Syst. Evol. Microbiol. 2001;51:2037–2048. doi: 10.1099/00207713-51-6-2037. PubMed DOI

Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980;16:111–120. doi: 10.1007/BF01731581. PubMed DOI

Saitou N, Nei M. A neighbour-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol. 1987;44:406–25. PubMed

Tamura K, et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. PubMed DOI PMC

Pikovskaya RI. Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologiya. 1948;17:362–370.

Nautiyal CS. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbial Lett. 1999;170:265–270. doi: 10.1111/j.1574-6968.1999.tb13383.x. PubMed DOI

Schwyn B, Neilands JB. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987;160:47–56. doi: 10.1016/0003-2697(87)90612-9. PubMed DOI

Alexander DB, Zuberer DA. Use of Chrome Azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol. Fertil. Soils. 1991;12:39–45. doi: 10.1007/BF00369386. DOI

Vincent, J. M. The cultivation, isolation and maintenance of rhizobia in A Manual for the Practical Study of Root-Nodule (ed. Vicent, J. M.) 1–13 (Oxford, 1970).

O’Hara GW, Goss TJ, Dilworth MJ, Glenn AR. Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl. Environ Microbiol. 1989;55:1870–1876. PubMed PMC

Diez-Méndez A, Rivas R. Improvement of saffron production using Curtobacterium herbarum as a bioinoculant under greenhouse conditions. Aims Microbiol. 2017;3:354–364. doi: 10.3934/microbiol.2017.3.354. PubMed DOI PMC

Wang H, Zhong Z, Cai T, Li S, Zhu J. Heterologous overexpression of quorum-sensing regulators to study cell-density-dependent phenotypes in a symbiotic plant bacterium Mesorhizobium huakuii. Arch. Microbiol. 2004;182:520–525. doi: 10.1007/s00203-004-0735-8. PubMed DOI

O’Toole GA, et al. Genetic approaches to study of biofilms. Method enzymol. 1999;310:91–109. doi: 10.1016/S0076-6879(99)10008-9. PubMed DOI

Fujishige NA, Kapadia NN, De Hoff PL, Hirsch A. Investigations of Rhizobium biofilm formation. FEMS Microbiol. Ecol. 2006;56:195–206. doi: 10.1111/j.1574-6941.2005.00044.x. PubMed DOI

Cheng HP, Walker GC. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 1998;180:5183–5191. PubMed PMC

Simon, R., Priefer, U. & Puhler, A. Vector plasmids for in vivo and in vitro manipulations of gram negative bacteria in Molecular Genetics of the Bacteria-Plant Interaction (ed. Puhler, A.) 98–106 (Berlín, 1983).

O’gara F, Shanmugam KT. Control of symbiotic nitrogen fixation in rhizobia. Regulation of NH4+ assimilation. Biochem Biophys. Acta. 1976;451:342–352. doi: 10.1016/0304-4165(76)90129-X. PubMed DOI

Beringer JE. R factors transfer in Rhizobium leguminosarum. J. Gen Microbiol. 1974;84:188–98. PubMed

Shahzad SM, Arif MS, Riaz M, Iqbal Z, Ashraf M. PGPR with varied ACC-deaminase activity induced different growth and yield response in maize (Zea mays L.) under fertilized conditions. Eur. J. Soil Biol. 2013;57:27–34. doi: 10.1016/j.ejsobi.2013.04.002. DOI

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