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Diversity, Quorum Sensing, and Plant Growth Promotion by Endophytic Diazotrophs Associated with Sugarcane with Special Reference to Gluconacetobacter diazotrophicus

  • Iqbal Ahmad
  • Mohd. Musheer AltafEmail author
  • Jyoti Sharma
  • Abdullah Safar Al-thubiani
Chapter
  • 1.1k Downloads

Abstract

Endophytic bacteria are widely distributed among plants and colonize both intracellular and intercellular spaces and do not harm the host plant. However, the distributions of endophytic diazotrophs are limited. Endophytic diazotrophs like Gluconacetobacter diazotrophicus are mainly associated with sugarcane and some other plants and responsible for significant contribution of biological nitrogen fixation with sugarcane. In this article, we described the diversity and role of quorum sensing. We also discussed the contributions of different bacterial traits that are necessary for successful colonization of the plant interior part. Further mechanisms of plant growth promotion are elaborated. Molecular characterization and identification of endophytic diazotrophs will further help in better understanding of plant colonization and plant growth promotion.

Keywords

Gluconacetobacter Plant growth promotion Endophytes Sugarcane Quorum sensing 

References

  1. Adriano-Anaya M, Salvador-Figueroa M, Ocampo JA et al (2005) Plant cell-wall degrading hydrolytic enzymes of Gluconacetobacter diazotrophicus. Symbiosis 40:151–156Google Scholar
  2. Ahmad I, Sharma J, Ahmad F (2004) Isolation and characterization of resistance traits of indigenous strains of Acetobacter diazotrophicus associated with sugarcane. Sugar Tech 6:41–46CrossRefGoogle Scholar
  3. Ait Barka E, Belarbi A, Hachet C et al (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera cocultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186:91–95CrossRefGoogle Scholar
  4. Ait Barka E, Gognies S, Nowak J et al (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Control 24:135–142CrossRefGoogle Scholar
  5. Ali S, Duan J, Charles TC (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343:193–198CrossRefPubMedGoogle Scholar
  6. Amann RI, Binder BJ, Olson RJ et al (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925PubMedPubMedCentralGoogle Scholar
  7. Bais HP, Weir TL, Perry LG et al (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266CrossRefPubMedGoogle Scholar
  8. Baldani JI, Baldani VLD, Seldin L et al (1986) Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a root-associated nitrogen-fixing bacterium. Int J Syst Bacteriol 36:86–93CrossRefGoogle Scholar
  9. Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608CrossRefGoogle Scholar
  10. Boddey RM, Polidoro JC, Resende AS et al (2001) Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses. Aus J Plant Physiol 28:889–895Google Scholar
  11. Boddey RM, Urquiaga S, Alves BJR et al (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149CrossRefGoogle Scholar
  12. Böhm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol Plant-Microbe Interact 20:526–533CrossRefPubMedGoogle Scholar
  13. Boniolo FS, Rodrigues RC, Delatorre EO et al (2009) Glycine betaine enhances growth of nitrogen-fixing bacteria Gluconacetobacter diazotrophicus PAL5 under saline stress conditions. Curr Microbiol 59:593–595CrossRefPubMedGoogle Scholar
  14. Brader G, Compant S, Mitter B et al (2014) A: metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cavalcante VA, Döbereiner J (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108:23–31CrossRefGoogle Scholar
  16. Chauhan H, Sharma A, Saini SK (2010) Response of sugarcane to endophytic bacterial inoculation. Ind J Sugar Tech 25:1–4Google Scholar
  17. Chernin L, Chet I (2002) Microbial enzymes in biocontrol of plant pathogens and pests. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York, pp 171–225Google Scholar
  18. Chi F, Shen SH, Cheng HP et al (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(11):7271–7278CrossRefPubMedPubMedCentralGoogle Scholar
  19. Cocking EC, Stone PJ, Davey MR (2006) Intracellular colonization of roots of Arabidopsis and crop plants by Gluconacetobacter diazotrophicus. In Vitro Cell Dev Biol 42:74–82CrossRefGoogle Scholar
  20. Compant S, Duffy B, Nowak J (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959CrossRefPubMedPubMedCentralGoogle Scholar
  21. Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678CrossRefGoogle Scholar
  22. Compant S, Mitter B, Colli-Mull JG (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197CrossRefPubMedGoogle Scholar
  23. Costa LEO, Queiroz MV, Borges AC et al (2012) Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (P. vulharis). Br J Microbiol 43:1562–1575CrossRefGoogle Scholar
  24. Dobereiner J, Day JM (1976) Associative symbiosis and free-living systems. In: Newton WE, Nyman CJ (eds) Proceedings of the 1st international symposium on nitrogen fixation. Washington State University Press, Pullman, pp 518–538Google Scholar
  25. Eskin N, Vessey K, Tian L (2014) Research progress and perspectives of nitrogen fixing bacterium, Gluconacetobacter diazotrophicus, in monocot plants. Int J Agron 2014(4):1–13Google Scholar
  26. Ezra D, Castillo UF, Strobel GA et al (2004) Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology 150:785–793CrossRefPubMedGoogle Scholar
  27. Farrar K, Bryant D, Cope‐Selby N (2014) Understanding and engineering beneficial plant microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J 12:1193–1206CrossRefPubMedPubMedCentralGoogle Scholar
  28. Foley JA, Ramankutty N, Brauman KA et al (2011) Solutions for a cultivated planet. Nature 478:337–342CrossRefPubMedGoogle Scholar
  29. Franke-Whittle IH, O’Shea MG, Leonard GJ et al (2005) Design, development, and use of molecular primers and probes for the detection of Gluconacetobacter species in the pink sugarcane mealy bug. Microb Ecol 50:128–139CrossRefPubMedGoogle Scholar
  30. Fuentes-Ramírez LE, Caballero-Mellado J, Sepúlveda J et al (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbio Ecol 29:117–128CrossRefGoogle Scholar
  31. Gaiero JR, McCall CA, Thompson KA et al (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100(9):1738–1750CrossRefPubMedGoogle Scholar
  32. Gillis M, Kersters K, Hoste B et al (1989) Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int J Syst Bacteriol 39:361–364CrossRefGoogle Scholar
  33. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39CrossRefPubMedGoogle Scholar
  34. Gomiero T, Pimentel D, Paoletti MG (2011) Environmental impact of different agricultural management practices: conventional vs. organic agriculture. Crit Rev Plant Sci 30:95–124CrossRefGoogle Scholar
  35. Hallmann J, Quadt-Hallmann A, Mahaffee WF et al (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  36. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471CrossRefPubMedGoogle Scholar
  37. Hari K (1995) Biofertilizers in sugarcane. Lead paper presented in 10th sugarcane research and development workers’ meeting for South Karnataka, Shimoga, Karnataka, IndiaGoogle Scholar
  38. Heffer P, Prud’homme M (2015) Fertilizer outlook 2015–2019. In: 83rd IFA annual conference, Istanbul (Turkey), 25–27 May 2015. International Fertilizer Industry Association (IFA), Paris, France, p 4Google Scholar
  39. Iniguez AL, Dong Y, Carter HD (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant-Microbe Interact 18:169–178CrossRefPubMedGoogle Scholar
  40. Jacobs MJ, Bugbee WM, Gabrielson DA (1985) Enumeration, location, and characterization of endophytic bacteria within sugar-beet roots. Can J Bot 63(7):1262–1265CrossRefGoogle Scholar
  41. James EK (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res 65:197–209CrossRefGoogle Scholar
  42. James EK, Olivares FB (1997) Infection and colonization of sugarcane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119CrossRefGoogle Scholar
  43. James EK, Olivares FL, De Oliveira ALM et al (2001) Further observations on the interaction between sugar cane and Gluconacetobacter diazotrophicus under laboratory and greenhouse conditions. J Exp Bot 52:747–760PubMedGoogle Scholar
  44. James EK, Gyaneshwar P, Manthan N (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant-Microbe Interact 15:894–906CrossRefPubMedGoogle Scholar
  45. Lee S, Flores-Encarnacion M, Contreras-Zentella M et al (2004) Indole-3-acetic acid biosynthesis is deficient in Gluconacetobacter diazotrophicus strains with mutations in cytochrome C biogenesis genes. J Bacteriol 186:5384–5391CrossRefPubMedPubMedCentralGoogle Scholar
  46. Lodewyckx C, Vangronsveld J, Porteous F et al (2002) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606CrossRefGoogle Scholar
  47. Loy A, Maixner F, Wagner M et al (2007) probe Base-an online resource for rRNA-targeted oligonucleotide probes: new features. Nucleic Acids Res 35:800–804CrossRefGoogle Scholar
  48. Luna MF, Galar ML, Aprea J et al (2010) Colonization of sorghum and wheat by seed inoculation with Gluconacetobacter diazotrophicus. Biotechnol Lett 32:1071–1076CrossRefPubMedGoogle Scholar
  49. Miche L, Balandreau J (2001) Effects of rice seed surface sterilization with hypochlorite on inoculated Burkholderia vietnamiensis. Appl Environ Microbiol 67:3046–3052CrossRefPubMedPubMedCentralGoogle Scholar
  50. Miché L, Battistoni F, Gemmer S et al (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant-Microbe Interact 19:502–511CrossRefPubMedGoogle Scholar
  51. Mohanta S, Sharma GD, Deb B (2010) Diversity of endophytic diazotrophs in non-leguminous crops – a review. Assam Univ J Sci Technol 6:109–122Google Scholar
  52. Murumkar DR, Nalawade SV, Indi DV (2016) Response of sugarcane seed plot to microbial inoculation by Gluconacetobacter diazotrophicus and phosphate-solubilizing bacteria. Sugar Tech. doi: 10.1007/s12355-016-0432-3 Google Scholar
  53. Nautiyal CS (2000) Plant beneficial rhizosphere competent bacteria. Proc Natl Acad Sci India 70:107–123Google Scholar
  54. Nieto-Penalver CG, Bertini EV, de Figueroa LIC (2012) Identification of N-acyl homoserine lactones produced by Gluconacetobacter diazotrophicus PAL5 cultured in complex and synthetic media. Arch Microbiol 194:615–622CrossRefPubMedGoogle Scholar
  55. Oliveira ALM, Canuto EL, Reis VM et al (2003) Response of micropropagated sugarcane varieties to inoculation with endophytic diazotrophic bacteria. Braz J Microbiol 34:59–61CrossRefGoogle Scholar
  56. Oliveira ALM, Canuto EDL, Urquiaga S et al (2006) Yield of micropropagated sugarcane varieties in different soil types following inoculation with diazotrophic bacteria. Plant Soil 284:23–32CrossRefGoogle Scholar
  57. Ortega-Rodes P, Ortega E, Kleiner D et al (2011) Low recovery frequency of Gluconacetobacter diazotrophicus from plants and associated mealybugs in Cuban sugarcane fields. Symbiosis 54:131–138CrossRefGoogle Scholar
  58. Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact? Front Plant Sci 2:100CrossRefPubMedPubMedCentralGoogle Scholar
  59. Paula MA, Reis VM, Dobereiner J (1991) Interactions of Glomus clarum with Acetobacter diazotrophicus in infection of sweet potato (Ipomoea batatas), sugarcane (Saccharum spp.), and d sweet sorghum (Sorghum vulgare). Biol Fertil Soils 11:111–115CrossRefGoogle Scholar
  60. Pereira GVM, Magalhães KT, Lorenzetii ER et al (2012) A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microb Ecol 63:405–417CrossRefGoogle Scholar
  61. Posada F, Vega FE (2005) Establishment of the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte in cocoa seedlings (Theobroma cacao). Mycologia 97:1195–1200CrossRefPubMedGoogle Scholar
  62. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408CrossRefGoogle Scholar
  63. Reading NC, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254:1–11CrossRefPubMedGoogle Scholar
  64. Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443CrossRefPubMedGoogle Scholar
  65. Reis Júnior FB, Silva LG, Reis VM et al (2000) Occurrence of diazothrophic bacteria in different sugar cane genotypes. [Ocorrência de bactérias diazotróficas em diferentes genótipos de cana-de-açúcar]. Pesq Agropec Bras 35:985–994CrossRefGoogle Scholar
  66. Reis VM, Baldani JI, Baldani VLD et al (2000) Biological dinitrogen fixation in gramineae and palm trees. Crit Rev Plant Sci 10:227–247CrossRefGoogle Scholar
  67. Reis V, Lee S, Kennedy C (2007) Biological nitrogen fixation in sugarcane. In: Emerich C, Newton WE (eds) Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Springer, Dordrecht, pp 213–232CrossRefGoogle Scholar
  68. Reiter B, Sessitsch A (2006) Bacterial endophytes of the wildflower Crocus albiflorus analyzed by characterization of isolates and by a cultivation-independent approach. Can J Microbiol 52:140–149CrossRefPubMedGoogle Scholar
  69. Riggs PJ, Chelius MK, Iniguez AL et al (2001) Enhanced maize productivity by inoculation with diazotrophic bacteria. Aus J Plant Physiol 28:829–836Google Scholar
  70. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Int 19:827–837CrossRefGoogle Scholar
  71. Rouws LFM, Meneses CHSG, Guedes HV et al (2010) Monitoring the colonization of sugarcane and rice plants by the endophytic diazotrophic bacterium Gluconacetobacter diazotrophicus marked with gfp and gusA reporter genes. Lett Appl Microbiol 51:325–330CrossRefPubMedGoogle Scholar
  72. Ryan RP, Germaine K, Franks A et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9CrossRefPubMedGoogle Scholar
  73. Sagarika M, Sharma GD, Deb B (2010) Diversity of endophytic diazotrophs in non leguminous crops – a review. Assam Univ J Sci Technol 6:109–122Google Scholar
  74. Saravanan VS, Madhaiyan M, Osborne J et al (2008) Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microb Ecol 55:130–140CrossRefPubMedGoogle Scholar
  75. Schultz N, Silva JA, Sousa JS (2014) Inoculation of sugarcane with diazotrophic bacteria. R Bras Ci Solo 38:407414CrossRefGoogle Scholar
  76. Schulz B, Boyle C (2006) What are endophytes? In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 1–13CrossRefGoogle Scholar
  77. Seghers D, Wittebolle L, Top EM et al (2004) Impact of agricultural practices on the Zea mays L. endophytic community. Appl Environ Microbiol 70:1475–1482CrossRefPubMedPubMedCentralGoogle Scholar
  78. Silva-Froufe LG, Boddey RM, Reis VM (2009) Quantification of natural populations of Gluconacetobacter diazotrophicus and Herbaspirillum spp. in sugarcane (Saccharum spp.) using different polyclonal antibodies. Braz J Microbiol 40:866–878CrossRefPubMedPubMedCentralGoogle Scholar
  79. Smith KP, Goodman RM (1999) Host variation for interactions with beneficial plant-associated microbes. Annu Rev Phytopathol 37:473–491CrossRefPubMedGoogle Scholar
  80. Smith SA, Tank DC, Boulanger LA et al (2008) Bioactive endophytes warrant intensified exploration and conservation. PLoS One 3, e3052CrossRefPubMedPubMedCentralGoogle Scholar
  81. Srinivasan TR, Naidu KM (1987) Response of sugarcane varieties to biofertilizers under different soil conditions. Sugarcane 3:5–11Google Scholar
  82. Suman A, Shasany AK, Singh M et al (2001) Molecular assessment of diversity among endophytic diazotrophs isolated from subtropical Indian sugarcane. World J Microbiol Biotechnol 17:39–45CrossRefGoogle Scholar
  83. Tejera NA, Ortega E, González-López J et al (2003) Effect of some abiotic factors on the biological activity of Gluconacetobacter diazotrophicus. J Appl Microbiol 95:528–535CrossRefPubMedGoogle Scholar
  84. Tian G, Pauls P, Dong Z et al (2009) Colonization of the nitrogen-fixing bacterium Gluconacetobacter diazotrophicus in a large number of Canadian corn plants. Can J Plant Sci 89:1009–1016CrossRefGoogle Scholar
  85. Tilman D, Cassman KG, Matson PA et al (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677CrossRefPubMedGoogle Scholar
  86. Timmusk S, Paalme V, Pavlicek T et al (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS ONE 6(3), e17968CrossRefPubMedPubMedCentralGoogle Scholar
  87. Vargas L, Santa Brígida AB, Mota Filho JP et al (2014) Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS ONE 9(12), e114744CrossRefPubMedPubMedCentralGoogle Scholar
  88. Velázquez E, Rojas M, Lorite MJ (2008) Genetic diversity of endophytic bacteria which could be found in the apoplastic sap of the medullary parenchyma of the stem of healthy sugarcane plants. J Basic Microbiol 48:118–124CrossRefPubMedGoogle Scholar
  89. Ward JK, Tissue DT, Thomas RB et al (1999) Comparative responses of model C3 and C4 plants to drought in low and elevated CO2. Glob Chang Biol 5:857–867CrossRefGoogle Scholar
  90. Yamada Y, Hoshino KI, Ishikawa T (1997) The phylogeny of acetic acid bacteria based on the partial sequences of 16S ribosomal RNA: the elevation of the subgenus gluconacetobacter to the generic level. Biosci Biotechnol Biochem 61:1244–1251CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2016

Authors and Affiliations

  • Iqbal Ahmad
    • 1
  • Mohd. Musheer Altaf
    • 1
    Email author
  • Jyoti Sharma
    • 2
  • Abdullah Safar Al-thubiani
    • 3
  1. 1.Department of Agricultural MicrobiologyAligarh Muslim UniversityAligarhIndia
  2. 2.Department of Science and TechnologyTechnology BhavanNew DelhiIndia
  3. 3.Department of BiologySchool of Applied Science, Umm Al-Qura UniversityMakkahSaudi Arabia

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