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Research Article

volume 43 issue 6 (december 2020) : 872-877,   Doi: 10.18805/LR-527

Contribution to the Study of the Relationship between Gammaproteobacteria and Rhizobia in Legume Species of the Genus Hedysarum

T
Torche Esma
R
Rouabhi Ahlem
T
Torche Boutheina
S
Slatnia Soumia
G
Gharzouli Razika
B
Benhizia Hayet
B
Benhizia Yacine
B
Benguedouar Ammar
1Faculté des Sciences de la Nature et de la Vie et des Sciences de la Terre et de l’Univers, Université 8 Mai 1945 Guelma, Guelma, Algeria. 

  • Submitted19-09-2019|

  • Accepted16-01-2020|

  • First Online 15-05-2020|

  • doi 10.18805/LR-527

Cite article:- Esma Torche, Ahlem Rouabhi, Boutheina Torche, Soumia Slatnia, Razika Gharzouli, Hayet Benhizia, Yacine Benhizia, Ammar Benguedouar (2020). Contribution to the Study of the Relationship between Gammaproteobacteria and Rhizobia in Legume Species of the Genus Hedysarum. Legume Research. 43(6): 872-877. doi: 10.18805/LR-527.

ABSTRACT

The nodular contents of the leguminous species of the genus Hedysarum (H. carnosum, H. spinosissimum subsp capitatum and H. pallidum) consist of cultivable bacteria belonging to the class Gammaproteobacteria, while the rhizobia of these leguminous species are not cultivable. Rhizobium sulla is the specific micro-symbiont of the H. coronarium leguminous species. The aim of this study is to see if the Gammaproteobacteria that inhabit the nodules of the three species of the genus Hedysarum (H. carnosum, H. spinosissimum subsp capitatum and H. pallidum) could have acquired the symbiotic criteria from rhizobia and cause nodulation in these host legume species by the transformation process. Transformation is carried out by extracting the plasmid DNA from the R. sulla strain and incorporate it into the bacterial strains of the Gammaproteobacteria class. Nodulation assay is performed to evaluate the ability of transformed strains to cause nodulation in legume species. The results showed that although there has been a transformation, there is a total failure of nodulation in the three legume species. This is explained by the specificity of molecular signals between bacteria and host plants as well as the genetic information carried by the plasmid is not sufficient to achieve a complete symbiotic relationship.

REFERENCES

  1. Abdelguerfi-Berrekia, R., Abdelguerfi, A., Bounaga, N.. Guittonneau, G.G. (1988). Contribution à l’étude des espèces spontanées du genre Hedysarum L. en Algérie. Ann. Inst. Nat. Agro. El-Harrach. 12: 191-219. 
  2. Abdelguerfi-Berrekia, R., Abdelguerfi, A., Bounaga, N.. Guittonneau, G.G. (1991). Répartition des espèces spontanées du genre Hedysarum selon certains facteurs du milieu en Algérie. Fourrages. 126: 187-207. 
  3. Benguedouar, A. (2000). Etude de la symbiose : Rhizobium –    Hedysarum coronarium. Essai de la caractérisation de l’espèce Rhizobium hedysary. Thèse de doctorat de l’université de Constantine, Algérie. 
  4. Benhizia, Y. (2006). Caractérisation phénotypique et phylogénétique des bactéries associées aux nodules de la légumineuse du genre Hedysarum: H.carnosum Desf., Hspinossissimum subsp.capitatum Desf. Et H.pallidum Desf. Thèse de doctorat d’état en microbiologie appliquée., Université Mentouri Constantine. 
  5. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A. and Squartini, A. (2004). Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol. 27(4): 462-468. 
  6. Benselama, A., Tellah S, Ourem F, and Ounane S. (2018). Characterization of rhizobia from root nodule and rhizosphere of Vicia faba in Algeria. Legume Research: An International Journal. 41(4): 624-628 
  7. Beringer, J.E. (1974). R-Factor transfer in rhizobium legume. J. Gen. Microbiol. 84: 188-198.
  8. Birnboim, H.C. (1983). A rapid alkaline extraction method for the isolation of plasmid DNA. Methods Enzymol. 100: 243 -    255.
  9. Caetano-Anolles, G., Lagares, A., and Bauer, W. D. (1990). Rhizobium meliloti exopolysaccharide Mutants Elicit Feedback Regulation of Nodule Formation in Alfalfa1. Plant Physiol. 92 (2): 368-374. 
  10. Casella, S., Gault, R.R., Reynolds, K.C., Dyson, J.R., Brockwell, J. (1984). Nodulation studies on legumes exotic to Australia: Hedysarum coronarium. FEMS. Microbial. Lett. 22: 37-45. 
  11. Castellane, T. C. L., Campanharo, J. C., Colnago, L. A., Coutinho, I. D., Lopes, É. M., Lemos, M. V. F. and de Macedo Lemos, E. G. (2017). Characterization of new exopolysaccharide production by Rhizobium tropici during growth on hydrocarbon substrate. International Journal of Biological Macromolecules. 96: 361-369. 
  12. Chataigné, G. (2007). Détermination structurale des lipopolysaccharides de surface chez Sinorhizobium. Doctorat en Chimie-Biologie-    Santé. Université Toulouse III. 
  13. Chuang -Yien Lee, J. (2000). Expression Studies on the exo Y Promoter Region in Rhizobium meliloti. Bug Journal. 3. 
  14. Ding, H. and Hynes, M. F. (2009). Plasmid transfer systems in the rhizobia. Can J Microbiol. 55(8): 917-927. 
  15. Dudeja, S.S., Sheokand, S. and Kumari, S. (2012). Legume root nodule development and functioning under tropics and subtropics: perspectives and challenges. Legume Research: An International Journal. 35(2): 85-103. 
  16. Fähreus, A. (1957). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16: 354-381. 
  17. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev. 68(2): 280-300. 
  18. Gharzouli, R. (2006). Influence d’agents mutagènes, les rayons Ultra-violet, sur la nodulation et les caractères phénotipiques de quelques espèces de Rhizobium sp. Mémoire de Magister en génétique moléculaire., Université Constantine. Algérie. 
  19. Gharzouli, R. (2013). Etude Structurale et Génétique des Exopolysaccharides produits par l’espèce Rhizobium sullae. Doctorat En Sciences, Constantine. 
  20. Ghosh, P.K. and Maiti, T.K. (2016). Structure of extracellular polysaccharides (EPS) produced by rhizobia and their functions in legume–bacteria symbiosis: A Review. Achievements in the Life Sciences. 10(2): 136-143. 
  21. Girija, D., Panchami, P.S., Praveena, E., Jose, T.S. and Sneha, N.S. (2018). Isolation and characterization of native cowpea rhizobia from Wayanad India. Legume Research: An International Journal. doi: 10.18805/LR-3951.
  22. Hirsch, A. M., Lum, M. R. and Downie, J. A. (2001). What Makes the Rhizobia-Legume Symbiosis So Special? Plant Physiology. 127(4):1484-1492. 
  23. Ibanez, F., Reinoso, H. and Fabra, A. (2010). Experimental evidences of pSym transfer in a native peanut-associated rhizobia. Microbiol Res. 165(6): 505-515. 
  24. Janczarek, M., and Skorupska, A. (2003). Exopolysaccharide synthesis in Rhizobium leguminosarum bv. trifolii is related to various metabolic pathways. Research in Microbiology. 154(6): 433-442. 
  25. Leigh, J. A., and Lee, C. C. (1988). Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. J Bacteriol. 170(8): 3327-3332. 
  26. Morgante, C., Castro, S, Fabra, A. (2005). Role of rhizobial exopolysaccharides in crack entry/intercellular infection of peanut. Soil Biology and Biochemistry. 37(8): 1436-1444. 
  27. Muresu, R., Polone, E., Sulas, L., Baldan, B., Tondello, A., Delogu, G., Cappuccinelli, P., Alberghini, S., Benhizia, Y., Benhizia, H., Benguedouar, A., Mori, B., Calamassi, R., Dazzo, F. B. and Squartini, A. (2008). Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol. 63(3): 383-400. 
  28. Navarini, L., Stredansky, M., Matulova, M. and Bertocchi, C. (1997). Production and characterization of an exopolysaccharide from Rhizobium hedysari HCNT 1. [journal article]. Biotechnology Letters. 19(12): 1231-1234. 
  29. Pelmont, J. (1995). Bactéries et environnement: Adaptation physiologique. (Vol. 2): Office des Publications Universitaires.
  30. Raposeiras, R., Patrícia, P.P.P., Raul, V.M., Lucy, S., Paiva, E., Scotti, M.R. and Sá, N.M.H. (2002). Variability of isolated colonies in bean nodulating Rhizobium strains before and after exposure to high temperature. Brazilian Journal of Microbiology. 33(2): 149-154.
  31. Senthil, K., M, Lakshmi, K. S., and Annapurna, K. (2017). Exopolysaccharide from Rhizobia: Production and Role in Symbiosis. Rhizobium Biology and Biotechnology. 50: 257-292 
  32. Singh, Z. and Singh, G. (2018). Role of Rhizobium in chickpea (Cicer arietinum) production-A review. Agricultural Reviews. 39(1): 31-39.
  33. Squartini, A., Struffi, P., Doring, H., Selenska-Pobell, S., Tola, E., Giacomini, A., Vendramin, E., Velazquez, E., Mateos, P.F., Martinez-Molina, E., Dazzo, F.B., Casella, S. and Nuti, M.P. (2002). Rhizobium sullae sp. nov. (formerly ‘Rhizobium hedysari’), the root-nodule microsymbiont of Hedysarum coronarium L. Int J Syst Evol Microbiol. 52(4): 1267-1276. 
  34. Strufi, P., Corich, V., Giacomini, A., Benguedouar, A., Squartini, A., and Casella, S. and Nuti, M.P. (1998). Metabolic properties, stress tolerance and macromolecular profiles of rhizobia nodulating Hedysarum coronarium. J Appl Microbiol. 84: 81- 89. 
  35. Tejerizo, G. T., Del Papa, M. F., Giusti, M. I. A., Draghi, W., Lozano, M., Lagares, A. and Pistorio, M. (2010). Characterization of extrachromosomol replicons present in the extended host range Rhizobium. sp. LPU83. Plasmid. 64: 177-185. 
  36. Tondello, A., Villani, M., Alessandrini, A., Baldan, B. and Squartini, A. (2011). Identification of the root nodule symbiont of the rare legume species Hedysarum confertum Desf. (Hedysarum humile L.) in its Italian relictual site. Plant Biosytems. 145: 901-905. 
  37. Torche, (2006). Isolement et caractérisation des bactéries nodulant les légumineuses du genre Hedysarum. Magister Biochimie microbiologie appliquée, université Mentouri Constantine. 
  38. Torche, A., Benhizia, H., Rosselli, R., Romoli, O., Zanardo, M., Baldan, E., Alberghini, S., Tondello, A., Baldan, B., Benguedouar, A., Squartini, A., and Benhizia, Y. (2014). Characterization of bacteria associated with nodules of two endemic legumes of Algeria, Hedysarum naudinianum and H. perrauderianum. Ann Microbiol. 64: 1065–1071. 
  39. Vincent, J. M. (1970). The manual for the practical study of root nodule bacteria. Blackwell Scientific Publication Ltd., Oxford, United Kingdom. 
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    Research Article

    volume 43 issue 6 (december 2020) : 872-877,   Doi: 10.18805/LR-527

    Contribution to the Study of the Relationship between Gammaproteobacteria and Rhizobia in Legume Species of the Genus Hedysarum

    T
    Torche Esma
    R
    Rouabhi Ahlem
    T
    Torche Boutheina
    S
    Slatnia Soumia
    G
    Gharzouli Razika
    B
    Benhizia Hayet
    B
    Benhizia Yacine
    B
    Benguedouar Ammar
    1Faculté des Sciences de la Nature et de la Vie et des Sciences de la Terre et de l’Univers, Université 8 Mai 1945 Guelma, Guelma, Algeria. 

    • Submitted19-09-2019|

    • Accepted16-01-2020|

    • First Online 15-05-2020|

    • doi 10.18805/LR-527

    Cite article:- Esma Torche, Ahlem Rouabhi, Boutheina Torche, Soumia Slatnia, Razika Gharzouli, Hayet Benhizia, Yacine Benhizia, Ammar Benguedouar (2020). Contribution to the Study of the Relationship between Gammaproteobacteria and Rhizobia in Legume Species of the Genus Hedysarum. Legume Research. 43(6): 872-877. doi: 10.18805/LR-527.

    ABSTRACT

    The nodular contents of the leguminous species of the genus Hedysarum (H. carnosum, H. spinosissimum subsp capitatum and H. pallidum) consist of cultivable bacteria belonging to the class Gammaproteobacteria, while the rhizobia of these leguminous species are not cultivable. Rhizobium sulla is the specific micro-symbiont of the H. coronarium leguminous species. The aim of this study is to see if the Gammaproteobacteria that inhabit the nodules of the three species of the genus Hedysarum (H. carnosum, H. spinosissimum subsp capitatum and H. pallidum) could have acquired the symbiotic criteria from rhizobia and cause nodulation in these host legume species by the transformation process. Transformation is carried out by extracting the plasmid DNA from the R. sulla strain and incorporate it into the bacterial strains of the Gammaproteobacteria class. Nodulation assay is performed to evaluate the ability of transformed strains to cause nodulation in legume species. The results showed that although there has been a transformation, there is a total failure of nodulation in the three legume species. This is explained by the specificity of molecular signals between bacteria and host plants as well as the genetic information carried by the plasmid is not sufficient to achieve a complete symbiotic relationship.

    REFERENCES

    1. Abdelguerfi-Berrekia, R., Abdelguerfi, A., Bounaga, N.. Guittonneau, G.G. (1988). Contribution à l’étude des espèces spontanées du genre Hedysarum L. en Algérie. Ann. Inst. Nat. Agro. El-Harrach. 12: 191-219. 
    2. Abdelguerfi-Berrekia, R., Abdelguerfi, A., Bounaga, N.. Guittonneau, G.G. (1991). Répartition des espèces spontanées du genre Hedysarum selon certains facteurs du milieu en Algérie. Fourrages. 126: 187-207. 
    3. Benguedouar, A. (2000). Etude de la symbiose : Rhizobium –    Hedysarum coronarium. Essai de la caractérisation de l’espèce Rhizobium hedysary. Thèse de doctorat de l’université de Constantine, Algérie. 
    4. Benhizia, Y. (2006). Caractérisation phénotypique et phylogénétique des bactéries associées aux nodules de la légumineuse du genre Hedysarum: H.carnosum Desf., Hspinossissimum subsp.capitatum Desf. Et H.pallidum Desf. Thèse de doctorat d’état en microbiologie appliquée., Université Mentouri Constantine. 
    5. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A. and Squartini, A. (2004). Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol. 27(4): 462-468. 
    6. Benselama, A., Tellah S, Ourem F, and Ounane S. (2018). Characterization of rhizobia from root nodule and rhizosphere of Vicia faba in Algeria. Legume Research: An International Journal. 41(4): 624-628 
    7. Beringer, J.E. (1974). R-Factor transfer in rhizobium legume. J. Gen. Microbiol. 84: 188-198.
    8. Birnboim, H.C. (1983). A rapid alkaline extraction method for the isolation of plasmid DNA. Methods Enzymol. 100: 243 -    255.
    9. Caetano-Anolles, G., Lagares, A., and Bauer, W. D. (1990). Rhizobium meliloti exopolysaccharide Mutants Elicit Feedback Regulation of Nodule Formation in Alfalfa1. Plant Physiol. 92 (2): 368-374. 
    10. Casella, S., Gault, R.R., Reynolds, K.C., Dyson, J.R., Brockwell, J. (1984). Nodulation studies on legumes exotic to Australia: Hedysarum coronarium. FEMS. Microbial. Lett. 22: 37-45. 
    11. Castellane, T. C. L., Campanharo, J. C., Colnago, L. A., Coutinho, I. D., Lopes, É. M., Lemos, M. V. F. and de Macedo Lemos, E. G. (2017). Characterization of new exopolysaccharide production by Rhizobium tropici during growth on hydrocarbon substrate. International Journal of Biological Macromolecules. 96: 361-369. 
    12. Chataigné, G. (2007). Détermination structurale des lipopolysaccharides de surface chez Sinorhizobium. Doctorat en Chimie-Biologie-    Santé. Université Toulouse III. 
    13. Chuang -Yien Lee, J. (2000). Expression Studies on the exo Y Promoter Region in Rhizobium meliloti. Bug Journal. 3. 
    14. Ding, H. and Hynes, M. F. (2009). Plasmid transfer systems in the rhizobia. Can J Microbiol. 55(8): 917-927. 
    15. Dudeja, S.S., Sheokand, S. and Kumari, S. (2012). Legume root nodule development and functioning under tropics and subtropics: perspectives and challenges. Legume Research: An International Journal. 35(2): 85-103. 
    16. Fähreus, A. (1957). The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. J. Gen. Microbiol. 16: 354-381. 
    17. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev. 68(2): 280-300. 
    18. Gharzouli, R. (2006). Influence d’agents mutagènes, les rayons Ultra-violet, sur la nodulation et les caractères phénotipiques de quelques espèces de Rhizobium sp. Mémoire de Magister en génétique moléculaire., Université Constantine. Algérie. 
    19. Gharzouli, R. (2013). Etude Structurale et Génétique des Exopolysaccharides produits par l’espèce Rhizobium sullae. Doctorat En Sciences, Constantine. 
    20. Ghosh, P.K. and Maiti, T.K. (2016). Structure of extracellular polysaccharides (EPS) produced by rhizobia and their functions in legume–bacteria symbiosis: A Review. Achievements in the Life Sciences. 10(2): 136-143. 
    21. Girija, D., Panchami, P.S., Praveena, E., Jose, T.S. and Sneha, N.S. (2018). Isolation and characterization of native cowpea rhizobia from Wayanad India. Legume Research: An International Journal. doi: 10.18805/LR-3951.
    22. Hirsch, A. M., Lum, M. R. and Downie, J. A. (2001). What Makes the Rhizobia-Legume Symbiosis So Special? Plant Physiology. 127(4):1484-1492. 
    23. Ibanez, F., Reinoso, H. and Fabra, A. (2010). Experimental evidences of pSym transfer in a native peanut-associated rhizobia. Microbiol Res. 165(6): 505-515. 
    24. Janczarek, M., and Skorupska, A. (2003). Exopolysaccharide synthesis in Rhizobium leguminosarum bv. trifolii is related to various metabolic pathways. Research in Microbiology. 154(6): 433-442. 
    25. Leigh, J. A., and Lee, C. C. (1988). Characterization of polysaccharides of Rhizobium meliloti exo mutants that form ineffective nodules. J Bacteriol. 170(8): 3327-3332. 
    26. Morgante, C., Castro, S, Fabra, A. (2005). Role of rhizobial exopolysaccharides in crack entry/intercellular infection of peanut. Soil Biology and Biochemistry. 37(8): 1436-1444. 
    27. Muresu, R., Polone, E., Sulas, L., Baldan, B., Tondello, A., Delogu, G., Cappuccinelli, P., Alberghini, S., Benhizia, Y., Benhizia, H., Benguedouar, A., Mori, B., Calamassi, R., Dazzo, F. B. and Squartini, A. (2008). Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol. 63(3): 383-400. 
    28. Navarini, L., Stredansky, M., Matulova, M. and Bertocchi, C. (1997). Production and characterization of an exopolysaccharide from Rhizobium hedysari HCNT 1. [journal article]. Biotechnology Letters. 19(12): 1231-1234. 
    29. Pelmont, J. (1995). Bactéries et environnement: Adaptation physiologique. (Vol. 2): Office des Publications Universitaires.
    30. Raposeiras, R., Patrícia, P.P.P., Raul, V.M., Lucy, S., Paiva, E., Scotti, M.R. and Sá, N.M.H. (2002). Variability of isolated colonies in bean nodulating Rhizobium strains before and after exposure to high temperature. Brazilian Journal of Microbiology. 33(2): 149-154.
    31. Senthil, K., M, Lakshmi, K. S., and Annapurna, K. (2017). Exopolysaccharide from Rhizobia: Production and Role in Symbiosis. Rhizobium Biology and Biotechnology. 50: 257-292 
    32. Singh, Z. and Singh, G. (2018). Role of Rhizobium in chickpea (Cicer arietinum) production-A review. Agricultural Reviews. 39(1): 31-39.
    33. Squartini, A., Struffi, P., Doring, H., Selenska-Pobell, S., Tola, E., Giacomini, A., Vendramin, E., Velazquez, E., Mateos, P.F., Martinez-Molina, E., Dazzo, F.B., Casella, S. and Nuti, M.P. (2002). Rhizobium sullae sp. nov. (formerly ‘Rhizobium hedysari’), the root-nodule microsymbiont of Hedysarum coronarium L. Int J Syst Evol Microbiol. 52(4): 1267-1276. 
    34. Strufi, P., Corich, V., Giacomini, A., Benguedouar, A., Squartini, A., and Casella, S. and Nuti, M.P. (1998). Metabolic properties, stress tolerance and macromolecular profiles of rhizobia nodulating Hedysarum coronarium. J Appl Microbiol. 84: 81- 89. 
    35. Tejerizo, G. T., Del Papa, M. F., Giusti, M. I. A., Draghi, W., Lozano, M., Lagares, A. and Pistorio, M. (2010). Characterization of extrachromosomol replicons present in the extended host range Rhizobium. sp. LPU83. Plasmid. 64: 177-185. 
    36. Tondello, A., Villani, M., Alessandrini, A., Baldan, B. and Squartini, A. (2011). Identification of the root nodule symbiont of the rare legume species Hedysarum confertum Desf. (Hedysarum humile L.) in its Italian relictual site. Plant Biosytems. 145: 901-905. 
    37. Torche, (2006). Isolement et caractérisation des bactéries nodulant les légumineuses du genre Hedysarum. Magister Biochimie microbiologie appliquée, université Mentouri Constantine. 
    38. Torche, A., Benhizia, H., Rosselli, R., Romoli, O., Zanardo, M., Baldan, E., Alberghini, S., Tondello, A., Baldan, B., Benguedouar, A., Squartini, A., and Benhizia, Y. (2014). Characterization of bacteria associated with nodules of two endemic legumes of Algeria, Hedysarum naudinianum and H. perrauderianum. Ann Microbiol. 64: 1065–1071. 
    39. Vincent, J. M. (1970). The manual for the practical study of root nodule bacteria. Blackwell Scientific Publication Ltd., Oxford, United Kingdom. 
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