Metabolic changes occurring in white lupine grain were investigated in response to Plant Growth Promoting Rhizobacteria (PGPR) root inoculation under field condition. We precisely targeted lipids and phenolics changes occurring in white lupine grain in response to Pseudomonas brenneri LJ215 and/or Paenibacillus glycanilyticus LJ121 inoculation. Lipids and phenolic composition were analyzed using an Ultra High‐Performance Liquid Chromatography/Tandem Mass Spectrometry Methods. As compared to grain of un-inoculated control plant, Paenibacillus glycaniliticus inoculation highly increased the total lipids content (from 232.55 in seeds of un-inoculated control plant to 944.95 mg/kg) and the relative percentage of several fatty acid such as oleic acid (+20.95%) and linoleic acid (+14.28%) and decreased the relative percentage of glycerophospholipids (− 13.11%), sterol (− 0.2% and − 0.34% for stigmasterol and campesterol, respectively) and prenol (− 17.45%) class. Paenibacillus glycaniliticus inoculation did not affect total phenolic content, while it modulated content of individual phenolic compounds and induced the accumulation of “new” phenolics compounds such as kaempferol. Paenibacillus glycanilyticus LJ121 can be a useful bio-fertilizer to enhance nutritional quality of white lupine grain.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol. https://doi.org/10.3389/fmicb.2017.00971
Ballard CR, Maróstica MR (2019) Health benefits of flavonoids. Bioactive compounds. Elsevier, Amsterdam, pp 185–201
Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478
Borek S, Pukacka S, Michalski K, Ratajczak L (2009) Lipid and protein accumulation in developing seeds of three lupine species: Lupinus luteus L., Lupinus albus L., and Lupinus mutabilis Sweet. J Exp Bot 60:3453–3466. https://doi.org/10.1093/jxb/erp186
Borek S, Ratajczak W, Ratajczak L (2015) Regulation of storage lipid metabolism in developing and germinating lupin (Lupinus spp) seeds. Acta Physiol Plant 37:119. https://doi.org/10.1007/s11738-015-1871-2
Cabello-Hurtado F, Keller J, Ley J et al (2016) Proteomics for exploiting diversity of lupin seed storage proteins and their use as nutraceuticals for health and welfare. J Proteomics 143:57–68. https://doi.org/10.1016/j.jprot.2016.03.026
Cipriano MAP, Lupatini M, Lopes-Santos L et al (2016) Lettuce and rhizosphere microbiome responses to growth promoting Pseudomonas species under field conditions. FEMS Microbiol Ecol 92:197. https://doi.org/10.1093/femsec/fiw197
Comte G, Martens S (2013) Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20. https://doi.org/10.1016/J.PLAPHY.2013.05.009
Couto C, Silva LR, Valentão P et al (2011) Effects induced by the nodulation with Bradyrhizobium japonicum on Glycine max (soybean) metabolism and antioxidant potential. Food Chem 127:1487–1495. https://doi.org/10.1016/j.foodchem.2011.01.135
Covas M-I (2007) Olive oil and the cardiovascular system. Pharmacol Res 55:175–186. https://doi.org/10.1016/j.phrs.2007.01.010
Dal Cortivo C, Barion G, Ferrari M et al (2018) Effects of field inoculation with VAM and bacteria consortia on root growth and nutrients uptake in common wheat. Sustainability 10:3286
Daur I, Saad MM, Eida AA et al (2018) Boosting alfalfa (Medicago sativa L) production with rhizobacteria from various plants in Saudi Arabia. Front Microbiol 9:477. https://doi.org/10.3389/fmicb.2018.00477
Della Corte A, Chitarrini G, Di Gangi IM et al (2015) A rapid LC–MS/MS method for quantitative profiling of fatty acids, sterols, glycerolipids, glycerophospholipids and sphingolipids in grapes. Talanta 140:52–61. https://doi.org/10.1016/j.talanta.2015.03.003
Ferchichi N, Toukabri W, Boularess M et al (2019) Isolation, identification and plant growth promotion ability of endophytic bacteria associated with lupine root nodule grown in Tunisian soil. Arch Microbiol. https://doi.org/10.1007/s00203-019-01702-3
Fontanari GG, Kobelnik M, Marques MR et al (2018) Thermal and kinetic studies of white lupin (Lupinus albus) oil. J Therm Anal Calorim 131:775–782. https://doi.org/10.1007/s10973-017-6468-0
Fritz C, Palacios-Rojas N, Feil R, Stitt M (2006) Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J 46:533–548. https://doi.org/10.1111/j.1365-313X.2006.02715.x
Gao M, Zhou JJ, Wang ET et al (2015) Multiphasic characterization of a plant growth promoting bacterial strain, Burkholderia sp. 7016 and its effect on tomato growth in the field. J Integr Agric 14:1855–1863
Hamama AA, Bhardwaj HL (2004) Phytosterols, triterpene alcohols, and phospholipids in seed oil from white lupin. J Am Oil Chem Soc 81:1039–1044. https://doi.org/10.1007/s11746-004-1019-z
Hondelmann W (1984) The lupin—ancient and modern crop plant. Theor Appl Genet 68:1–9. https://doi.org/10.1007/BF00252301
Imran A, Mirza M, Shah T et al (2015) Differential response of kabuli and desi chickpea genotypes toward inoculation with PGPR in different soils. Front Microbiol. https://doi.org/10.3389/fmicb.2015.00859
Jandacek RJ, Jandacek JR (2017) Linoleic acid: a nutritional quandary. Healthcare 5:25. https://doi.org/10.3390/healthcare5020025
Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27. https://doi.org/10.2307/3546567
Kapravelou G, Martínez R, Andrade AM et al (2013) Health promoting effects of Lupin (Lupinus albus var. multolupa) protein hydrolyzate and insoluble fiber in a diet-induced animal experimental model of hypercholesterolemia. Food Res Int 54:1471–1481. https://doi.org/10.1016/j.foodres.2013.10.019
Kumari S, Yadav RC, Jha S (2018) Effect of microbial inoculants and nitrogen levels on oil content and fatty acid composition in winged bean [Psophocarpus tetragonolobus L. (DC)] seed. ~ 513 ~ J Pharmacogn Phytochem 7:513–517
Leser C, Treutter D (2005) Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees. Physiol Plant 123:49–56. https://doi.org/10.1111/j.1399-3054.2004.00427.x
Lucas MM, Stoddard FL, Annicchiarico P et al (2015) The future of lupin as a protein crop in Europe. Front Plant Sci 6:705. https://doi.org/10.3389/fpls.2015.00705
Martínez-Villaluenga C, Frías J, Vidal-Valverde C (2006) Functional lupin seeds (Lupinus albus L. and Lupinus luteus L.) after extraction of α-galactosides. Food Chem 98:291–299. https://doi.org/10.1016/j.foodchem.2005.05.074
Mesa-Marín J, Del-Saz NF, Rodríguez-Llorente ID et al (2018) PGPR reduce root respiration and oxidative stress enhancing spartina maritima root growth and heavy metal rhizoaccumulation. Front Plant Sci 9:1500. https://doi.org/10.3389/fpls.2018.01500
Nandi M, Selin C, Brawerman G et al (2017) Hydrogen cyanide, which contributes to Pseudomonas chlororaphis strain PA23 biocontrol, is upregulated in the presence of glycine. Biol Control 108:47–54
Naureen Z, Rehman NU, Hussain H et al (2017) Exploring the potentials of Lysinibacillus sphaericus ZA9 for plant growth promotion and biocontrol activities against phytopathogenic fungi. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01477
Niewiadomska A, Sulewska H, Wolna-Maruwka A et al (2018) An assessment of the influence of co-inoculation with endophytic bacteria and rhizobia, and the influence of PRP SOL and PRP EBV fertilisers on the microbial parameters of soil and nitrogenase activity in yellow lupine (Lupinus luteus L.) cultivation. Polish J Environ Stud 27:2687–2702. https://doi.org/10.15244/pjoes/78890
Nosheen A, Naz R, Tahir AT et al (2018) Improvement of safflower oil quality for biodiesel production by integrated application of PGPR under reduced amount of NP fertilizers. PLoS ONE 13:e0201738. https://doi.org/10.1371/journal.pone.0201738
Novinscak A, Filion M (2018) Enhancing total lipid and stearidonic acid yields in Buglossoides arvensis through PGPR inoculation. J Appl Microbiol 125:203–215. https://doi.org/10.1111/jam.13749
Pérez-Montaño F, Alías-Villegas C, Bellogín RA et al (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336
Perez-Vizcaino F, Fraga CG (2018) Research trends in flavonoids and health. Arch Biochem Biophys 646:107–112. https://doi.org/10.1016/j.abb.2018.03.022
Prusinski J (2017) White lupin (Lupinus albus L.)–nutritional and health values in human nutrition—a review. Czech J Food Sci 35:95–105
Rolletschek H, Radchuk R, Klukas C et al (2005) Evidence of a key role for photosynthetic oxygen release in oil storage in developing soybean seeds. New Phytol 167:777–786. https://doi.org/10.1111/j.1469-8137.2005.01473.x
Shakeri E, Modarres-Sanavy SAM, Amini Dehaghi M et al (2016) Improvement of yield, yield components and oil quality in sesame (Sesamum indicum L.) by N-fixing bacteria fertilizers and urea. Arch Agron Soil Sci 62:547–560. https://doi.org/10.1080/03650340.2015.1064901
Song Y, Wang X-D, Rose RJ (2017) Oil body biogenesis and biotechnology in legume seeds. Plant Cell Rep 36:1519–1532. https://doi.org/10.1007/s00299-017-2201-5
Tariq M, Noman M, Ahmed T et al (2017) Antagonistic features displayed by plant growth promoting rhizobacteria (PGPR): a review. J Plant Sci Phytopathol 1:38–43
Trabelsi D, Mengoni A, Ben Ammar H, Mhamdi R (2011) Effect of on-field inoculation of Phaseolus vulgaris with rhizobia on soil bacterial communities. FEMS Microbiol Ecol 77:211–222. https://doi.org/10.1111/j.1574-6941.2011.01102.x
Valette M, Rey M, Gerin F et al (2019) A common metabolomic signature is observed upon inoculation of rice roots with various rhizobacteria. J Integr Plant Biol. https://doi.org/10.1111/jipb.12810
van de Noort M (2017) Chapter 10—Lupin: an important protein and nutrient source a2 - nadathur, sudarshan R. In: Wanasundara JPD, Scanlin L (eds) Sustainable protein sources. Academic Press, San Diego, pp 165–183
Villarino CBJ, Jayasena V, Coorey R et al (2016) Nutritional, health, and technological functionality of lupin flour addition to bread and other baked products: benefits and challenges. Crit Rev Food Sci Nutr 56:835–857. https://doi.org/10.1080/10408398.2013.814044
Vrhovsek U, Masuero D, Gasperotti M et al (2012) A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages. J Agric Food Chem 60:8831–8840. https://doi.org/10.1021/jf2051569
Wolko B, Clements JC, Naganowska B, et al (2011) Wild crop relatives: genomic and breeding resources. Lupinus 153–206
Xiang N, Lawrence KS, Kloepper JW et al (2017) Biological control of Heterodera glycines by spore-forming plant growth-promoting rhizobacteria (PGPR) on soybean. PLoS ONE 12:e0181201. https://doi.org/10.1371/journal.pone.0181201
This work was supported by the Centre of Biotechnology of Borj Cedria and a scholarship from the government of Tunisia (University Tunis El Manar). We are grateful to Fondazione Edmund Mach of Trentino, Italy.
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by Erko Stackebrandt.
About this article
Cite this article
Ferchichi, N., Toukabri, W., Vrhovsek, U. et al. Inoculation of Lupinus albus with the nodule-endophyte Paenibacillus glycanilyticus LJ121 improves grain nutritional quality. Arch Microbiol 202, 283–291 (2020). https://doi.org/10.1007/s00203-019-01745-6