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Can co-inoculation of Bradyrhizobium and Azospirillum alleviate adverse effects of drought stress on soybean (Glycine max L. Merrill.)?

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Abstract

Harnessing the beneficial potential of plant growth-promoting rhizobacteria may be an alternative strategy to improve plant tolerance to drought stress. The effect of inoculation with Bradyrhizobium japonicum and Azospirillum brasilense either alone or in combination on the plant growth and drought tolerance of soybean [Glycine max (L.) Merrill.] was investigated in this study in greenhouse conditions. Treatments were arranged in a randomized block design in a 3 × 4 factorial: three irrigation regimes [100% of pot capacity—PC (well-watered control), 50% of PC (moderate stress) and 25% of PC (severe stress)] and four inoculation treatments [control (non-inoculated), inoculation with B. japonicum, inoculation with A. brasilense, and co-inoculation with B. japonicum and A. brasilense]. Leaf relative water content, cell membrane stability, root nodulation, plant growth, and morphophysiological indexes were recorded. The inoculation of soybean plants with B. japonicum and A.brasilense either alone or in combination improved leaf membrane stability under drought stress conditions when compared to non-inoculated plants; however, this lower damage to cell membranes was not sufficient to maintain the leaf water content of the plant under drought stress. Plants co-inoculated with B. japonicum and A.brasilense improved the root nodulation under severe drought conditions. Inoculation of B. japonicum and A. brasilense either alone or in combination reduced the pod abortion rate under moderate drought stress, but had no effect under severe drought stress. In summary, the co-inoculation of A. brasilense and B. japonicum alleviate adverse effects limited by drought stress to the growth of soybeans.Author: Please check and confirm that the authors [Elijanara Raissa Silva, Carlos Eduardo Silva Oliveira, Alan Mario Zuffo, Eduardo Pradi Vendruscolo] and their initials have been correctly identified and amend if necessary.The authors were correctly identified.

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References

  • Abbasi S, Zahedi H, Sadeghipour O, Akbari R (2013) Effect of plant growth promoting rhizobacteria (PGPR) on physiological parameters and nitrogen content of soybean grown under different irrigation regimes. Res Crops 14:798–803

    Google Scholar 

  • Agami RA, Medani RA, Abd El-Mola IA, Taha RS (2016) Exogenous application with plant growth promoting rhizobacteria (PGPR) or proline induces stress tolerance in basil plants (Ocimum basilicum L.) exposed to water stress. Int J Agric Environ Res 5:78–92

    Google Scholar 

  • Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World J Microbiol Biotechnol 27:197–205

    Article  CAS  Google Scholar 

  • Assaha DV, Liu L, Ueda A, Nagaoka T, Saneoka H (2016) Effects of drought stress on growth, solute accumulation and membrane stability of leafy vegetable, huckleberry (Solanum scabrum Mill.). J Environ Biol 37:107–114

    CAS  PubMed  Google Scholar 

  • Bai Y, Zhou-**ao M, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781

    Article  Google Scholar 

  • Benincasa MPM (2003) Análise de crescimento de plantas: noções básicas. FUNEP, Jaboticabal, p 42

    Google Scholar 

  • Benintende S, Uhrich W, Herrera M, Gangge F, Sterren M, Benintende M (2010) Comparación entre coinoculación con Bradyrhizobium japonicum y Azospirillum brasilense e inoculación simple con Bradyrhizobium japonicum en la nodulación, crecimiento y acumulación de N en el cultivo de soja. Agriscientia 37:71–77

    Google Scholar 

  • Bulegon LG, Rampim L, Klein J, Kestring D, Guimarães VF, Battistus AG, Inagaki AM (2016) Componentes de produção e produtividade da cultura da soja submetida à inoculação de Bradyrhizobium e Azospirillum. Terra Latinoam 34:169–176

    Google Scholar 

  • Bulegon LG, Guimarães VF, Klein J, Batisttus AG, Inagaki AM, Offmann LC, Souza AKP (2017) Enzymatic activity, gas exchange and production of soybean co-inoculated with Bradyrhizobium japonicum and Azospirillum brasilense. Aust J Crop Sci 11:888–896

    Article  CAS  Google Scholar 

  • Casaroli D, Lier QJ (2008) Critérios para determinação da capacidade de vaso. Rev Bras Ciênc Solo 32:59–66

    Article  Google Scholar 

  • Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35

    Article  CAS  Google Scholar 

  • Cerezini P, Kuwano BH, Santos MB, Terassi F, Hungria M, Nogueira MA (2016) Strategies to promote early nodulation in soybean under drought. Field Crops Res 196:160–167

    Article  Google Scholar 

  • Chibeba AM, Guimarães MF, Brito OR, Nogueira MA, Araujo RS, Hungria M (2015) Co-inoculation of soybean with Bradyrhizobium and Azospirillum promotes early nodulation. Am J Plant Sci 6:1641–1649

    Article  Google Scholar 

  • Curá JA, Franz DR, Filosofía JE, Balestrasse KB, Burgueño LE (2017) Inoculation with Azospirillum sp. and Herbaspirillum sp. bacteria increases the tolerance of maize to drought stress. Microorganisms 5:41

    Article  CAS  PubMed Central  Google Scholar 

  • Embrapa (1997) Empresa Brasileira de Pesquisa Agropecuária. Manual de métodos de análise de solo, 2. edn. EMBRAPA/CNPS, Rio de Janeiro, p 212

    Google Scholar 

  • Fipke GM, Conceição GM, Grando LF, Teleken L, Nunes RL, Ubirajara R, Martin TN (2016) Co-inoculation with diazotrophic bacteria in soybeans associated to urea topdressing. Ciênc Agrotec 40:522–533

    Article  CAS  Google Scholar 

  • German MA, Burdman S, Okon Y, Kigel J (2000) Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol Fertil Soil 32:259–264

    Article  Google Scholar 

  • Gray SB, Brady SM (2016) Plant developmental responses to climate change. Dev Biol 419:64–77

    Article  CAS  PubMed  Google Scholar 

  • Gusain YS, Singh US, Sharma AK (2015) Bacterial mediated amelioration of drought stress in drought tolerant and susceptible cultivars of rice (Oryza sativa L.). Afr J Biotechnol 14:764–773

    Article  CAS  Google Scholar 

  • Hungria M, Mendes IC (2015) Nitrogen fixation with soybean: the perfect symbiosis? In: Bruijn FJ (ed) Biological nitrogen fixations. Wiley, Ney Jersey, pp 1009–1021

    Chapter  Google Scholar 

  • Hungria M, Nogueira MA, Araujo RS (2015) Soybean seed co-inoculation with Bradyrhizobium spp. and Azospirillum brasilense: a new biotechnological tool to improve yield and sustainability. Am J Plant Sci 6:811–817

    Article  CAS  Google Scholar 

  • Inagaki AM, Guimarães VF, Rodrigues LFOS, Silva MB, Diamante MS, Rampim L, Mioranza TM, Duarte Júnior JB (2014) Phosphorus fertilization associated to inoculation of maize with diazotrophic bacteria. Afr J Agric Res 9:3480–3487

    Article  Google Scholar 

  • Juge C, Prévost D, Bertrand A, Bipfubusa M, Chalifour FP (2012) Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae. Appl Soil Ecol 61:147–157

    Article  Google Scholar 

  • Liu F, **ng S, Ma H, Du Z, Ma B (2013) Cytokinin producing, plant growth promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164

    Article  CAS  PubMed  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) Effects of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. J Plant Growth Regul 19:207–218

    Article  CAS  Google Scholar 

  • Mantovani D, Veste M, Boldt-Burisch K, Fritsch S, Koning LA, Freese D (2015) Carbon allocation, nodulation, and biological nitrogen fixation of black locust (Robinia pseudoacacia L.) under soil water limitation. Ann For Sci 58:259–274

    Google Scholar 

  • Marks BB, Megías M, Nogueira MA, Hungria M (2013) Biotechnological potential of rhizobial metabolites to enhance the performance of Bradyrhizobium japonicum and Azospirillum brasilense inoculants with the soybean and maize crops. Appl Microbiol Biotechnol 3:1–10

    Google Scholar 

  • Mertz-Henning LM, Ferreira LC, Henning FA, Mandarino JMG, Santos ED, Oliveira MCND, Nepomuceno AEL, Farias JRB, Neumaier N (2018) Effect of water deficit-induced at vegetative and reproductive stages on protein and oil content in soybean grains. Agronomy 8:1–11

    Google Scholar 

  • Naveed M, Hussain MB, Zahir ZA, Mitter B, Sessitsch A (2014) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul 73:121–131

    Article  CAS  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  CAS  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    Article  CAS  PubMed  Google Scholar 

  • Sangtarash MH (2010) Responses of different wheat genotypes to drought stress applied at different growth stages. Pak J Biol Sci 13:114–119

    Article  CAS  PubMed  Google Scholar 

  • Vieira EA, Silva MG, Moro CF, Laura VA (2017) Physiological and biochemical changes attenuate the effects of drought on the Cerrado species Vatairea macrocarpa (Benth.) Ducke. Plant Physiol Biochem 115:472–483

    Article  CAS  PubMed  Google Scholar 

  • Vurukonda SSKP, Vardharajula S, Shrivastava M, Skz A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24

    Article  PubMed  Google Scholar 

  • Wellstein C, Poschlod P, Gohlke A, Chelli S, Campetella G, Rosbakh S, Canullo R, Kreyling J, Jentsch A, Beierkuhnlein C (2017) Effects of extreme drought on specific leaf area of grassland species: a meta-analysis of experimental studies in temperate and sub-Mediterranean systems. Glob Change Biol 23:2473–2481

    Article  Google Scholar 

  • Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signal Behav 5:649–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoz T, Steiner F, Guimarães VF, Castagnara DD, Meinerz CC, Fey R (2013) Peroxidase activity as an indicator of water deficit tolerance in soybean cultivars. Biosci J 29:1664–1671

    Google Scholar 

  • Zuffo AM, Bruzi AT, Rezende PM, Bianchi MC, Zambiazzi EV, Soares IO, Ribeiro ABM, Vilela GLD (2016) Morphoagronomic and productive traits of RR soybean due to inoculation via Azospirillum brasilense groove. Afr J Microbiol Res 10:438–444

    Article  CAS  Google Scholar 

Download references

Acknowledgements

To CNPq (National Council for Scientific and Technological Development) and UEMS (State University of Mato Grosso do Sul) for the scientific initiation scholarship granted to the second author.

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Authors and Affiliations

  1. Department of Crop Science, State University of Santa Catarina, UDESC, Lages, Santa Catarina, 88035-901, Brazil

    Elijanara Raissa Silva

  2. Department of Crop Science, State University of Mato Grosso do Sul, UEMS, Cassilândia, Mato Grosso Do Sul, 79540-000, Brazil

    Jardel Zoz, Carlos Eduardo Silva Oliveira, Fábio Steiner, Tiago Zoz & Eduardo Pradi Vendruscolo

  3. Department of Agronomy, Federal University of Mato Grosso do Sul, UFMS, Chapadão do Sul, MS, 79560-000, Brazil

    Alan Mario Zuffo

Authors
  1. Elijanara Raissa Silva
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  2. Jardel Zoz
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  3. Carlos Eduardo Silva Oliveira
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  4. Alan Mario Zuffo
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  5. Fábio Steiner
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  6. Tiago Zoz
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  7. Eduardo Pradi Vendruscolo
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Contributions

ERS, JA, AMZ, and FA designed and carried out the experiment. ERS, JZ, FS, and AMZ collected the data. FS and AMZ performed the analysis. ERS, JZ, CESO, and AMZ contributed to the interpretation of the results. FA wrote the manuscript. TZ and EPV contributed to the final version of the manuscript. All authors provided critical feedback and helped to shape the research, analysis, and manuscript.

Corresponding author

Correspondence to Fábio Steiner.

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Communicated by Erko Stackebrandt.

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Silva, E.R., Zoz, J., Oliveira, C.E.S. et al. Can co-inoculation of Bradyrhizobium and Azospirillum alleviate adverse effects of drought stress on soybean (Glycine max L. Merrill.)?. Arch Microbiol 201, 325–335 (2019). https://doi.org/10.1007/s00203-018-01617-5

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