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Effects of Bacillus amyloliquefaciens and different phosphorus sources on Maize plants as revealed by NMR and GC-MS based metabolomics

Abstract

Aims

Plant growth-promoting bacteria of the genus Bacillus are known to solubilize phosphates and enhance plant growth in many plant species. We explored the effects of the inoculation with a commercial isolate Bacillus amyloliquefaciens on the growth and metabolic processes of maize plants in pot soils treated with triple superphosphate, rock phosphate, and either cow- or horse-manure composts, as P-fertilizers.

Methods

The metabolic profiles of maize leaves in the different treatments were determined by both Gas Chromatography–Mass Spectrometry and Nuclear Magnetic Resonance spectroscopy. Principle Components Analysis (PCA) based on data matrix from both techniques revealed a relationship between treatments and specific plant metabolites.

Results

Inoculated plants showed larger P and N contents and a more differentiated metabolome when treated with the two composts than with inorganic fertilizers. B. amyloliquefaciens in combination with composts significantly increased glucose, fructose, alanine and GABA metabolites in maize leaves, thus suggesting an improved photosynthetic activity due to enhanced P and N uptake. Both composts sustained plant growth and the phosphate solubilizing activity of B. amyloliquefaciens, while differences in P and N contents in plant leaves were attributed to the different content in compost of lignin residues and alkyl moieties, and consequent impact on microbial growth.

Conclusions

The combination of B. amyloliquefaciens inoculation with composted organic P-fertilizers rich in available metabolic carbon appears as an efficient alternative to mineral fertilizers to enhance nutrients uptake and foster growth mechanisms in maize plants.

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References

  • Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Tercet-Laforgue T (2012) The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 63:5017–5033

    Article  PubMed  CAS  Google Scholar 

  • Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, Wishart DS (2016) Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res 44:147–153

    Article  CAS  Google Scholar 

  • Brady NC, Weil RR (2008) The nature and properties of soils (fourteenth ed.), Prentice Hall, Upper Saddle River, NJ, USA

  • Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3–21

    Article  CAS  Google Scholar 

  • Chapman S, Barreto H (1997) Using a chlorophyll meter to estimate specific leaf nitrogen of tropical maize during vegetative growth. Agron J 89:557–562

    Article  Google Scholar 

  • Chien SH, Menon RG (1995) Factors affecting the agronomic effectiveness of phosphate rock for direct application. Fertil Res 41:227–234

    Article  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Cozzolino V, Di Meo V, Piccolo A (2013) Impact of arbuscular mycorrhizal fungi applications on maize production and soil phosphorus availability. J Geochem Explor 129:40–44

  • Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo, A (2016) The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fert Soils 52:15–29

  • Fait A, Fromm H, Walter D, Galili G, Fernie AR (2008) Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13:14–19

    Article  PubMed  CAS  Google Scholar 

  • Foyer C, Spencer C (1986) The relationship between phosphate status and photosynthesis in leaves. Planta 167:369–375

    Article  PubMed  CAS  Google Scholar 

  • Ganie AH, Ahmad A, Pandey R, Aref IM, Yousuf PY, Ahmad S, Iqbal M (2015) Metabolite profiling of low-P tolerant and low-P sensitive maize genotypes under phosphorus starvation and restoration conditions. PLoS One 10:e0129520

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gericke S, Kurmies B (1952) Die kolorimetrische Phosphorsaurebestimmung mit Ammonium-Vanadat-Molybdat und ihre Anwendung in der Pflanzenanalyse. Z Pflanzenernähr Bodenkd 59:32–35

    Google Scholar 

  • Gyaneshwar P, Naresh KG, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    Article  CAS  Google Scholar 

  • Hargreaves JC, Adl MS, Warman PR (2008) A review of the use of composted municipal solid waste in agriculture. Agric Ecosyst Environ 123:1–14

    Article  Google Scholar 

  • Hernández G, Ramírez M, Valdés-López O et al (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hirel B, Andrieu B, Valadier MH, Renard S, Quilleré I, Chelle M, Drouet JL (2005) Physiology of maize II: identification of physiological markers representative of the nitrogen status of maize (Zea mays) leaves during grain filling. Physiol Plant 124:178–188

    Article  CAS  Google Scholar 

  • Hofstra G, Nelson CD (1969) The translocation of photosynthetically assimilated in 14C in corn. Can J Bot 47:1435–1442

    Article  CAS  Google Scholar 

  • Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49:691–703

    Article  PubMed  CAS  Google Scholar 

  • Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50(10):1223–1229

    Article  PubMed  CAS  Google Scholar 

  • Koliaei AA, Akbari Gh A, Armandpisheh O, Labbafi MR, Zarghami R (2011) Effects of phosphate chemical fertilizers and biologic fertilizers in various moisture regimes on some morphological characteristics and seeds performance in maize S.C.704. Asian Journal of Agriculture and Food Sciences 3:223–234

    Google Scholar 

  • Kowaljow E, Mazzarino MJ (2007) Soil restoration in semiarid Patagonia: Chemical and biological response to different compost quality. Soil Biol Biochem 39:1580–1588

    Article  CAS  Google Scholar 

  • Lazcano C, Gómez-Brandón M, Revilla P, Domínguez J (2013) Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function. Biol Fertil Soils 49:723–733

    Article  CAS  Google Scholar 

  • Lekfeldt JDS, Rex M, Mercl F, Kulhánek M, Tlustoš P, Magid J, de Neergaard A (2016) Effect of bioeffectors and recycled P-fertiliser products on the growth of spring wheat. Chem Biol Technol Agric 3:22

  • Lemaire G, Gastal F (1997) N uptake and distribution in plant canopies. In: Lemaire G (ed) Diagnosis of the nitrogen status in crops. Springer-Verlag, Berlin, pp 3–43

    Chapter  Google Scholar 

  • Li M, Welti R, Wang X (2006) Quantitative profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142:750–761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li M, Cozzolino V, Mazzei P, Drosos M, Monda H, Hu Z, Piccolo A (2017) Effects of microbial bioeffectors and P amendements on P forms in a maize cropped soil as evaluated by 31 P–NMR spectroscopy. Plant Soil:1–18

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids, the pigments of photosynthetic biomembranes. In: Douce R, Packer L (eds) Methods Enzymol. 148, 350–382. Academic Press Inc., New York

    Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Malik MA, Marschner P, Khan KS (2012) Addition of organic and inorganic P sources to soil–effects on P pools and microorganisms. Soil Biol Biochem 49:106–113

    Article  CAS  Google Scholar 

  • Michaeli S, Fromm H (2015) Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci 6:419

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy J, Riley JP (1962) A modifed single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Pane C, Piccolo A, Spaccini R, Celano G, Villecco D, Zaccardelli M (2013) Agricultural waste-based composts exhibiting suppressivity to diseases caused by the phytopathogenic soil-borne fungi Rhizoctonia solani and Sclerotinia minor. Appl Soil Ecol 65:43–51

    Article  Google Scholar 

  • Qiao J-Q, Wu H-J, Huo R, Gao X-W, Borriss R (2014) Stimulation of plant growth and biocontrol by Bacillus amyloliquefaciens subsp. plantarum FZB42 engineered for improved action. Chem Biol Technol Agric 1:12. https://doi.org/10.1186/s40538-014-0012-2

    Article  CAS  Google Scholar 

  • Reddy MS, Kumar S, Khosla B (2002) Biosolubilization of poorly soluble rock phosphates by Aspergillus tubingensis and Aspergillus niger. Bioresour Technol 84:187–189

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339

    Article  PubMed  CAS  Google Scholar 

  • Rodziewicz P, Swarcewicz B, Chmielewska K, Wojakowska A, Stobiecki M (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol Plant 36:1–19

    Article  CAS  Google Scholar 

  • Schlüter U, Colmsee C, Scholz U, Bräutigam A, Weber APM, Zellerhoff N, Bucher M, Fahnenstich H, Sonnewald U (2013) Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balance. BMC Genomics 14:442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P, Werck-Reichhart D (2001) CYP98A3 from Arabidopsis thaliana is a 30-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J Biol Chem 276:36566–36574

    Article  PubMed  CAS  Google Scholar 

  • Schröder JJ, Smit a L, Cordell D, Rosemarin A (2011) Improved phosphorus use efficiency in agriculture: a key requirement for its sustainable use. Chemosphere 84:822–831

    Article  PubMed  CAS  Google Scholar 

  • Sengupta S, Mukherjee S, Basak P, Majumder AL (2015) Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Front Plant Sci. 26 6:656

    Google Scholar 

  • Spaccini R, Piccolo A (2009) Molecular characteristics of humic acids extracted from compost at increasing maturity stages. Soil Biol Biochem 41:1164–1172

    Article  CAS  Google Scholar 

  • Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75

    Article  CAS  Google Scholar 

  • Sugiharto B, Miyata K, Nakamoto H, Sasakawa H, Sugiyama T (1990) Regulation of expression of carbon-assimilating enzymes by nitrogen in maize leaf. Plant Physiol 92:963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun CX, Gao XX, Li MQ, Fu JQ, Zhang YL (2015) Metabolic response of maize (Zea mays L.) plants to combined drought and salt stress. Plant Soil 388:99–117

    Article  CAS  Google Scholar 

  • Takahama U (1998) Ascorbic acid-dependant regulation of redox levels of chlorogenic acid and its isomers in the apoplast of leaves of Nicotiana tabacum L. Plant Cell Physiol 39:681–689

    Article  CAS  Google Scholar 

  • Thomas H, Stoddart JL (1980) Leaf senescence. Annu Rev Plant Physiol 31:83–111

    Article  CAS  Google Scholar 

  • Thonar C, Lekfeldt JDS, Cozzolino V, Kundel D, Kulhánek M, Mosimann C, Neumann G, Piccolo A, Rex M, Symanczik S, Walder F, Weinmann M, de Neergaard A, Mäder P (2017) Potential of three microbial bio-effectors to promote maize growth and nutrient acquisition from alternative phosphorous fertilizers in contrasting soils. Chem Biol Technol Agric 4:7. https://doi.org/10.1186/s40538-017-0088-6

    Article  CAS  Google Scholar 

  • Vane CH, Martin SC, Snape CE, Abbott GD (2001) Degradation of lignin in wheat straw during growth of the oyster mushroom (Pleurotus ostreatus) using off-line thermochemolysis with tetramethylammonium hydroxyde and solid state 13C NMR. J Agric Food Chem 49:2709–2716

    Article  PubMed  CAS  Google Scholar 

  • Vogt T (2010) Phenylpropanoid Biosynthesis. Mol Plant 3:2–20

    Article  PubMed  CAS  Google Scholar 

  • Zapata F, Zaharah AR (2002) Phosphorus availability from phosphate rock and sewage sludge as influence by the addition of water soluble phosphate fertilizer. Nutr Cycl Agroecosyst 63:43–48

    Article  CAS  Google Scholar 

  • Zhang L, Ding X, Chen S, He X, Zhang F, Feng G (2014) Reducing carbon: phosphorus ratio can enhance microbial phytin mineralization and lessen competition with maize for phosphorus. J Plant Interact 9:850–856

    Article  CAS  Google Scholar 

  • Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium. New Phytol 210:1022–1032

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Hu J, Huang Y, Wang H, Adeleye A, Ortiz C, Keller A (2016) 1H NMR and GC MS based metabolomics reveal nano-Cu altered cucumber (Cucumis sativus) fruit nutritional supply. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2016.02.010

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Acknowledgements

This work was conducted in partial fulfillment of first author PhD requirements, and received funding from the European Community’s Seventh Framework Programme (FP7/2007–2013) under grant agreement n° 312117 (BIOFECTOR).

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Correspondence to Giovanni Vinci or Vincenza Cozzolino.

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Responsible Editor: Tim S. George.

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Vinci, G., Cozzolino, V., Mazzei, P. et al. Effects of Bacillus amyloliquefaciens and different phosphorus sources on Maize plants as revealed by NMR and GC-MS based metabolomics. Plant Soil 429, 437–450 (2018). https://doi.org/10.1007/s11104-018-3701-y

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  • DOI: https://doi.org/10.1007/s11104-018-3701-y

Keywords

  • Metabolomics
  • Phosphate-solubilizing-bacteria
  • Compost
  • Rock phosphate
  • Triple Superphosphate
  • GC-MS
  • 1H-NMR
  • Thermochemolysis