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Improvement of rice seedling growth and nitrogen use efficiency by seed inoculation with endophytic denitrifiers

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Abstract

The aim of the present study is to investigate the effect of seed inoculation with endophytic denitrifiers on rice seedling growth and nitrogen use efficiency under low- and high-urea conditions. Pseudomonas sp. B2, Streptomyces sp. A9, and Fusarium sp. F3 were isolated from rice plant tissues. Rice seeds inoculated with the denitrifiers were sown in soil fertilized with 100 and 300 mg/kg urea concentrations, respectively. The denitrifiers increased soil ammonia concentrations or kept high ammonia concentration for a longer time in soils. However, soil nitrate concentrations with the denitrifier treatments were lower than that of the control. All the denitrifier treatments increased the chlorophyll content by more than 200% under the low urea condition. Compared to the control, the denitrifier inoculation treatments significantly increased shoot length, fresh weight, and dry weight of rice seedlings under the low- and high-urea conditions (P < 0.05). The chlorophyll concentrations, shoot length, wet weight, and dry weight of all the denitrifier treatments under the low urea fertilization were significantly higher than those of the control under the high-urea fertilization (P < 0.05). The nitrogen use efficiency of rice seedlings might be attributable to nitrate reductases of the denitrifiers, acting as the rice nitrate reductase. The treatment of endophytic denitrifiers significantly improved rice seedling growth and nitrogen use efficiency under both low- and high-urea conditions.

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References

  • Cao L, Jiang M, Zeng Z, Du A, Tan H, Liu Y (2008) Trichoderma atroviride F6 improves phytoextraction efficiency of mustard (Brassia juncea (L) Coss. var. foliosa Bailey ) in Cd, Ni contaminated soils. Chemosphere 71:1769–1773

    Article  CAS  Google Scholar 

  • Cong PT, Dung TD, Hien TM, Hien NT, Choudhury ATMA, Kecskes NL, Kennedy I (2009) Inoculant plant growth-promoting microorganisms enhance utilisation of urea-N and grain yield of paddy rice in Southern Vietnam. Eur J Soil Biol 45:52–61

    Article  CAS  Google Scholar 

  • Fang Z, Xia K, Yang X, Grotemeyer MS, Meier S, Rentsch D, Xu X, Zhang M (2013) Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnol J 11:446–458

    Article  CAS  Google Scholar 

  • Ikeda S, Sasaki K, Okubo T, Yamashita A, Terasawa K, Bao ZH, Liu DY, Watanabe T, Murase J, Asakawa S, Eda S, Mitsui H, Sato T, Minamisawa K (2014) Low nitrogen fertilization adapts rice root microbiome to low nutrient environment by changing biogeochemical functions. Microbes Environ 29:50–59

    Article  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485

    Article  CAS  Google Scholar 

  • Ishii S, Yamamoto M, Kikuchi M, Oshima K, Hattori M, Otsuka S, Senoo K (2009) Microbial populations responsive to denitrification-inducing conditions in rice paddy soil, as revealed by comparative 16S rRNA gene analysis. Appl Environ Microbiol 75:7070–7078

    Article  CAS  Google Scholar 

  • Jiang M, Cao L, Zhang R (2008) Effects of acacia (Acacia auriculaeformis A. Cunn)-associated fungi on mustard (Brassica Juncea (L.) Coss. var. foliosa Bailey) growth in Cd- and Ni-contaminated soils. Lett Appl Microbiol 47:561–565

    Article  CAS  Google Scholar 

  • Jimtha JC, Smitha PV, Anisha C, Deepthi T, Meekha G, Radhakrishnan EK, Gayatri GP, Remakanthan A (2014) Isolation of endophytic bacteria from embryogenic suspension culture of banana and assessment of their plant growth promoting properties. Plant Cell Tiss Org 118:57–66

    Article  Google Scholar 

  • Ker K, Seguin P, Driscoll BT, Fyles JW, Smith DL (2014) Evidence for enhanced N availability during switchgrass establishment and seeding year production following inoculation with rhizosphere endophytes. Arch Agro Soil Sci 60:1553–1563

    Article  CAS  Google Scholar 

  • Koutroubas SD, Ntanos DA (2003) Genotypic differences for grain yield and nitrogen utilization in Indica and Japonica rice under Mediterranean conditions. Field Crop Res 83:251–260

    Article  Google Scholar 

  • Kraiser T, Gras DE, Gutierrez AG, Gonzalez B, Gutierrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466

    Article  CAS  Google Scholar 

  • Li X, Zhou Y, Mace W, Qin J, Liu H, Chen W, Ren A, Gao Y (2016) Endophytes species influence the biomass prodcution of the native grass Achnatherum sibiricum (L.) Keng under high nitrogen availability. Ecol Evol 6:8595–8606

    Article  Google Scholar 

  • Lin D, Fan X, Hu F, Zhao H, Luo J (2007) Ammonia volatilization and nitrogen utilization efficiency in response to urea application in rice fields of the Taihu lake region, China. Pedosphere 17:639–645

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Kang BG, Lee YJ, Chung JB, Sa TM (2010) Effect of co-inoculation of methylotrophic Methylobacterium oryzae with Azospirillum brasilense and Burkholderia pyrrocinia on the growth and nutrient uptake of tomato, red pepper and rice. Plant Soil 328:71–82

    Article  CAS  Google Scholar 

  • Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 55:27–34

    Article  CAS  Google Scholar 

  • Norman RJ, Stucki JW (1981) The determination of nitrate and nitrite in soil extracts by ultraviolet spectrophotometry. Soil Sci Soc Am J 45:347–353

    Article  CAS  Google Scholar 

  • Okubo T, Ikeda S, Sasaki K, Ohshima K, Hattori M, Sato T, Minamisawa K (2014) Phylogeny and functions of bacterial communities associated with field-grown rice shoots. Microbes Environ 29:329–332

    Article  Google Scholar 

  • Pan Y, Ni BJ, Yuan Z (2013) Modeling electron competition among nitrogen oxides reduction and N2O accumulation in denitrification. Environ Sci Technol 47:11083–11091

    Article  CAS  Google Scholar 

  • Patton CJ, Crouch SR (1977) Spectrophotometric and kinetics investigation of the berthelot reaction for the determination of ammonia. Anal Chem 49:464–469

    Article  CAS  Google Scholar 

  • Pedraza RO, Bellone CH, Bellone SC, Sorte PMFB, Teixeira KRS (2009) Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rained crop. Eur J Soil Biol 45:36–43

    Article  CAS  Google Scholar 

  • Robinson RJ, Fraaije BA, Clark IM, Jackson RW, Hirsch PR, Mauchline TH (2016) Endophytic bacterial community composition in wheat (Triticum aestivum) is determined by plant tissue type, developmental stage and soil nutrient availability. Plant Soil 405:381–396

    Article  CAS  Google Scholar 

  • Rose MT, Phuong TL, Nhan DK, Cong PT, Hien NT, Kennedy IR (2014) Up to 52% N fertilizer replaced by biofertilizer in lowland rice via farmer participatory research. Agron Sustain Dev 34:857–868

    Article  Google Scholar 

  • Saha P, Raychaudhhuri SS, Chakraborty A, Sudarshan M (2010) PIXE analysis of trace elements in relation to chlorophyll concentration in Plantago ovata Forsk. Appl Radiat Isotopes 68:444–449

    Article  CAS  Google Scholar 

  • Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Int 25:28–36

    Article  CAS  Google Scholar 

  • Shen T (1969) The induction of nitrate reductase and the preferential assimilation of ammonium in germinating rice seedlings. Plant Physiol 44:1650–1655

    Article  CAS  Google Scholar 

  • Silveira APD, Sala VMR, Cardoso EJBN, Labanca EG, Cipriano MAP (2016) Nitrogen metabolism and growth of wheat plant under diazotrophic endophyic bacteria inoculation. Appl Soil Ecol 107:313–319

    Article  Google Scholar 

  • Singh RK, Malik N, Singh S (2013) Impact of rhizobial inoculation and nitrogen utilization in plant growth promotion of maize (Zea mays L.) Nusan Biosci 5:8–14

    Google Scholar 

  • Suzuki MT, Giovannoni SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62:625–630

    CAS  Google Scholar 

  • Tian X, Cao L, Tan H, Han W, Chen M, Liu Y, Zhou S (2007) Diversity of cultivated and uncultivated actinobacterial endophytes in the stems and roots of rice. Microb Ecol 53:700–707

    Article  Google Scholar 

  • Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209 http://genomebiology.com/2013/14/6/209

    Article  Google Scholar 

  • Wallenstein MD, Myrold DD, Firestone M, Voytek M (2006) Environmental controls on denitrifying communities and denitrification rates: insights from molecular methods. Ecol Appl 16:2143–2152

    Article  Google Scholar 

  • Yao W, Byrne RH, Waterbury RD (1998) Determination of nanomolar concentration of nitrite and nitrate in natural waters using long path length absorbance spectroscopy. Environ Sci Technol 32:2646–2649

    Article  CAS  Google Scholar 

  • Yoshida M, Ishii S, Otsuka S, Senoo K (2009) Temporal shifts in diversity and quantity of nirS and nirK in a rice paddy field soil. Soil Biol Biochem 41:2044–2051

    Article  CAS  Google Scholar 

  • Zhu S, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333

    Article  Google Scholar 

Download references

Acknowledgements

This work was partly supported by grants from the Chinese National Natural Science Foundation (No. 41471181).

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Authors and Affiliations

  1. Department of Laboratory, Henan Provincial People’s Hospital, Zhengzhou, 450003, China

    Wenfeng Wang

  2. School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China

    Yanyan Zhai, Lixiang Cao & Hongming Tan

  3. School of Environmental Science and Engineering, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China

    Renduo Zhang

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  1. Wenfeng Wang
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  2. Yanyan Zhai
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  3. Lixiang Cao
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  4. Hongming Tan
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  5. Renduo Zhang
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Correspondence to Lixiang Cao or Renduo Zhang.

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Responsible editor: Philippe Garrigues

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Wang, W., Zhai, Y., Cao, L. et al. Improvement of rice seedling growth and nitrogen use efficiency by seed inoculation with endophytic denitrifiers. Environ Sci Pollut Res 24, 14477–14483 (2017). https://doi.org/10.1007/s11356-017-9064-8

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  • DOI: https://doi.org/10.1007/s11356-017-9064-8

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