Skip to main content
SpringerLink
Log in

Detection of endophytic association between Aeschynomene nodulating Bradyrhizobium sp. and traditional Desariya rice roots under rice-Aeschynomene ecosystem of chaur land, Bihar, India

  • Original Paper
  • Published:
Biologia Futura Aims and scope Submit manuscript

Abstract

Engineering diazotrophic rice having either an integral component of diazotrophic microbes or placing microbial origin nif gene to the rice plant is the dream of biotechnologist. Rice-Aeschynomene ecosystem of pristine chaur land provides a suitable niche to search Rhizobium endophytes in rice. Accordingly, the work was initiated to search suitable endophytic Rhizobium strain for artificial symbiosis within the roots of Desariya rice and its source through morphological, biochemical and molecular approaches. Detection of Acetylene reduction assay (ARA) activity in sterilized Desariya rice root confirmed the presence of putative diazotrophic endophytes in rice root. Isolates from Aeschynomene aspera L. nodulating and Desariya rice endophytic Rhizobium were evaluated for growth, IAA, morphological and biochemical features. Carbon profiling pattern of both these isolates indicated that Desariya rice endophytic Rhizobium has its similarity with Aeschynomene aspera L. nodulating Rhizobium. 16S rRNA gene sequencing confirmed the presence of endophytic Bradyrhizobium sp. in Desariya rice roots and its similarity with Aeschynomene aspera L. nodulating Bradyrhizobium. Desariya rice Bradyrhizobium may be an ideal candidate in the future for creating artificial symbiosis in rice due to its similarity with Aeschynomene aspera L. Bradyrhizobium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alazard D (1985) Stem and root nodulation in Aeschynomene spp. Appl Environ Microbiol 50:732–734

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alazard D, Duhoux E (1990) Development of stem nodules in a tropical forage legume, Aeschynomeneafraspera. J Exp Bot 41:1199–1206

    Google Scholar 

  • Alazard D, Becker M (1987) Aeschynomene as green manure for rice. Plant Soil 101:141–143

    Google Scholar 

  • Austin RB (1999) Yield of wheat in the United Kingdom: recent advances and prospects. Crop Sci 39:1604–1610

    Google Scholar 

  • Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H (2008) Divergence of evolutionary ways among common symgenes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signaling pathway. Plant Cell Physiol 49:1659–1671

    CAS  PubMed  Google Scholar 

  • Bennett J, Ladha JK (1992) Introduction: feasibility of nodulation and nitrogen fixation in rice. In: Khus GS, Bennett J (eds) nodulation and nitrogen fixation in rice. IRRI, Philippines, pp 1–14

    Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobium inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650

    CAS  Google Scholar 

  • Ceccarelli S (2015) Efficiency of plant breeding. Crop Sci 55:87–97

    Google Scholar 

  • Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, De Lajudie P, Dreyfus B (2000) Photosynthetic Bradyrhizobia are natural endophytes of the African wild rice Oryzabreviligulata. Appl Environ Microbiol 66:5437–5447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conforti P (2011) Looking ahead in world food and agriculture: perspectives to 2050. Food and Agriculture Organization of the United Nations (FAO)

  • Dawe D (2000a) The contribution of rice research to poverty alleviation. In: Sheehy JE, Mitchell PL, Hardy B (eds) Studies in plant science. Redesigning rice photosynthesis to increase yield. Proceedings of the workshop on the quest to reduce hunger: Redesigning rice photosynthesis, 30 Nov.-3 Dec. 1999, Los Banos, Philippines, Makati city (Philippines): International Rice Research Institute and Amsterdam (The Netherlands): Elsevier Science B.V. vol 7. pp 3–12

  • Dawe D (2000b) The potential role of biological nitrogen fixation in meeting future demand for rice and fertilizer. In: Thequestfor nitrogen fixationin rice, Proceedings of the third working group meetingon assessing opportunities for nitrogen fixation in rice, Banos Laguna, Philippines, Makati City, Philippines, 9–12 Aug. 1999; International Rice Research Institute, Banos Laguna, Philippines, Makati City, Philippines, 1

  • Dawson JC, Huggins DR, Jones SS (2008) Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crops Res 107:89–101

    Google Scholar 

  • Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, Martin W, Dagan T (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 25:748–761

    CAS  PubMed  Google Scholar 

  • Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17:7843–7853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrlich PR, Harte J (2015) Opinion: to feed the world in 2050 will require a global revolution. Proc Natl Acad Sci 112:14743–14744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elsheikh EAE, Wood M (1989) Response of chickpea and soybean rhizobia to salt: influence of carbon source, temperature and pH. Soil Biol Biochem 21:883–887

    Google Scholar 

  • Gachande BD, Khansole GS (2011) Morphological, cultural and biochemical characteristics of Rhizobium japonicumsyn and Bradyrhizobium japonicum of’ soybean. Biosci Discov 2:1–4

    Google Scholar 

  • Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    CAS  PubMed  PubMed Central  Google Scholar 

  • Geurts R, Lillo A, Bisseling T (2012) Exploiting an ancient signalling machinery to enjoy a nitrogen fixing symbiosis. Curr Opin Plant Biol 15:438–443

    PubMed  Google Scholar 

  • Giraud E, Fleischman D (2004) Nitrogen-fixing symbiosis between photosynthetic bacteria and legumes. Photosynth Res 82(2):115–130

    CAS  PubMed  Google Scholar 

  • Holm LG, Holm L, Holm E, Pancho JV, Herberger JP (1997) World weeds: natural histories and distribution. Wiley, New York

    Google Scholar 

  • Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology. Williams and Wilkins Press, Baltimore

    Google Scholar 

  • Isawa T, Hiruma N, Imada T, Noda M, Kurihara Y, Kon M (2006) Japan agriculture forestry, fisheries ministry and mayekawa manufacturing Co. Rice containing endophytic bacteria and method of producing it. U. S. Patent no. 7,084,331.

  • Jacobsen SE, Sørensen M, Pedersen SM, Weiner J (2013) Feeding the world: genetically modified crops versus agricultural biodiversity. Agron Sustain Dev 33:651–662

    Google Scholar 

  • Javed K, Asghari B (2008) Potential allelopathic effects of sunflowers on microorganisms. Afr J Biotechnol 7:4208–4211

    Google Scholar 

  • Jha MN, Mishra SK (2004) Transgenicdiazotroph: an Indian prospctive. Indian J Biotec 3:502–510

    Google Scholar 

  • Jha MN, Prasad AN, Misra SK (2002) A step towards artificial symbiosis by Nostochatei in rice. Asian J Microbiol Biotechnol Envrion Sci 4:567–569

    Google Scholar 

  • Jha MN, Prasad AN, Sharma SG, Bharati RC (2001) Effects of fertilization rate and crop rotation on diazotrophic cyanobacteria in paddy field. World J Microbiol Biotechnol 17:463–468

    CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kundu DK, Ladha JK (1995) Efficient management of soil and biologically fixed N2 in intensively-cultivated rice fields. Soil Biol Biochem 27:431–439

    CAS  Google Scholar 

  • Ladha JK, Barraquio WL, Revilla L (1997) Isolation of endophyticdiazotrophic bacteria from wetland rice. In: Opportunities for biological nitrogen fixation in rice and other non-legumes. Springer, Dordrecht, pp 15–24

  • Ladha JK, Reddy PM (1995) Extension of nitrogen fixation to rice-necessity and possibilities. Geo J 35:363–372

    Google Scholar 

  • Ladha JK, So RB (1994) Numerical taxonomy of photosynthetic rhizobia nodulating Aeschynomene species. Int J Syst Evol Microbio 44:62–73

    Google Scholar 

  • Mae T (1997) Physiological nitrogen efficiency in rice: nitrogen utilization, photosynthesis and yield potential. Plant Soil 196:201–210

    CAS  Google Scholar 

  • Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: Hownovel are nodules? Trends Plant Sci 14:77–86

    CAS  PubMed  Google Scholar 

  • Meena RS, Vijayakumar V, Yadav GS, Mitran T (2018) Response and interaction of Bradyrhizobium japonicum and arbuscularmycorrhizal fungi in the soybean rhizosphere. Plant Growth Regul 84:207–223

    CAS  Google Scholar 

  • Miché L, Moulin L, Chaintreuil C, Contreras-Jimenez JL, Munive-Hernández JA, Del Carmen V-H, Crozier F, Béna G (2010) Diversity analyses of Aeschynomenesymbionts in Tropical Africa and Central America reveal that nod-independent stem nodulation is not restricted to photosynthetic Bradyrhizobia. Environ Microbiol 12:2152–2164

    PubMed  Google Scholar 

  • Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B, Gillis M, deLajudie P, Masson-Boivin C (1999) Photosynthetic bradyrhizobia from Aeschynomene spp. are specific to stem-nodulated species and form a separate 16S ribosomal DNA restriction fragment length polymorphism group. Appl Environ Microbiol 65:3084–3094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M (2009) Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol 181:950–959

    CAS  PubMed  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Normanly J, Cohen JD, Fink GR (1993) Arabidopsis thalianaauxotrophs reveal atryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc Natl A Sci 90:10355–10359

    CAS  Google Scholar 

  • Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328

    CAS  PubMed  Google Scholar 

  • Piromyou P, Greetatorn T, Teamtisong K, Okubo T, Shinoda R, Nuntakij A, Tittabutr P, Boonkerd N, Minamisawa K, Teaumroong N (2015) Preferential association of endophyticBradyrhizobia with different rice cultivars and its implications for rice endophyte evolution. Appl Environ Microbiol 81:3049–3061

    CAS  PubMed  PubMed Central  Google Scholar 

  • Piromyou P, Songwattana P, Greetatorn T, Okubo T, Kakizaki KC, Prakamhang J, Tittabutr P, Boonkerd N, Teaumroong N, Minamisawa K (2015) The type III secretion system (T3SS) is a determinant for rice-endophyte colonization by non-photosynthetic Bradyrhizobium. Microbes Environ 30(4):291–300

    PubMed  PubMed Central  Google Scholar 

  • Rosegrant MW, Agcaoili-Sombilla MC, Perez ND (1995) Global food projections to 2020: implications for investment. Diane Publishing, Darby, PA

    Google Scholar 

  • Sarkar D, Laha S (2013) Production of phytohormone auxin (IAA) from soil bornrhizobiumsp, isolated from different leguminous plant. Int J Appl Environ Sci 8:521–528

    Google Scholar 

  • Sarwar M, Frankenberger WT (1994) Influence of L-tryptophan and auxins applied to the rhizosphere on the vegetative growth of Zea mays L. Plant Soil 160:97–104

    CAS  Google Scholar 

  • Sautter C, Poletti S, Zhang P, Gruissem W (2006) Biofortification of essential nutritional compounds and trace elements in rice and cassava. ProcNutrSoc 65:153–159

    CAS  Google Scholar 

  • Seck PA, Diagne A, Mohanty S, Wopereis MC (2012) Crops that feed the world 7: rice. Food Secur 4:7–24

    Google Scholar 

  • Singh B, Ravneet K, Kashmir S (2008) Characterization of Rhizobium strain isolated from the roots of Trigonellafoenumgraecum (fenugreek). Afr J Biotechnol 7:3671–3676

    CAS  Google Scholar 

  • Songwattana P, Noisangiam R, Teamtisong K, Prakamhang J, Teulet A, Tittabutr P, Piromyou P, Boonkerd N, Giraud E, Teaumroong N (2017) Type 3 secretion system (T3SS) of Bradyrhizobium sp. DOA9 and its roles in legume symbiosis and rice endophytic association. Front Microbiol 8:1810

    PubMed  PubMed Central  Google Scholar 

  • Stoltzfus JR, So RMPP, Malarvithi PP, Ladha JK, De Bruijn FJ (1997) Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant Soil 194:25–36

    CAS  Google Scholar 

  • SubbaRao NS (1988) Microbiological aspects of green manure in lowland rice soils. In: International Rice Research Institute Green manureinrice farming, IRRI, Los Banos, Philippines, 131–149.

  • SubbaRao NS, Tilak KVR, Singh CS (1988) Root nodulation studies in Aeschynomeneaspera. Plant Soil 56:491–494

    Google Scholar 

  • Thrall PH, Bever JD, Slattery JF (2008) Rhizobium mediation of Acacia adaptation to soil salinity: Evidence of underlying trade-offs and tests of expected pattern. J Ecol 96:746–755

    Google Scholar 

  • Turbé A, De Toni A, Benito P, Lavelle P, Lavelle P, Camacho NR, Van DerPutten WH, Labouze E, Mudgal S (2010) Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service, IRD, and NIOO, Report for European Commission, DG Environment.

  • Van Loon L, Bakker PAHM (2003) Signalling in rhizobacteria-plant interactions. In: Root ecology. Springer, Berlin, pp 297–330

  • Vincent JM, Nutman PS, Skinner FA (1979) The identification and classification of Rhizobium. In: Identification methods for microbiology, 2nd ed. SocApplBacteriol Tech Ser, vol 14, pp 49–69

  • Wang Q, Quensen JF, Fish JA, Lee TK, Sun Y, Tiedje JM, Cole JR (2013) Ecological patterns of nifH genes in four terrestrial climatic zones explored with targeted metagenomics using Frame Bot, a new informatics tool. MBio 4:e00592-13. https://doi.org/10.1128/mBio.00592-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav AN, Verma P, Kumar M, Pal KK, Dey R, Gupta A, Padaria JC, Gujar GT, Kumar S, Suman A, Prasanna R (2015) Diversity and phylogenetic profiling of niche-specific Bacilli from extreme environments of India. Ann Microbiol 65:611–629

    Google Scholar 

  • Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D, Schmidt TM (1997) Natural endophytic association between Rhizobium leguminosarumbv. trifolii and rice roots and assessment of its potential to promote rice growth. In: Opportunities for biological nitrogen fixation in rice and other non-legumes. Springer, Dordrecht, pp 99–114

Download references

Acknowledgements

The authors are thankful to ICAR New Delhi for providing financial support through AINP-Soil Biodiversity and Biofertilizers project. The Department of Microbiology, College of Basic Sciences & Humanities, Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar, India, are gratefully acknowledged for their support during the present study. All authors are also thankful to ICAR-Central Arid Zone Research Institute for the support during publication.

Funding

This research was funded by Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar, India, and the Indian Council of Agricultural Research, New Delhi, India.

Author information

Authors and Affiliations

  1. Department of Microbiology, College of Basic Sciences and Humanities, Dr. Rajendra Prasad Central Agricultural University, Pusa, Samastipur, Bihar, 848125, India

    Abhilasha Rai, Manindra Nath Jha, Devendra Singh & Sanjeet Kumar Chaurasia

  2. ICAR—Central Arid Zone Research Institute, Jodhpur, Rajasthan, 342003, India

    Devendra Singh

  3. ICAR-National Bureau of Agriculturally Important Microorganisms, Kushmaur, MaunathBhanjan, Uttar Pradesh, 275103, India

    Shobit Thapa

  4. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Gopaljee Jha

Authors
  1. Abhilasha Rai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manindra Nath Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Devendra Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shobit Thapa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sanjeet Kumar Chaurasia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gopaljee Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization was performed by Manindra Nath Jha and Devendra Singh. Data curation was performed by Sanjeet Kumar Chaurasia. Abhilasha Rai collected data. Manuscript was written by Devendra Singh. Devendra Singh also performed statistical analysis of data. Gopaljee Jha performed the 16 s rRNA gene sequencing of rhizobium isolates. Final review editing was done by Manindra Nath Jha and Shobit Thapa. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Devendra Singh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rai, A., Jha, M.N., Singh, D. et al. Detection of endophytic association between Aeschynomene nodulating Bradyrhizobium sp. and traditional Desariya rice roots under rice-Aeschynomene ecosystem of chaur land, Bihar, India. BIOLOGIA FUTURA 73, 95–105 (2022). https://doi.org/10.1007/s42977-021-00105-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42977-021-00105-0

Keywords

Search

Navigation