SpringerLink
Log in

Quorum-Sensing Mechanism in Rhizobium sp.: Revealing Complexity in a Molecular Dialogue

  • Chapter
  • First Online:
Implication of Quorum Sensing System in Biofilm Formation and Virulence

Abstract

Nitrogen fixation by a biological process is an important phenomenon for improving agricultural soil fertility by fixing atmospheric nitrogen in the form of ammonia, which is mediated by the symbiotic association between Rhizobium species and leguminous plants. During symbiosis bacteria aggregate to form biofilms and coordinate their behavior in response to environmental conditions by a process called Quorum sensing (QS). The mechanism of quorum sensing depends on the interaction between signal molecule and a sensor that helps bacteria to communicate and regulate gene expression related to nodulation, biofilm formation and symbiosis and nitrogen fixation. Rhizobium utilizes N- acyl homoserine lactones (AHLs) as signalling molecules to coordinate and regulates gene expression. In addition to this, host response to bacteria is important to combat pathogenic bacteria and attract beneficial ones. For this leguminous plants sense the presence of bacteria precisely and release chemical compounds like flavonoids to make appropriate responses to symbiosis. The review clearly emphasizes interkingdom chemical signaling governing molecular interactions between leguminous plants and Rhizobium species in the establishment of symbiosis and nitrogen fixation.

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

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (Germany)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 117.69
Price includes VAT (Germany)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
EUR 160.49
Price includes VAT (Germany)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews, 68, 280–300.

    Article  CAS  Google Scholar 

  2. Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E., & Walker, G. C. (2007). How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nature Reviews Microbiology, 5, 619–633.

    Article  CAS  Google Scholar 

  3. Rinaudi, L. V., & Giordano, W. (2010). An integrated view of biofilm formation in rhizobia. FEMS Microbiology Letters, 304, 1–11.

    Article  CAS  Google Scholar 

  4. Hartmann, A., Rothballer, M., Hense, B. A., & Schröder, P. (2014). Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Frontiers in Plant Science, 5, 131.

    Article  Google Scholar 

  5. Wisniewski-Dye, F., & Downie, J. A. (2002). Quorum-sensing in Rhizobium. Antonie Van Leeuwenhoek, 81, 397–407.

    Article  CAS  Google Scholar 

  6. Schumpp, O., & Deakin, W. J. (2010). How inefficient rhizobia prolong their existence within nodules. Trends in Plant Science, 15, 189–195.

    Article  CAS  Google Scholar 

  7. Downie, J. A. (2010). The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiology Reviews, 34, 150–170.

    Article  CAS  Google Scholar 

  8. Long, S. R. (1996). Rhizobium symbiosis: Nod factors in perspective. Plant Cell, 8, 1885–1898.

    Article  CAS  Google Scholar 

  9. Ardourel, M., Demont, N., Debelle, F. D., et al. (1994). Rhizobium meliloti lipooligosaccharide nodulation factors – Different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell, 6, 1357–1374.

    Article  CAS  Google Scholar 

  10. D’Haeze, W., Mergaert, P., Prome, J. C., & Holsters, M. (2000). Nod factor requirements for efficient stem and root nodulation of the tropical legume Sesbania rostrata. The Journal of Biological Chemistry, 275, 15676–15684.

    Article  Google Scholar 

  11. Goormachtig, S., Capoen, W., & Holsters, M. (2004a). Rhizobium infection: Lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends in Plant Science, 9, 518–522.

    Article  CAS  Google Scholar 

  12. Goormachtig, S., Capoen, W., James, E. K., & Holsters, M. (2004b). Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proceedings of the National Academy of Sciences of the USA, 101, 6303–6308.

    Article  CAS  Google Scholar 

  13. Walker, S. A., & Downie, J. A. (2000). Entry of Rhizobium leguminosarum bv. Viciae into root hairs requires minimal nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Molecular Plant-Microbe Interactions, 13, 754–762.

    Article  CAS  Google Scholar 

  14. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Prom’e, J. C., & D’enari’e, J. (1990). Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature, 344, 781–784.

    Article  CAS  Google Scholar 

  15. Jitacksorn, S., & Sadowsky, M. J. (2008). Nodulation gene regulation and quorum sensing control density-dependent suppression and restriction of nodulation in the Bradyrhizobium japonicum–soybean symbiosis. Applied and Environmental Microbiology, 74, 3749–3756.

    Article  CAS  Google Scholar 

  16. McIver, J., Djordjevic, M. A., Weinman, J. J., Bender, G. L., & Rolfe, B. G. (1989). Extension of host range of Rhizobium leguminosarum bv. trifolii caused by point mutations in nodD that result in alterations in regulatory function and recognition of inducer molecules. Molecular Plant-Microbe Interactions, 2, 97–106.

    Article  CAS  Google Scholar 

  17. Radutoiu, S., Madsen, L. H., Madsen, E. B., et al. (2003). Plant recognition of symbiotic bacteria requires two LysM receptorlike kinases. Nature, 425, 585–592.

    Article  CAS  Google Scholar 

  18. Oldroyd, G. E. D., & Downie, J. A. (2004). Calcium, kinases and nodulation signalling in legumes. Nature Reviews Molecular Cell Biology, 5, 566–576.

    Article  CAS  Google Scholar 

  19. Lohar, D. P., Sharopova, N., Endre, G., Peñuela, S., Samac, D., Town, C., et al. (2006). Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiology, 140, 221–234.

    Article  CAS  Google Scholar 

  20. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., & Lappin-Scott, H. M. (1995). Microbial biofilms. Annual Review of Microbiology, 49, 711–745.

    Article  CAS  Google Scholar 

  21. Fraysse, N., Couderc, F., & Poinsot, V. (2003). Surface polysaccharide involvement in establishing the Rhizobium–legume symbiosis. European Journal of Biochemistry, 270, 1365–1380.

    Article  CAS  Google Scholar 

  22. Dazzo, F. B., Truchet, G. L., Sherwood, J. E., Hrabak, E. M., Abe, M., & Pankratz, S. H. (1984). Specific phases of root hair attachment in the Rhizobium trifolii–clover symbiosis. Applied and Environmental Microbiology, 48, 1140–1150.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Laus, M. C., Logman, T. J., Lamers, G. E., Van Brussel, A. A. N., Carlson, R. W., & Kijne, J. W. (2006). A novel polar surface polysaccharide from Rhizobium leguminosarum binds host plant lectin. Molecular Microbiology, 59, 1704–1713.

    Article  CAS  Google Scholar 

  24. Russo, D. M., Williams, A., Edwards, A., et al. (2006). Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. Journal of Bacteriology, 188, 4474–4486.

    Article  CAS  Google Scholar 

  25. Williams, A., Wilkinson, A., Krehenbrink, M., Russo, D. M., Zorreguieta, A., & Downie, J. A. (2008). Glucomannan-mediated attachment of rhizobium leguminosarum to pea root hairs is required for competitive nodule infection. Journal of Bacteriology, 190, 4706–4715.

    Article  CAS  Google Scholar 

  26. Mongiardini, E. J., Ausmees, N., Perez-Gimenez, J., Althabegoiti, M. J., Quelas, J. I., Lopez-Garcia, S. L., & Lodeiro, A. R. (2008). The rhizobial adhesion protein RapA1 is involved in adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiology Ecology, 65, 279–288.

    Article  CAS  Google Scholar 

  27. Verstraeten, N., Braeken, K., Debkumari, B., Fauvart, M., Fransaer, J., Vermant, J., & Michiels, J. (2008). Living on a surface: Swarming and biofilm formation. Trends in Microbiology, 16(10), 496–506.

    Article  CAS  Google Scholar 

  28. Gonzalez, J. E., & Marketon, M. M. (2003). Quorum sensing in nitrogen-fixing rhizobia. Microbiology and Molecular Biology Reviews, 67, 574–592.

    Article  CAS  Google Scholar 

  29. Danino, V. E., Wilkinson, A., Edwards, A., & Downie, J. A. (2003). Recipient-induced transfer of the symbiotic plasmid pRL1JI in Rhizobium leguminosarum bv. Viciae is regulated by a quorum-sensing relay. Molecular Microbiology, 50, 511–525.

    Article  CAS  Google Scholar 

  30. Lithgow, J. K., Wilkinson, A., Hardman, A., Rodelas, B., Wisniewski Dye, F., Williams, P., & Downie, J. A. (2000). The regulatory locus cinRI in rhizobium leguminosarum controls a network of quorum-sensing loci. Molecular Microbiology, 37, 81–97.

    Article  CAS  Google Scholar 

  31. Rodelas, B., Lithgow, J. K., Wisniewski-Dyé, F., Hardman, A., Wilkinson, A., Economou, A., Williams, P., & Downie, J. A. (1999). Analysis of quorum-sensing-dependent control of rhizosphere-expressed (rhi) genes in Rhizobium leguminosarum bv. Viciae. Journal of Bacteriology, 181, 3816–3823.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Wisniewski-Dyé, F., & Allan Downie, J. (2002). Quorum sensing in Rhizobium. Antonie Van Leeuwenhoek, 81, 397–407. https://doi.org/10.1023/A:1020501104051.

    Article  PubMed  Google Scholar 

  33. Cubo, M. T., Economou, A., Murphy, G., Johnston, A. W., & Downie, J. A. (1992). Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. Journal of Bacteriology, 174, 4026–4035.

    Article  CAS  Google Scholar 

  34. Dibb, N. J., Downie, J. A., & Brewin, N. J. (1984). Identification of a rhizosphere protein encoded by the symbiotic plasmid of Rhizobium leguminosarum. Journal of Bacteriology, 158, 621–627.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Wilkinson, A., Danino, V., Wisniewski-Dye, F., Lithgow, J. K., & Downie, J. A. (2002a). N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. Journal of Bacteriology, 184, 4510–4519.

    Article  CAS  Google Scholar 

  36. Edwards, A., Frederix, M., Wisniewski-Dye, F., Jones, J., Zorreguieta, A., & Downie, J. A. (2009). The cin and rai quorum-sensing regulatory systems in Rhizobium leguminosarum are coordinated by ExpR and CinS, a small regulatory protein coexpressed with CinI. Journal of Bacteriology, 191, 3059–3067.

    Article  CAS  Google Scholar 

  37. Zorreguieta, A., Finnie, C., & Downie, J. A. (2000). Extracellular glycanases of Rhizobium leguminosarum are activated on the cell surface by an exopolysaccharide-related component. Journal of Bacteriology, 182, 1304–1312.

    Article  CAS  Google Scholar 

  38. Sanchez-Canizares, C., & Palacios, J. (2013). Construction of a marker system for the evaluation of competitiveness for legume nodulation in Rhizobium strains. Journal of Microbiological Methods, 92. https://doi.org/10.1016/j.mimet.2012.12.022.

    Article  Google Scholar 

  39. Teplitski, M., Robinson, J. B., & Bauer, W. D. (2000). Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Molecular Plant-Microbe Interactions, 13, 637–648.

    Article  CAS  Google Scholar 

  40. Gao, M. S., Teplitski, M., Robinson, J. B., & Bauer, W. D. (2003). Production of substances by Medicago truncatula that affect bacterial quorum sensing. Molecular Plant-Microbe Interactions, 16, 827–834.

    Article  CAS  Google Scholar 

  41. Daniels, R., De Vos, D. E., Desair, J., et al. (2002). The cin quorum sensing locus of Rhizobium etli CNPAF512 affects growth and symbiotic nitrogen fixation. The Journal of Biological Chemistry, 277, 462–468.

    Article  CAS  Google Scholar 

  42. Deakin, W. J., & Broughton, W. J. (2009). Symbiotic use of pathogenic strategies: Rhizobial protein secretion systems. Nature Reviews Microbiology, 7, 312–321.

    Article  CAS  Google Scholar 

  43. Okazaki, S., Kaneko, T., Sato, S., & Saeki, K. (2013). Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proceedings of the National Academy of Sciences of the United States of America, 110, 17131–17136.

    Article  CAS  Google Scholar 

  44. Bozsoki, Z., Cheng, J., Feng, F., Gysel, K., Vinther, M., Andersen, K. R., et al. (2017). Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. Proceedings of the National Academy of Sciences of the United States of America, 114, 8118–8127.

    Article  Google Scholar 

  45. Zipfel, C., & Oldroyd, G. E. (2017). Plant signalling in symbiosis and immunity. Nature, 543, 328–336.

    Article  CAS  Google Scholar 

  46. Cao, Y., Halane, M. K., Gassmann, W., & Stacey, G. (2017). The role of plant innate immunity in the legume-Rhizobium symbiosis. Annual Review of Plant Biology, 68, 535–561. https://doi.org/10.1146/annurev-arplant-042916-041030.

    Article  CAS  PubMed  Google Scholar 

  47. Jones, K. M., Sharopova, N., Lohar, D. P., Zhang, J. Q., VandenBosch, K. A., & Walker, G. C. (2008). Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proceedings of the National Academy of Sciences USA, 105, 704–709.

    Article  CAS  Google Scholar 

  48. Liang, Y., Cao, Y., Tanaka, K., Thibivilliers, S., Wan, J., Choi, J., et al. (2013). Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science, 341, 1384–1387.

    Article  CAS  Google Scholar 

  49. Wang, Q., Liu, J., & Zhu, H. (2018). Genetic and molecular mechanisms underlying symbiotic specificity in legume-Rhizobium interactions. Frontiers in Plant Science, 9, 313.

    Article  Google Scholar 

Download references

Acknowledgments

The Corresponding author is thankful to Department of Science and Technology (DST), New Delhi for providing financial support (LS1246/2015).

Author information

Authors and Affiliations

  1. CSIR-Indian Institute of Chemical Technology, Hyderabad, Telangana, India

    R. N. Amrutha & R. S. Prakasham

  2. Department of Biotechnology, Krishna University, Machilipatnam, Andhra Pradesh, India

    Pallaval Veera Bramhachari

Authors
  1. R. N. Amrutha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pallaval Veera Bramhachari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. S. Prakasham
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Biotechnology, Krishna University, Machilipatnam, Andhra Pradesh, India

    Pallaval Veera Bramhachari

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Amrutha, R.N., Pallaval Veera Bramhachari, Prakasham, R.S. (2018). Quorum-Sensing Mechanism in Rhizobium sp.: Revealing Complexity in a Molecular Dialogue. In: Pallaval Veera Bramhachari (eds) Implication of Quorum Sensing System in Biofilm Formation and Virulence. Springer, Singapore. https://doi.org/10.1007/978-981-13-2429-1_16

Download citation

Publish with us

Policies and ethics

Search

Navigation