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Biochar improved nodulation and nitrogen metabolism of soybean under salt stress

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Abstract

To investigate salt stress and biochar application effects on nodulation and nitrogen metabolism of soybeans (Glycine max cv. M7), an experiment was conducted under the control condition. The treatments comprised three biochar rates (non, 50 and 100 g kg−1 soil) and three salinities (0, 5 and 10 dS m−1 NaCl), with four replications of treatments. Salt stress diminished the number of nodules and their weights in the soybean roots. Nitrogen content and metabolism decreased in nodules, roots and shoots, while reducing the activity of glutamate dehydrogenase (GDH), glutamine synthetase (GS), glutamine oxoglutarate aminotransferase (GOGAT) and nitrate reductase (NR). Also, salinity brought down root and shoot weight, total plant biomass, chlorophyll content, leaf area (LA) and rubisco activity in the soybean. On the other hand, application of biochar improved nodulation, nitrogen content, rubisco activity, GDH, GS, GOGAT and NR activities in different parts of the soybean and nodules under salt stress, and consequently improved chlorophyll content, LA, root and shoot weight. Both the 50 and 100 g kg−1 biochar rates showed similar effects in improving nitrogen metabolism and plant performance under salt stress. Generally, biochar increased nodulation and nitrogen metabolism of the soybean under saline conditions.

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References

  • Abd-Alla MH, Vuong TD, Harper JE (1998) Genotypic differences in dinitrogen fixation response to NaCl stress in intact and grafted soybean. Crop Sci 38:72–77

    Article  Google Scholar 

  • Akhtar SS, Andersen MN, Liu F (2015) Residual effects of biochar on improving growth, physiology and yield of wheat under salt stress. Agric Water Manag 158:61–68

    Article  Google Scholar 

  • Antal MJ, Gronli M (2003) The art, science, and technology of charcoal production. Ind Eng Chem Res 42:1619–1640

    Article  CAS  Google Scholar 

  • Araújo SS, Beebe S, Crespi M, Delbreil B, González EM, Gruber V, Lejeune-Henaut I, Link W, Monteros MJ, Prats E, Rao I (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ascough PL, Bird MI, Brock F, Higham TFG, Meredith W, Snape CE, Vane CH (2009) Hydropyrolysis as a new tool for radiocarbon pre-treatment and the quantification of black carbon. Quat Geochronol 4:140–147

    Article  Google Scholar 

  • Becker TW, Carrayol E, Hirel B (2000) Glutamine synthetase and glutamate dehydrogenase isoforms in maize leaves: localization, relative proportion and their role in ammonium assimilation or nitrogen transport. Planta 211:800–806

    Article  CAS  PubMed  Google Scholar 

  • Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164

    Article  CAS  PubMed  Google Scholar 

  • Blanco-Canqui H, Lal R (2009) Crop residue removal impacts on soil productivity and environmental quality. Crit Rev Plant Sci 28:139–163

    Article  CAS  Google Scholar 

  • Chakrabarti N, Mukherji S (2003) Effect of phytohormone pretreatment on nitrogen metabolism in Vigna radiata under salt stress. Biol Plant 46:63–66

    Article  CAS  Google Scholar 

  • Chan KY, Xu Z (2009) Biochar: nutrient properties and their enhancement. Biochar for environmental management: science and technology. Earthscan, London, pp 67–84

    Google Scholar 

  • Comba ME, Benavides MP, Tomaro ML (1998) Effect of salt stress on antioxidant defense system in soybean root nodules. Funct Plant Biol 25:665–671

    CAS  Google Scholar 

  • Duke SH, Ham GE (1976) The effect of nitrogen addition on N2-fixation and on glutamate dehydrogenase and glutamate synthase activities. In nodules and roots of soybeans inoculated with various strains of Rhizobium japonicum. Plant Cell Physiol 17:1037–1044

    CAS  Google Scholar 

  • Evans JR (1983) Nitrogen and photosynthesis in the flag leaf of wheat (Triticum aestivum L.) Plant Physiol 72:297–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faghire M, Bargaz A, Farissi M, Palma F, Mandri B, Lluch C, García NAT, Herrera-Cervera JA, Oufdou K, Ghoulam C (2011) Effect of salinity on nodulation, nitrogen fixation and growth of common bean (Phaseolus vulgaris) inoculated with rhizobial strains isolated from the Haouz region of Morocco. Symbiosis 55:69–75

    Article  CAS  Google Scholar 

  • Faghire M, Mohamed F, Taoufiq K, Fghire R, Bargaz A, Mandri B, Oufdou K, Laury A, Drevon JJ, Ghoulam C (2013) Genotypic variation of nodules’ enzymatic activities in symbiotic nitrogen fixation among common bean (Phaseolus vulgaris L.) genotypes grown under salinity constraint. Symbiosis 3:115–122

    Article  Google Scholar 

  • Fahad S, Hussain S, Saud S, Hassan S, Tanveer M, Ihsan MZ, Shah AN, Ullah A, Khan F, Ullah S, Alharby H (2016) A combined application of biochar and phosphorus alleviates heat-induced adversities on physiological, agronomical and quality attributes of rice. Plant Physiol Biochem 103:191–198

    Article  CAS  PubMed  Google Scholar 

  • Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Pascual M, De Lorenzo C, de Felipe MR, Rajalakshmi S, Gordon AJ, Thomas BJ, Minchin FR (1996) Possible reasons for relative salt stress tolerance in nodules of white lupin cv. Multolupa J Exp Bot 47:1709–1716

    Article  Google Scholar 

  • Flowers TJ, Gaur PM, Gowda CL, Krishnamurthy L, Samineni S, Siddique KH, Colmer TD (2010) Salt sensitivity in chickpea. Plant Cell Environ 33:490–509

    Article  CAS  PubMed  Google Scholar 

  • Fougere F, Le Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid, and carbohydrate composition of roots, bacteroids, and cytosol of alfalfa (Medicago sativa L.) Plant Physiol 96:1228–1236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garsia-Sanchez F, Jufon JL, Carvaial M, Syverstem JP (2002) Gas exchange, chlorophyll and nutrient contents in relation to Na+ and cl− accumulation in ‘sunburst’ mandarin grafted on different rootstocks. Plant Sci 162:705–712

    Article  Google Scholar 

  • Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot 47:39–50

    Article  CAS  Google Scholar 

  • Grieve CM, Grattan SR, Maas EV (2012) Plant salt tolerance. Agricultural salinity assessment and management, 2nd edn. ASCE Manual Rep Eng Pract 71:405–459

    Google Scholar 

  • Hammer EC, Forstreuter M, Rillig MC, Kohler J (2015) Biochar increases arbuscular mycorrhizal plant growth enhancement and ameliorates salinity stress. Appl Soil Ecol 96:114–121

    Article  Google Scholar 

  • Huchzermeyer B, Heins T (2000) Energy metabolism and salt stress. INCO-DC annual report. University of Osnabrück Publication, Osnabrück, pp 48–73

    Google Scholar 

  • James EK, Sprent JI, Hay GT, Minchin FR (1993) The effect of irradiance on the recovery of soybean nodules from sodium chloride-induced senescence. J Exp Bot 44:997–1005

    Article  CAS  Google Scholar 

  • Jaworski EG (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43:1274–1279

    Article  CAS  PubMed  Google Scholar 

  • Jones DL, Rousk J, Edwards-Jones G, DeLuca TH, Murphy DV (2012) Biochar-mediated changes in soil quality and plant growth in a three-year field trial. Soil Biol Biochem 45:113–124

    Article  CAS  Google Scholar 

  • Koyro HW, Huchzermeyer B (1999) Influence of high NaCl-salinity on growth, water and osmotic relations of the halophyte Beta Vulgaris Ssp. Maritima. Development of a quick check. Prog Biometeorol 13:87–101

    Google Scholar 

  • Kusano M, Fukushima A, Redestig H, Saito K (2011) Metabolomic approaches toward understanding nitrogen metabolism in plants. J Exp Bot 62:1439–1453

    Article  CAS  PubMed  Google Scholar 

  • Lehmann J, Czimczik C, Laird D, Sohi S (2009) Stability of biochar in soil. Biochar for environmental management: science and technology. Earthscan, London, pp 183–206

    Google Scholar 

  • Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D (2011) Biochar effects on soil biota-a review. Soil Biol Biochem 43:1812–1836

    Article  CAS  Google Scholar 

  • Lobo AKM, de Oliveira MM, Neto MCL, Machado EC, Ribeiro RV, Silveira JAG (2015) Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. J Plant Physiol 179:113–121

    Article  CAS  PubMed  Google Scholar 

  • López-Gómez M, Hidalgo-Castellanos J, Lluch C, Herrera-Cervera JA (2016) 24-Epibrassinolide ameliorates salt stress effects in the symbiosis Medicago Truncatula-Sinorhizobium meliloti and regulates the nodulation in cross-talk with polyamines. Plant Physiol Biochem 108:212–221

    Article  PubMed  Google Scholar 

  • Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil 253:201–218

    Article  CAS  Google Scholar 

  • Ogawa M, Okimori Y (2010) Pioneering works in biochar research, Japan. Soil Res 48:489–500

    Article  CAS  Google Scholar 

  • Qian L, Chen B, Hu D (2013) Effective alleviation of aluminum phytotoxicity by manure-derived biochar. Environ Sci Technol 47:2737–2745

    Article  CAS  PubMed  Google Scholar 

  • Quilliam RS, Rangecroft S, Emmett BA, Deluca TH, Jones DL (2013) Is biochar a source or sink for polycyclic aromatic hydrocarbon (PAH) compounds in agricultural soils? GCB Bioenergy 5:96–103

    Article  CAS  Google Scholar 

  • Rambo L, Ma BL, Xiong Y, da Silvia Ferreira PR (2010) Leaf and canopy optical characteristics as crop-N-status indicators for field nitrogen management in corn. J Plant Nutr Soil Sci 173:434–443

    Article  CAS  Google Scholar 

  • Sawhney V, Singh R (1985) Effect of applied nitrate on enzymes of ammonia assimilation in nodules of Cicer arietinum L. Plant Soil 86:241–248

    Article  CAS  Google Scholar 

  • Serraj R, Roy G, Drevon JJ (1994) Salt stress induces a decrease in the oxygen uptake of soybean nodules and in their permeability to oxygen diffusion. Physiol Plant 91:161–168

    Article  CAS  Google Scholar 

  • Sinclair TR, Horie T (1989) Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci 29:90–98

    Article  Google Scholar 

  • Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83

    Article  CAS  PubMed  Google Scholar 

  • Singleton PW, Bohlool BB (1984) Effect of salinity on nodule formation by soybean. Plant Physiol 74:72–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slattery JF, Coventry DR, Slattery WJ (2001) Rhizobial ecology as affected by the soil environment. Anim Prod Sci 41:289–298

    Article  CAS  Google Scholar 

  • Steinbeiss S, Gleixner G, Antonietti M (2009) Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol Biochem 41:1301–1310

    Article  CAS  Google Scholar 

  • Taffouo VD, Wamba OF, Yombi E, Nono GV, Akoe A (2010) Growth, yield, water status and ionic distribution response of three bambara groundnut (Vigna subterranean L. verdc.) landraces grown under saline conditions. Int J Bot 6:53–58

    Article  CAS  Google Scholar 

  • Thomas SC, Frye S, Gale N, Garmon M, Launchbury R, Machado N, Melamed S, Murray J, Petroff A, Winsborough C (2013) Biochar mitigates negative effects of salt additions on two herbaceous plant species. Environ Manag 129:62–68

    CAS  Google Scholar 

  • Tu JC (1981) Effect of salinity on rhizobium-root-hair interaction, nodulation and growth of soybean. Can J Plant Sci 61:231–239

    Article  Google Scholar 

  • Van Zwieten L, Kimber S, Morris S, Chan KY, Downie A, Rust J, Joseph S, Cowie A (2010) Effects of biochar from slow pyrolysis of papermill waste on agronomic performance and soil fertility. Plant Soil 327:235–246

    Article  Google Scholar 

  • Van Zwieten L, Rose T, Herridge D, Kimber S, Rust J, Cowie A, Morris S (2015) Enhanced biological N2 fixation and yield of faba bean (Vicia faba L.) in an acid soil following biochar addition: dissection of causal mechanisms. Plant Soil 395:7–20

    Article  Google Scholar 

  • Wang YF, Jiang D, Yu ZW, Cao WX (2003) Effects of nitrogen rates on grain yield and protein content of wheat and its physiological basis. Sci Agric Sin 36:513–520 in Chinese with English abstract

    Google Scholar 

  • Wang Y, Pan F, Wang G, Zhang G, Wang Y, Chen X, Mao Z (2014) Effects of biochar on photosynthesis and antioxidative system of Malus hupehensis Rehd. Seedlings under replant conditions. Sci Hort 175:9–15

    Article  CAS  Google Scholar 

  • Yu-kui R, Yun-feng P, Zheng-rui W, Jian-bo S (2012) Stem perimeter, height and biomass of maize (Zea mays L.) grown under different N fertilization regimes in Beijing, China. Int J Plant Prod 3:85–90

    Google Scholar 

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Acknowledgements

We appreciate the University of Tabriz for providing greenhouse and laboratory.

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Authors and Affiliations

  1. Department of Plant Eco-Physiology, Faculty of Agriculture, University of Tabriz, Tabriz, Iran

    Salar Farhangi-Abriz

  2. Department of Agronomy, College of Agriculture, Isfahan University of Technology, Isfahan, Iran

    Shahram Torabian

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  1. Salar Farhangi-Abriz
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Correspondence to Shahram Torabian.

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Farhangi-Abriz, S., Torabian, S. Biochar improved nodulation and nitrogen metabolism of soybean under salt stress. Symbiosis 74, 215–223 (2018). https://doi.org/10.1007/s13199-017-0509-0

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