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Characterization of the primary metabolome during the long-term response to NaHCO3-derived alkalinity in Lotus japonicus ecotypes Gifu B-129 and Miyakojima MG-20

Acta Physiologiae Plantarum volume 39, Article number: 76 (2017) Cite this article

Abstract

This study compares the response of two ecotypes of the model species Lotus japonicas, MG-20 and Gifu-B-129, to soil alkalinity, in terms of plant survival and changes in global primary metabolome profiles. After 54 days of treatment with 30 mM NaHCO3, a higher survival was registered in MG-20, with respect to Gifu-B-129 plants. Gas chromatography–mass spectrometry (GC–MS) analysis of shoot extracts from both ecotypes yielded 123 different analytes, 62 of which were identified, including organic acids (OA), amino acids (AA), sugars and polyols. Glycolysis, TCA cycle and amino acids metabolism pathways were differently affected by alkalinity according to the ecotype. The lower tolerance of Gifu B-129 plants to 10 mM NaHCO3, compared with MG-20 ones could be related, at least partially, to the differential accumulation of phosphoric, lactic, threonic, succinic and p-coumaric acids, as well as β-alanine and valine.

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References

  • Babuin MF, Campestre MP, Rocco R et al (2014) Response to long-term NaHCO3-derived alkalinity in model Lotus japonicus Ecotypes Gifu B-129 and Miyakojima MG-20: transcriptomic profiling and physiological characterization. PLoS One 9:e97106. doi:10.1371/journal.pone.0097106

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnett NM, Naylor AW (1966) Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol 41:1222–1230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bie Z, Ito T, Shinohara Y (2004) Effects of sodium sulfate and sodium bicarbonate on the growth, gas exchange and mineral composition of lettuce. Sci Hortic (Amsterdam) 99:215–224. doi:10.1016/S0304-4238(03)00106-7

    Article  CAS  Google Scholar 

  • Colebatch G, Desbrosses G, Ott T et al (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512. doi:10.1111/j.1365-313X.2004.02150.x

    Article  PubMed  Google Scholar 

  • Desbrosses GG, Kopka J, Udvardi MK (2005) Lotus japonicus metabolic profiling. Development of gas chromatography–mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol 137:1302. doi:10.1104/pp.104.054957.1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Rienzo JA, Casanoves F, Balzarini MG et al (2010) InfoStat versión 2010

  • Díaz P, Borsani O, Monza J (2005) Lotus-related species and their agronomic importance. In: Marquez AJ (ed) Lotus Japan handbook. Springer, The Netherlands, pp 25–37

    Chapter  Google Scholar 

  • Ding YZ, Song ZG, Feng RW et al (2014) Interaction of organic acids and pH on multi-heavy metal extraction from alkaline and acid mine soils. Int J Environ Sci Technol 11:33–42

    Article  CAS  Google Scholar 

  • Duda CT, Cherry JH (1971) Chromatin- and nuclei-directed ribonucleic acid synthesis in sugar beet root. Plant Physiol 47:262–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Escaray FJ, Menéndez AB, Gárriz A et al (2012) Ecological and agronomic importance of the plant genus Lotus. Its application in grassland sustainability and the amelioration of constrained and contaminated soils. Plant Sci 182:121–133. doi:10.1016/j.plantsci.2011.03.016

    Article  CAS  PubMed  Google Scholar 

  • Fiehn O, Kopka J, Dörmann P et al (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18:1157–1161

    Article  CAS  PubMed  Google Scholar 

  • Gilbert GA, Gadush MV, Wilson C, Madore MA (1998) Amino acid accumulation in sink and source tissues of Coleus blumei Benth during salinity stress. J Exp Bot 49:107–114. doi:10.1093/jxb/49.318.107

    Article  CAS  Google Scholar 

  • Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190

    Article  CAS  Google Scholar 

  • Guo R, Yang Z, Li F et al (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15:170–183

    Article  PubMed  PubMed Central  Google Scholar 

  • Hageman RH (1984) Ammonium versus nitrate nutrition of higher plants. In: Hauck RD (ed) Nitrogen in crop production. ASA, CSSA, SSSA, Madison, pp 67–85

    Google Scholar 

  • Hatfield RD, Marita JM (2010) Enzymatic processes involved in the incorporation of hydroxycinnamates into grass cell walls. Phytochem Rev 9:35–45

    Article  CAS  Google Scholar 

  • Heldt H-W, Piechulla B (2011) Plant biochemistry, 4th edn. p 656

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:1–32

    Google Scholar 

  • Hu L, Zhang P, Jiang Y, Fu J (2015) Metabolomic analysis revealed differential adaptation to salinity and alkalinity stress in kentucky bluegrass (Poa pratensis). Plant Mol Biol Rep 33:56–68

    Article  CAS  Google Scholar 

  • Iwata Y, Koizumi N (2012) Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci 17:720–727. doi:10.1016/j.tplants.2012.06.014

    Article  CAS  PubMed  Google Scholar 

  • Kopka J, Schauer N, Krueger S et al (2005) GMD@CSB.DB: the Golm Metabolome Database. Bioinformatics 21:1635–1638

    Article  CAS  PubMed  Google Scholar 

  • Kumar K, Kumar M, Kim S-R et al (2013) Insights into genomics of salt stress response in rice. Rice 6:27. doi:10.1186/1939-8433-6-27

    Article  PubMed  PubMed Central  Google Scholar 

  • Lisec J, Schauer N, Kopka J et al (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. p 651

  • Nikiforova V, Freitag J, Kempa S et al (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650

    Article  CAS  PubMed  Google Scholar 

  • Pang Q, Zhang A, Zang W et al (2016) Integrated proteomics and metabolomics for dissecting the mechanism of global responses to salt and alkali stress in Suaeda corniculata. Plant Soil. doi:10.1007/s11104-015-2774-0

    Google Scholar 

  • Paz RC, Rocco RA, Reinoso H et al (2012) Comparative study of alkaline, saline, and mixed saline-alkaline stresses with regard to their effects on growth, nutrient accumulation, and root morphology of Lotus tenuis. J Plant Growth Regul 31:448–459. doi:10.1007/s00344-011-9254-4

    Article  CAS  Google Scholar 

  • Rao KP, Rains D-W (1976) Nitrate absorption by Barley: I. Kinet Energ Plant Physiol 57:55–58. doi:10.1104/pp.57.1.55

    Article  CAS  Google Scholar 

  • Rellán-Álvarez R, Giner-Martínez-Sierra J, Orduna J et al (2010) Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102

    Article  PubMed  Google Scholar 

  • Roessner U, Luedemann A, Brust D et al (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Grillet L, Isaure MP et al (2011) Plant cell nucleolus as a hot spot for iron. J Biol Chem 286:27863–27866. doi:10.1074/jbc.C111.269720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Conéjéro G, Divol F et al (2013) New insights into Fe localization in plant tissues Front. Plant Sci 4:350. doi:10.3389/fpls.2013.00350

    Google Scholar 

  • Rose MT, Rose TJ, Pariasca-Tanaka J et al (2012) Root metabolic response of rice (Oryza sativa L.) genotypes with contrasting tolerance to zinc deficiency and bicarbonate excess. Planta 236:959–973

    Article  CAS  PubMed  Google Scholar 

  • Schauer N, Steinhauser D, Strelkov S et al (2005) GC–MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579:1332–1337

    Article  CAS  PubMed  Google Scholar 

  • Shahidi F, Chandrasekara A (2010) Hydroxycinnamates and their in vitro and in vivo antioxidant activities. Phytochem Rev 9:147–170

    Article  CAS  Google Scholar 

  • Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by d-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115:1211–1219. doi:10.1104/pp.115.3.1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szabados L, Kovacs H, Zilberstein A, Bouchereau A (2011) Plants in extreme environments: importance of protective compounds in stress tolerance. Adv Bot Res 57:105–150

    Article  CAS  Google Scholar 

  • Taji T, Takahashi S, Shinozaki K (2006) Inositols and their metabolites in abiotic and biotic stress responses. In: Majumder AL, Biswas BB (eds) Biology of inositols and phosphoinositides SE-10. Springer, New York, pp 239–264

    Chapter  Google Scholar 

  • Valdez-Aguilar LA, Reed DW (2010) Groth and nutrition of young bean plants under high alkalinity as affected by mixtures of ammonium, potassium, and sodium. J Plant Nutr 33:1472–1488. doi:10.1080/01904167.2010.489985

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Agencia Nacional de promoción Científica y Tecnológica/FONCyT PICTs 2034 and 1611, and the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina). We also thank the University of Valencia for metabolomic facilities.

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    Authors and Affiliations

    1. Instituto de Investigaciones Biotecnológicas-Instituto Tecnológico de Chascomús/Universidad Nacional de General San Martín-Consejo Nacional de Investigaciones Científicas y Técnicas (IIB-INTECH/UNSAM-CONICET), Chascomús, Argentina

      Cesar D. Bordenave, Rubén Rocco, María Florencia Babuin, María Paula Campestre, Francisco J. Escaray, Andrés Gárriz, Cristian Antonelli & Oscar A. Ruiz

    2. Departamento de Bioquímica y Biología Vegetal-Universitat de Valencia, Valencia, Spain

      Pedro Carrasco

    3. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina

      Ana B. Menéndez

    4. INMIBO (CONICET), Buenos Aires, Argentina

      Ana B. Menéndez

    Author notes

    1. C. D. Bordenave and R. Rocco contributed equally to this work and, therefore, should be regarded both as first authors.

      A. B. Menéndez and O. A. Ruiz shared the same responsibility on this work and, therefore, should be regarded both as senior authors.

      Authors
      1. Cesar D. Bordenave
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      2. Rubén Rocco
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      3. María Florencia Babuin
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      4. María Paula Campestre
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      5. Francisco J. Escaray
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      6. Andrés Gárriz
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      7. Cristian Antonelli
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      8. Pedro Carrasco
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      9. Oscar A. Ruiz
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      10. Ana B. Menéndez
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      Correspondence to Ana B. Menéndez.

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      Communicated by M. Stobiecki.

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      Bordenave, C.D., Rocco, R., Babuin, M.F. et al. Characterization of the primary metabolome during the long-term response to NaHCO3-derived alkalinity in Lotus japonicus ecotypes Gifu B-129 and Miyakojima MG-20. Acta Physiol Plant 39, 76 (2017). https://doi.org/10.1007/s11738-017-2369-x

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      • DOI: https://doi.org/10.1007/s11738-017-2369-x

      Keywords

      • Alkalinity
      • Lotus japonicus
      • Gifu B-120
      • Miyakojima MG-20
      • Metabome
      • GC–MS