Root nodule bacteria from Clitoria ternatea L. are putative invasive nonrhizobial endophytes

Canadian Journal of Microbiology

Volumn 61, Issue 2, 2015, Pages 131-142

  Aeron, Abhinav ^a,b   Chauhan, Puneet Singh ^c   Dubey, Ramesh Chand ^a   Maheshwari, Dinesh Kumar ^a   Bajpai, Vivek K ^d  

^a GURUKUL KANGRI UNIVERSITY   (India)

^b SHARDA UNIVERSITY   (India)

^c CSIR NATIONAL BOTANICAL RESEARCH INSTITUTE   (India)

^d Yeungnam University   (South Korea)

Author keywords

ARDRA; Clitoria ternatea L.; Endophytes; ERIC; Rhizobia

Indexed keywords

RNA 16S;

BACTERIUM; BIOASSAY; COLONIZATION; ENDOPHYTE; LEGUME; NITROGEN FIXATION; NODULATION; PHENOTYPE; RHIZOSPHERE; SYMBIOSIS;

AMPLIFIED RIBOSOMAL DNA RESTRICTION ANALYSIS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL PLANT DISEASE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; BETAPROTEOBACTERIA; BIOCHEMICAL EQUIPMENT; CLITORIA TERNATEA; CONTROLLED STUDY; ENDOPHYTE; ENTEROBACTERIACEAE; GAMMAPROTEOBACTERIA; NITROGEN FIXATION; NODULATION; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHIZOBIACEAE; RNA SEQUENCE; SPHINGOBACTERIA; BACTERIUM; CLITORIA; CLUSTER ANALYSIS; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHENOTYPE; RHIZOBIUM; SPECIES DIFFERENCE; SYMBIOSIS;

BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; CLITORIA TERNATEA; GAMMAPROTEOBACTERIA; SPHINGOBACTERIA;

BACTERIA; BETAPROTEOBACTERIA; CLITORIA; CLUSTER ANALYSIS; ENDOPHYTES; GAMMAPROTEOBACTERIA; NITROGEN FIXATION; PHENOTYPE; PHYLOGENY; POLYMERASE CHAIN REACTION; RHIZOBIUM; RNA, RIBOSOMAL, 16S; ROOT NODULES, PLANT; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 84922281427     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2014-0483     Document Type: Article

References (46)

1. Araujo, W. L., Marcon, J., Maccheroni, W., Jr., Van Elsas, J. D., Van Vuurde, J. W. L., and Azevedo, J. L. 2002. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl. Environ. Microbiol. 68: 4906-4914. doi: 10. 1128/AEM. 68. 10. 4906-4914. 2002. PMID: 12324338.
2. Asis, C. A., and Adachi, K. 2003. Isolation of endophytic diazotroph Pantoea agglomerans and non-diazotroph Enterobacter asburiae from sweet potato stem in Japan. Lett. Appl. Microbiol. 38: 19-23. PMID: 14687210.
3. Barea, J. M. B., Marıa, J., Rosario, A. P., and Concepcion, A. 2005. Microbial cooperation in the rhizosphere. J. Exp. Bot. 56(417): 1761-1778. doi: 10. 1093/jxb/eri197. PMID: 15911555.
4. Bazzicalupo, M., and Fani, R. 1995. The use of RAPD for generating specific DNA probes for microorganisms. In Methods in molecular biology, species diagnostic protocols: PCR and other nucleic acid methods. Edited by J. P. Clap. Humana Press Inc., Totowa N. J., USA. pp. 155-175.
5. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A., and Squartini, A. 2004a. The root nodules of Hedysarum carnosum, H. spinosissimum subsp. capitatum, and Hedysarum pallidum (Leguminosae) host Gammaproteobacteria. In Proceedings of the 6th European Nitrogen Fixation Conference, Toulouse, France, 24-27 July 2004.
6. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A., and Squartini, A. 2004b. Gammaproteobacteria can nodulate legumes of the genus Hedysarum. Syst. Appl. Microbiol. 27: 462-468. doi: 10. 1078/0723202041438527. PMID: 15368852.
7. Dalton, D. A., Kramer, S., Azios, N., Fusaro, S., Cahill, E., and Kennedy, C. 2004. Endophytic nitrogen fixation in dune grasses (Ammophila arenaria and Elymus mollis) from Oregon. FEMS Microbiol. Ecol. 49: 469-479. doi: 10. 1016/j. femsec. 2004. 04. 010. PMID: 19712295.
8. Deng, Z. S., Zhao, L. F., Kong, Z. Y., Yang, W. Q., Lindstrom, K., Wang, E. T., and Wei, G. H. 2011. Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol. Ecol. 76: 463-475. doi: 10. 1111/j. 1574-6941. 2011. 01063. x. PMID: 21303396.
9. Dobereiner, J., Baldani, V. L. D., and Reis, V. M. 1995. Endophytic occurrence of diazotrophic bacteria in non-leguminous crops. In Azospirillum VI and related microorganisms. Edited by I. Fendrik, M. del Gallo, J. Vanderleyden, and M. de Zamarocy. Springer Verlag, Berlin, Germany. pp. 3-14. doi: 10. 1007/978-3-642-79906-8_1.
10. Forchetti, G., Masciarelli, O., Alemano, S., Alvarez, D., and Abdala, G. 2007. Endophytic bacteria in sunflower (Helianthus annuus L.): isolation, characterization and production of jasmonates and abscisic acid in culture medium. Appl. Microbiol. Biotechnol. 76: 1145-1152. doi: 10. 1007/s00253-007-1077-7. PMID: 17657487.
11. Gu, C. T., Wang, E. T., Sui, X. H., Chen, W. F., and Chen, X. C. 2007. Diversity and geographical distribution of rhizobia associated with Lespedeza spp. in temperate and subtropical regions of China. Arch. Microbiol. 188: 355-365. doi: 10. 1007/s00203-007-0256-3. PMID: 17530227.
12. Haynes, W. C., and Burkholder, W. H. 1957. Genus I. Pseudomonas Migula 1894. In Bergey's manual of determinative bacteriology. 7th ed. Edited by R. S. Breed, R. G. E. Murray, and N. R. Smith. Williams and Wilkins, Baltimore, Md., USA. pp. 89-152.
13. Hinton, D. M., and Bacon, C. W. 1995. Enterobacter cloacae is an endophytic symbiont of corn. Mycopathologia, 129: 117-125. doi: 10. 1007/BF01103471. PMID: 7659140.
14. Ibanez, F., Angelini, J., Taurian, T., Tonelli, M. L., and Fabra, A. 2009. Endophytic occupation of peanut root nodules by opportunistic Gammaproteobacteria. Syst. Appl. Microbiol. 32: 49-55. doi: 10. 1016/j. syapm. 2008. 10. 001. PMID: 19054642.
15. Jarabo-Lorenzo, A., Perez-Galdona, R., Donate-Correa, J., Rivas, R., Velazquez, E., Hernandez, M., et al. 2003. Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst. Appl. Microbiol. 26(4): 611-623. doi: 10. 1078/072320203770865927. PMID: 14666990.
16. Jha, P., and Kumar, A. 2009. Characterization of novel plant growth promoting endophytic bacterium Achromobacter xylosoxidans from wheat plant. Microb. Ecol. 58: 179-188. doi: 10. 1007/s00248-009-9485-0. PMID: 19224271.
17. Kuklinsky-Sobral, J., Araujo, W. L., Mendes, R., Geraldi, I. O., Pizzirani Kleiner, A. A., and Azevedo, J. L. 2004. Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ. Microbiol. 6: 1244-1251. doi: 10. 1111/j. 1462-2920. 2004. 00658. x. PMID: 15560822.
18. Laguerre, G., Allard, M. R., Revoy, F., and Amarger, N. 1994. Rapid identification of rhizobia by restriction fragment length polymorphism analysis of PCR amplifies 16S rRNA genes. Appl. Environ. Microbiol. 60: 56-63. PMID: 16349165.
19. Li, J. H., Wang, E. T., Chen, W. F., and Chen, W. X. 2008. Genetic diversity and potential for promotion of plant growth detected in nodule endophytic bacteria of soybean grown in Heliongjiang province of China. Soil Biol. Biochem. 40: 238-246. doi: 10. 1016/j. soilbio. 2007. 08. 014.
20. Ludwig, W., Amann, R., Martinez-Romero, E., Schonhuber, W., Bauer, S., Neef, A., and Schleifer, K. H. 1998. rRNA based identification and detection systems for rhizobia and other bacteria. Plant Soil, 204: 1-19. doi: 10. 1023/A: 1004350708767.
21. Mano, H., and Morisaki, H. 2008. Endophytic bacteria in the rice plant. Microbes Environ. 23: 109-117. doi: 10. 1264/jsme2. 23. 109. PMID: 21558696.
22. McInroy, J. A., and Kloepper, J. W. 1995. Survey of indigenous bacterial endophytes from cotton and sweet corn. Plant Soil, 173: 337-342. doi: 10. 1007/BF00011472.
23. Moretti, M., Gilardi, G., Gullino, M. L., and Garibaldi, A. 2008. Biological control potential of Achromobacter xylosoxydans for suppressing Fusarium wilt of tomato. Int. J. Bot. 4(4): 369-375. doi: 10. 3923/ijb. 2008. 369. 375.
24. Moulin, L., Munive, A., Dreyfus, B., and Boivin-Masson, C. 2001. Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature, 411: 948-950. doi: 10. 1038/35082070. PMID: 11418858.
25. Muresu, R., Polone, E., Sulas, L., Baldan, B., Tondello, A., Delogu, G., et al. 2008. Coexistence of predominantly non-culturable rhizobia with diverse endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol. Ecol. 63: 383-400. doi: 10. 1111/j. 1574-6941. 2007. 00424. x. PMID: 18194345.
26. Old, K., and Nicholson, T. 1978. The root cortex as part of a microbial continuum. In Microbial ecology. Edited by M. Loutit and J. Miles. Springer-Verlag, New York, USA. pp. 291-294.
27. Palaniappan, P., Chauhan, P. S., Saravanan, V. S., Anandham, R., and Sa, T. M. 2010. Isolation and characterization of plant growth promoting endophytic bacterial isolates from root nodule of Lespedeza sp. Biol. Fertil. Soils, 46: 807-816. doi: 10. 1007/s00374-010-0485-5.
28. Palleroni, N. J., and Bradbury, J. F. 1993. Stenotrophomonas, a new bacterial genus for Xanthomonas maltophilia (Hugh 1980). Int. J. Syst. Bacteriol. 43: 606-609. doi: 10. 1099/00207713-43-3-606. PMID: 8347518.
29. Pandey, P., Sahgel, M., Maheshwari, D. K., and Johri, B. N. 2004. Genetic diversity of rhizobia isolated from medicinal legumes growing in the sub-Himalayan region of Uttaranchal. Curr. Sci. 86: 202-207.
30. Parniske, M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6(10): 763-775. doi: 10. 1038/nrmicro1987. PMID: 18794914.
31. Perotti, R. 1926. On the limits of biological enquiry in soil science. Proc. Int. Soc. Soil Sci. 2: 146-161.
32. Phillips, D. A., Martynez-Romero, E., Yang, G. P., and Joseph, C. M. 2000. Release of nitrogen: a key trait in selecting bacterial endophytes for agronomically useful nitrogen fixation. In The quest for nitrogen fixation in rice. Edited by J. K. Ladha and P. M. Reddy. International Rice Research Institute, Manila, The Philippines. pp. 205-217.
33. Rajendran, G., Sing, F., Desai, A. J., and Archana, G. 2008. Enhanced growth and nodulation of pigeon pea by co-inoculation of Bacillus strains with Rhizobium spp. Bioresour. Technol. 99: 4544-4550. doi: 10. 1016/j. biortech. 2007. 06. 057. PMID: 17826983.
34. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular cloning: a laboratory manual. Vol. I. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y., USA.
35. Selvakumar, G., Kundu, S., Gupta, A. D., Shouche, Y. S., and Gupta, H. S. 2007. Isolation and characterization of non-rhizobial plant growth promoting bacteria from nodules of Kudzu (Pueraria thunbergiana) and their effect on wheat seedling growth. Curr. Microbiol. 56(2): 134-139. doi: 10. 1007/s00284-007-9062-z. PMID: 18074178.
36. Senthilkumar, M., Swarnalakshmi, K., Govindasamy, V., Lee, Y. K., and Annapurna, K. 2009. Biocontrol potential of soybean bacterial endophytes against charcoal rot fungus, Rhizoctonia bataticola. Curr. Microbiol. 58: 288-293. doi: 10. 1007/s00284-008-9329-z. PMID: 19067044.
37. Stephan, R., Trappen, S. V., Cleenwerck, I., Vancanneyt, M., Vos, P. D., and Lehne, A. 2007. Enterobacter turicensis sp. nov. and Enterobacter helveticus sp. nov., isolated from fruit powder. Int. J. Syst. Evol. Microbiol. 57: 820-826. doi: 10. 1099/ijs. 0. 64650-0. PMID: 17392213.
38. Sturz, A. V., Christie, B. R., Matheson, B. G., and Nowak, J. 1997. Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol. Fertil. Soils, 25: 13-19. doi: 10. 1007/s003740050273.
39. Sturz, A. V., Christie, B. R., Matheson, B. G., Arsenault, W. J., and Buchanan, N. A. 1999. Endophytic bacterial communities in the periderm of potato tubers and their potential to improve resistance to soil-borne plant pathogens. Plant Pathol. 48: 360-369. doi: 10. 1046/j. 1365-3059. 1999. 00351. x.
40. Tilak, K., Ranganayak, N., Pal, K., Dey, R., Saxena, A., Shekhar-Nautiyal, C., et al. 2005. Diversity of plant growth and soil health-supporting bacteria. Curr. Sci. 89(1): 136-150.
41. Van damme, P., Pot., B., Gillis, M., De Vos, P., Kerstens, K., and Swings, J. 1996. Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol. Rev. 60: 407-438. PMID: 8801440.
42. Van Zyl, E., and Steyn, P. L. 1990. Differentiation of phytopathogenic Pseudomonas and Xanthomonas species and pathovars by numerical taxonomy and protein gel electrophoregrams. Syst. Appl. Microbiol. 13: 60-71. doi: 10. 1016/S0723-2020(11)80181-5.
43. Vincent, J. M. 1970. A manual for the practical study of the root-nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications, Oxford, UK.
44. Wade, W. 2002. Unculturable bacteria-the uncharacterized organisms that cause oral infections. J. R. Soc. Med. 95: 81-83. doi: 10. 1258/jrsm. 95. 2. 81. PMID: 11823550.
45. Yao, Z. Y., Kan, F. L., Wang, E. T., and Chen, W. X. 2002. Characterization of rhizobia that nodulate legume species within the genus Lespedeza and description of Bradyrhizobium yuanmingense sp. nov. Int. J. Syst. Evol. Microbiol. 52: 2219-2230. doi: 10. 1099/ijs. 0. 01408-0. PMID: 12508891.
46. Zakhia, F., Jeder, H., Willems, A., Gillis, M., Dreyfus, B., and de Lajudie, P. 2006. Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb. Ecol. 51: 375-393. doi: 10. 1007/s00248-006-9025-0. PMID: 16598639.