| Peer-Reviewed

Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.)

Received: 25 October 2014    Accepted: 10 November 2014    Published: 20 November 2014
Views:       Downloads:
Abstract

We aimed to characterize 83 endophytic bacteria isolated from roots (73 isolates coded IRC) and epicotyls (11 isolates coded IEC) of young Carob (Ceratonia siliqua L.) seedlings. These seedlings were obtained from seeds collected in several regions in Morocco. 30 IRC and 4 IEC were selected on the basis of PCR-Pep for the further analyses. All the strains exhibited a wide tolerance to NaCl and 30 % tolerated well concentration up to 11 % NaCl. Strains showed also a wide tolerance to the variable pH. 60 % of strains grew well at pH4. Most of the strains were resistant to different antibiotics but were sensitive to kanamycin and tetracycline. The strains showed a resistance to heavy metals except mercury chloride that was toxic at a low concentration 50 µg.ml-1. According to their phenotypical features, the associative bacteria were very similar to eight symbiotic bacteria previously identified by Missbah in 1996 and used in this work.

Published in American Journal of Life Sciences (Volume 2, Issue 5)
DOI 10.11648/j.ajls.20140205.22
Page(s) 325-332
Creative Commons

This is an Open Access article, distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium or format, provided the original work is properly cited.

Copyright

Copyright © The Author(s), 2024. Published by Science Publishing Group

Keywords

Isolation, Associative Endophytic Bacteria, Phenotypic Characterization, Managed Ecosystem

References
[1] Hill, G. T., N. A. Mitkowski, L. Aldrich-Wolfe, L. R. Emele, D. D. Jurkonie, A. Ficke, S. Maldonado-Ramirez, S. T. Lynch and E. B. Nelson. 2000. Methods for assessing the composition and diversity of soil microbial communities. Appl. Soil Microbiol. 15: 25- 36.
[2] Haiiman, J., A. Quadt-Hallman, W. F. Mahafee, and J. W. Kleopper. 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43: 895- 914.
[3] Sturz, A. V., and Nowak. 2000. Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Ecol Appl. Soil. 15: 183- 190.
[4] Jacobs, M. J., W. M. Bugdee, and D. A. Gabrielson. 1985. Enumeration, location, and characterization of endophytic bacteria within sugar-beet roots. Can. J. Bot. 63: 1262- 1265.
[5] De Bary A. 1866. Morphologie und physiologie der Pilze, Flechten und Myxomyceten. Hofmeister’s Handbook of Physiological Botany, Vol. 2, Leipzig
[6] Stone, J. K. 1986. Foliar endophytes of Pseudotsugamenziesli (Mirb) Franco. Cytology and physiology of the host-endophyte relationship. DSc Thesis, Univ. of Oregon, Eugene, Canada.
[7] Baldani, J. I., and V. L. D. Baldani. 2005. History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An. Acad. Bras. Cienc. 77: 549- 579.
[8] Petrini, O. 1991. Fungal endophytes of tree leaves. In:Andrews J. and Hirano (Eds), Microbial ecology of leaves. New York: Springer Verlag, p. 179- 197.
[9] Kloepper, J. W., R. M. Zablotowicz, E. M. Tipping, R. Lifshitz. 1991. Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister, D. L., Cregow, P. B. (Eds), The rhizosphere and plant growth. Kluwer Academic Publishers, Dordrecht, pp. 315-326.
[10] Lazarovits, G., and J. Nowak. 1997. Rhizobacteria for improvement of plant growth and establishment. HortScience 32: 188-192.
[11] Alami, Y., W. Achouak, C. Marol, and T. Heulin. 2000. Rhizosphere soil aggregation and plant growth promotion of Sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from Sunflower roots. Appl. Environ. Microbiol. 66: 3393-3398.
[12] Chen, C., E. M. Bauske, G. Musson, R. Rodriguez-Cabaña, J. Kloepper. 1995. Biological control of Fusarium on cotton by use of endophytic bacteria. Biolo. Control. 5: 83-91.
[13] Lodewyckx, C., J. Vangrosveld, F. Portteous, E. R. B. Moore, S. Taghavi, M. Mezgeay, and D. van der Lelie. 2002. Endophytic bacteria and their potential applications. Crit. Rev. Plant Sci. 21: 583-606.
[14] Scroth, M. N., and J. G. Hancock. 1981. Selected topics in biological control. An. Rev. Microbiol. 35: 453-476.
[15] Weller, D. M. 1988. Biological control of soil-borne plant pathogens in the rhizosphere with bacteria. An. Rev. Phytopathol. 26: 379-407.
[16] Webster, G., V. Jain, M. R. Davey, C. Gough, J. Vasse, J. Dénarié, and E. C. Cocking. 1998. The flavonoid naringenin stimulates the intercellular colonization of wheat roots by Azorhizaobium caulinodans. Plant Cell and Environ. 21: 373-383.
[17] Gough, C., C. Galera, J. Vasse, G. Webster, E. C. Cocking and J. Dénarié. 1997a. Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol. Plant-Interac. 10: 560-570.
[18] Ndoye, I., F. De Billy, J. Vasse, B. Dreyfus, and G. Truchet. 1994. Root nodulation of Sesbania rostrata. J. of Bacteriol. 176: 1060-1068.
[19] Patriquin, D. G., J. Döbereiner, and D. K. Jain. 1983. Sites and processes of association between diazotrophs and grasses. Can J. Microbiol. 29: 900-915.
[20] Boddey, R. M., O. C. De Oliveira, S. Urquiagea, V. M. Reis, F. L. De Olivares, V. L. D. Baldani, and J. Doebereiner. 1995. Biological nitrogen fixation associated with sugarcane and rice: contribution and prospects for improvement. Plant Soil 174: 195-209.
[21] Urquiaga, S., K. H. S. Cruz, and R. M. Boddey. 1992. Contribution of nitrogen fixation to sugar cane: nitrogen-15 and nitrogen-balance estimates. Soil Sci. Soc. Am. J. 56: 105-114.
[22] Bryan J.A., Berlyn G. P. And Gordon J.C. 1996. Towards a new concept of the evolution of symbiotic nitrogen fixation in the Leguminosae. Plant Soil, 186: 151-159.
[23] Bormann, F. H., G. E. Likens, and J. M. Melillo. 1980. Nitrogen budget for an aggrading northern hardwood forest ecosystem. Sciences. 196: 981-983.
[24] Reinhold-Hurek, B., and T. Hurek. 1998. Life in grasses: diazorophic endophytes. Trends Microbiol. 6: 139-144.
[25] Compant, S., B. Reiter, A. Sessistsch, J. Nowak, C. Clément, and E. A. Barka. 2005. Endophytic colonization of Vitis vinifera L. by palnt growth-promoting bacterium Burkholderia sp. strain PsJN. Appl. Environ. Microbilo. 71: 1685-1693.
[26] Gillis M., T. Tran van, R. Bardin, M. Goor, P. Herbar, A. Willems, P. Segers, K. Kersters, T. Heulin, and M. P. Fernandez. 1995. Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and preposition of Burkholderia vietnamiensis sp. nov., for N2-fixing isolates from rice in Vietnam. Int. J. Syst. Evol. Microbiol. 45: 274-289.
[27] Reinhold-Hurek, B., and T. Hurek, M. Gillis, B. Hoste, M. Vancanneyt, K. Kersters, and J. De Ley. 1993b. Azoarcus gen. nov., nitrogen-fixing proteobacteria associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth) and description of two species Azoarcus indigens sp. nov. and Azoarcus communis sp. nov. Int. J. Syst. Bacteriol. 43: 574-584.
[28] Chabot, R., H. Antoun, J. W. Kloepper, and C. J. Beauchamp. 1996. Root colonization of Maize and Lettuce by Bioluminescent Rhizobium leguminosarum biovar phaseoli. Appl. Environ. Microbiol. 62: 2767-2772.
[29] Chaintreuil, C., E. Giraud, Y. Prin, J. Lorquin, A. Bâ, M. Gillis, P. De Lajudie, and B. Dreyfus. 2000. Photosynthetic Bradyrhizobia are natural endophytes of the african wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66: 5437-5447.
[30] Chi, F., S. H. Shen, H. P. Cheng, Y. X. Jing, Y. G. Yanni, and F. B. Dazzo. 2005. Ascending migration of endophytic Rhizobia, from roots to leaves, inside rice plants and assessment to benefits to rice growth physiology. Appl. Environ. Microbiol. 71: 7271-7278.
[31] Matiru, V. N., and F. D. Dakora. 2004. Potential use of rhizobial as promoters of plant growth for inceased yield in landraces of African cereal crops. Afr. J. Biotechnol. 3: 1-7.
[32] O’Callaghan, K. J., M. R. Davey, and E. C. Cocking. 1997. Xylem colonization of the legume Sesbania rostrata by Azorhizobium caulinodans. Proc. R. Soc. Lond. B. 264: 1821-1826.
[33] Webster, G., C. Gough, J. Vasse, C. A. Batchelor, K. J. O’Callaghan, S. L. Kothari, M. R. Davey, J. Dénarié, and E. C. Cocking. 1997. Interaction of rhizobia with rice and wheat. Plant Soil. 194: 115-22.
[34] Yanni Y. G., R. Y. Rizk, V. Corich, A. Squartini, K. Ninke, S. Philip-Hollingsworth, G. Orgambide, F. De Buijn, R. Stoltzfus, D. Buckley, T. Schmidt, P. F. Mateos, J. K. Ladha, and F. B. Dazzo. 1997. Natural endophytic association between Rhizobium leguminosarum bv. Trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil. 194: 99-114.
[35] Koulibaly, A., D. Goetze, S. Porembski and L. Aké-Assi. 2010. Vegetation characteristics and changes under cash crop cultivation in forest-savanna mosaics in Côte d’Ivoire. In: X van der Burgt, J. van der Maesen & J.M. Onana (eds), Systematics and Conservation of African Plants. Royal Botanic Gardens, Kew, pp. 805-814.
[36] Kebe I.B., Mpika J., N’Guessan K.F., Hebbar P.K., Samuels G.S. and Ake S. 2009. Isolement et identification de microorganisms indigenes de cacaoyères en Côte d’Ivoire et mise en evidence de leurs effets antanistes vis-vis de Phytosphtora palmivora, agent de la pourriture brune des cabosses. Sciences & Nature, 6 (1) : 71-82.
[37] Christodoukakis, N. S. 1992. Structural diversity and adaptation in some Mediterranean evergreen sclerophyllous species. Environ. Experment. Bot. 32: 295- 305.
[38] Batlle, I., and J. Tous. 1997. Carob tree (Ceratonia siliqua L.), promoting the conservation and use of under utilized and neglected crops. 17, Institute of Plant Genetic and Crop Plant Research, Galersleben/International Plant Genetics Resources Institute, Rome.
[39] Hamed, T. E., A. Ezzat, and S. Y. Al-Okbi. 2003. Therapeutic diets for diarrhea: Biological evaluation in Rats. Pak. J. Biol. Sci. 6: 1501-1508.
[40] Loed, H., Y. Vandenplas, P. Wursch, and P. Guesry. 1989. Tannin-rich Carob pad for the treatment of acute-onset diarrhea. J. Pediatr Gastroentrol Nutr. 8: 480.
[41] Yatzidis, H. 1980. Traitement de l’insuffisance rénale chronique par la gomme de caroube. Nouvelle Presse Méditerranéenne. 9: 3065.
[42] Konate I., E.B. Berraho and A. Filali-Maltouf. 2009. Inter-Simple Sequence Repeat Markers Variation among Natural Accessions of Moroccan Carob Tree (Ceratonia siliqua L.), International Journal of Agriculture and Biology, 11: 168-172.
[43] Vincent, J. M. 1970. A manual for the practical study of root nodule bacteria. IBP (Int. Biol. Programme) Handbook 15 Blackwell, Scientific Publcations. Ltd. Oxford.
[44] Missbah M. E. I., A. Aujjar, A. Belabed, Y. Dessaux, and A. Filali-Maltouf. 1996. Characterization of rhizobia isolated from Carob (Ceratonia siliqua). J. Appl. Bacteriol. 80: 165-173.
[45] Shenoy, V. V., G. M. Kalagudi, and B. V. Gurudatta. 2001. Towards nitrogen autotrophic rice. Curr. Sci. 81: 451-457.
[46] Kleopper, J. W., and C. J. Beauchamp. 1992. A review of issues related to measuring colonization of plant roots by bacteria. Can. J. Microbiol. 38: 1219-1232.
[47] Gillis M., K. Kerskers, B. Hoste, D. Janssens, R. M. Krosppenstedt, M. P. Stephan, K. R. S. Teixeira, J. Döbereiner, and J. De Ley. 1989. Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int. J. Syst. Bacteriol. 39: 361- 364.
[48] James, E. K., F. L. Olivares, J. I. Baldani, and J. Dödereiner. 1997. Herbaspirillum an endophytic diazotroph colonizing vascular tissue in leaves of Sorghonum bicolor L. Moench. J. Exp. Bot. 48: 785- 797.
[49] Sabry, S. R. S., S. A. Saleh, C. A. Batchelor, J. Jones, J. Jotham, G. Webster, S. L. Kothari, M. R. Davey, and E. C. Cocking. 1997. Endophytic establishment of Azorhizobium caulinodans in wheat. Proceding of the Royal Society, London: Biological Sciences. 264: 341- 346.
[50] Christiansen-Weniger, C. 1996. Endophytic establishment of Azorhizobium caulinodans through auxin-induced root tumours of rice (Oryza sativa L.). Biol. Fert. Soil. 21: 293- 302.
[51] Van Thi P. N and Cao Ngoc D. 2014. Isolation, characterization and phylogenetic analysis of endophytic bacteria in rice plant cultivated on soil of Phu Yen provence, Vietnam. American Journal of Life Sciences. 2 (3): 117-127.
[52] Seghers, D., L. Wittebolle, E. M. Top, W. Verstraete, and S. D. Siciliano. 2004. Impact of agricultural practise on the Zea mays L. endophytic community. Appl. Environ. Microbiol. 70: 1475-1482.
[53] Misaghi, I. J., and C. R. Donndelinger. 1990. Endophytic bacteria in symptom-free cotton plant. Phytopathology. 9: 808-811.
[54] Reva, O. N., V.V. Smirnov, B. Pettersson, and F. G. Priest. 2002. Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (Gossypium sp.). Int. J. Syst. Microbiol. 52: 101-107.
[55] Bell, C. R., G. A. Dickie, W. L. G. Harvey, and J. W. Y. F. Chan. 1995. Endophytic bacteria in grapevine. Can. J. Microbiol. 41: 46-53.
[56] Shishido, M., C. Breuil, and C. P. Chanway. 1999. Endophytic colonization of spruce by plant growth-promoting rhizobia. FEMS Microbiol. Ecol. 29: 191-196.
[57] Jimenez-Salgado, T., L. E. Fuentes-Ramirez, A. Tapia-Hernandez, A. M. Mascarua-Esperanza, E. Martinez-Romero, and J. Caballero-Mellado. 1997. Coffea arabica L. a new host for Acetobacter diazotrophicus and isolation of other nitrogen-fixing Acetobacteria. Appl. Environ. Microbiol. 63: 3676-3683.
[58] Cruz L. M., E. M. Souza, O. B. Weber, J. I. Baldani, J. Döbereiner, and F. O. Pedrosa. 2001. 16S rDNA characterization of nitrogen-fixing bacteria isolated from Banana (Musa sp.) and Pineapple (Ananas comosus (L.) Merril). Appl. Environ. Microbiol. 67: 2376-2379.
[59] Tilak, K. V. B. R., N. Ranganayaki, K. K. Pal, R. De, A. K. Saxena, C. S. Nautiyal, S. Mittal, A. K. Tripathi, and B. N. Johri. 2005. Diversity of plant growth and soil health supporting bacteria. Curr. Sci. 89: 136-150.
[60] Kulkarni, S. and C. S. Nautiyal. 2000. Effect of salt and pH stress on temperature-tolerant Rhizobium sp. NBRI330 nodulating Prosopis juliflora. Curr. Microbiol. 40: 221-226.
[61] Boncompagni, E., M. Osterås, M. Poggi, and D. Le Rudulier. 1999. Occurrence of choline and glycine betaine uptake metabolism in rhizobia. Appl. Environ. Microbil. 65: 2072-2077.
[62] Stephan, M. P., M. Oliveira, K. R. S. Texiera, G. Martinez-Drets, and J. Döbereiner. 1991. Physiology and dinitrogen fixation of Acetobacter diazotrophicus. FEMS Microbiol. Lett. 77: 67-72.
[63] Day, J. M., and J. Döbereiner. 1976. Physiological aspect of N2 fixation by a Spirillum from Digitaria root. Soil Biol. Biochem. 8: 45-50.
[64] Cooper, J. E. 1982. Acid production, acid tolerance and growth rate of Lotus rhizobia in laboratory media. Soil Biol. Biochem. 14: 127-131.
[65] Graham, P. H., and C. A. Parker. 1994. Diagnostic features of the root-nodule bacteria of legumes. Plant Soil. 20: 383-396.
[66] Maâtallah, J., E. B. Berraho, J. Sanjuan, and C. Lluch. 2002. Phenotypic characterization of rhizobia isolated from chickpea (Cicer arietinum) growing in Moroccan soils. Agronomie. 22: 321- 29.
[67] Schwinghamer, E. A. 1967. Effectiveness of rhizobium as modified by mutation for resistance to antibiotics. Antonie van Leeuwenhoek. J. Microbiol. Serol. 33: 121-136.
[68] Cole, M. A., and G. H. Elkan. 1979. Multiple antibiotic resistance in Rhizobium japonicum. Appl. Environ. Microbiol. 37: 867-870.
[69] Mohammed S.H., A. Smouni, M. Neyra, D. Kharchef And A. Filali-Maltouf. 2000. Phenotypic characterization of root nodulating bacteria isolated from Acacia spp. Grown in Lybia. Plant Soil. 224: 171-183.
Cite This Article
  • APA Style

    Ibrahim Konate, Annick Koulibaly, Mathurin Koffi, Amina Sorouri, El Bekkay Berraho, et al. (2014). Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.). American Journal of Life Sciences, 2(5), 325-332. https://doi.org/10.11648/j.ajls.20140205.22

    Copy | Download

    ACS Style

    Ibrahim Konate; Annick Koulibaly; Mathurin Koffi; Amina Sorouri; El Bekkay Berraho, et al. Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.). Am. J. Life Sci. 2014, 2(5), 325-332. doi: 10.11648/j.ajls.20140205.22

    Copy | Download

    AMA Style

    Ibrahim Konate, Annick Koulibaly, Mathurin Koffi, Amina Sorouri, El Bekkay Berraho, et al. Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.). Am J Life Sci. 2014;2(5):325-332. doi: 10.11648/j.ajls.20140205.22

    Copy | Download

  • @article{10.11648/j.ajls.20140205.22,
      author = {Ibrahim Konate and Annick Koulibaly and Mathurin Koffi and Amina Sorouri and El Bekkay Berraho and Abdelkarim Filali-Maltouf},
      title = {Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.)},
      journal = {American Journal of Life Sciences},
      volume = {2},
      number = {5},
      pages = {325-332},
      doi = {10.11648/j.ajls.20140205.22},
      url = {https://doi.org/10.11648/j.ajls.20140205.22},
      eprint = {https://article.sciencepublishinggroup.com/pdf/10.11648.j.ajls.20140205.22},
      abstract = {We aimed to characterize 83 endophytic bacteria isolated from roots (73 isolates coded IRC) and epicotyls (11 isolates coded IEC) of young Carob (Ceratonia siliqua L.) seedlings. These seedlings were obtained from seeds collected in several regions in Morocco. 30 IRC and 4 IEC were selected on the basis of PCR-Pep for the further analyses. All the strains exhibited a wide tolerance to NaCl and 30 % tolerated well concentration up to 11 % NaCl. Strains showed also a wide tolerance to the variable pH. 60 % of strains grew well at pH4. Most of the strains were resistant to different antibiotics but were sensitive to kanamycin and tetracycline. The strains showed a resistance to heavy metals except mercury chloride that was toxic at a low concentration 50 µg.ml-1. According to their phenotypical features, the associative bacteria were very similar to eight symbiotic bacteria previously identified by Missbah in 1996 and used in this work.},
     year = {2014}
    }
    

    Copy | Download

  • TY  - JOUR
    T1  - Phenotypic Variations of Endophytic Bacteria Associated with Carob Tree (Ceratonia Siliqua L.)
    AU  - Ibrahim Konate
    AU  - Annick Koulibaly
    AU  - Mathurin Koffi
    AU  - Amina Sorouri
    AU  - El Bekkay Berraho
    AU  - Abdelkarim Filali-Maltouf
    Y1  - 2014/11/20
    PY  - 2014
    N1  - https://doi.org/10.11648/j.ajls.20140205.22
    DO  - 10.11648/j.ajls.20140205.22
    T2  - American Journal of Life Sciences
    JF  - American Journal of Life Sciences
    JO  - American Journal of Life Sciences
    SP  - 325
    EP  - 332
    PB  - Science Publishing Group
    SN  - 2328-5737
    UR  - https://doi.org/10.11648/j.ajls.20140205.22
    AB  - We aimed to characterize 83 endophytic bacteria isolated from roots (73 isolates coded IRC) and epicotyls (11 isolates coded IEC) of young Carob (Ceratonia siliqua L.) seedlings. These seedlings were obtained from seeds collected in several regions in Morocco. 30 IRC and 4 IEC were selected on the basis of PCR-Pep for the further analyses. All the strains exhibited a wide tolerance to NaCl and 30 % tolerated well concentration up to 11 % NaCl. Strains showed also a wide tolerance to the variable pH. 60 % of strains grew well at pH4. Most of the strains were resistant to different antibiotics but were sensitive to kanamycin and tetracycline. The strains showed a resistance to heavy metals except mercury chloride that was toxic at a low concentration 50 µg.ml-1. According to their phenotypical features, the associative bacteria were very similar to eight symbiotic bacteria previously identified by Missbah in 1996 and used in this work.
    VL  - 2
    IS  - 5
    ER  - 

    Copy | Download

Author Information
  • Unité de formation et de Recherche en Agroforesterie et en Environnement, Université Jean Lorougnon Guédé, BP 150 Daloa, C?te d’Ivoire

  • Unité de formation et de Recherche en Agroforesterie et en Environnement, Université Jean Lorougnon Guédé, BP 150 Daloa, C?te d’Ivoire

  • Unité de formation et de Recherche en Agroforesterie et en Environnement, Université Jean Lorougnon Guédé, BP 150 Daloa, C?te d’Ivoire

  • Faculty of Sciences, Laboratory of Microbiology and Molecular Biology, University Mohammed V-Agdal, Rabat, Morocco

  • Faculty of Sciences, Laboratory of Microbiology and Molecular Biology, University Mohammed V-Agdal, Rabat, Morocco

  • Faculty of Sciences, Laboratory of Microbiology and Molecular Biology, University Mohammed V-Agdal, Rabat, Morocco

  • Sections