Understanding and engineering beneficial plant-microbe interactions: Plant growth promotion in energy crops

Plant Biotechnology Journal

Volumn 12, Issue 9, 2014, Pages 1193-1206

  Farrar, Kerrie ^a   Bryant, David ^a   Cope Selby, Naomi ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

LEANOME; Bacterial endophyte; Biofertilization; Plant microbe signalling; Sustainable agriculture; Symbiosis

Indexed keywords

BACTERIA (MICROORGANISMS);

BIOFUEL;

CROP; GENETIC ENGINEERING; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; PLANT; PLANT DEVELOPMENT; SYMBIOSIS;

BIOFUELS; CROPS, AGRICULTURAL; GENETIC ENGINEERING; PLANT DEVELOPMENT; PLANTS; SYMBIOSIS;

EID: 84911976589     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12279     Document Type: Review

References (165)

1. Abeles, F.B., Morgan, P.W. and Saltveit Jr, P.E. (1992) Ethylene in Plant Biology, 2nd edn. New York, NY: Academic Press.
2. Antunes, M.S., Morey, K.J., Smith, J.J., Albrecht, K.D., Bowen, T.A., Zdunek, J.K., Troupe, J.F., Cuneo, M.J., Webb, C.T., Hellinga, H.W. and Medford, J.I. (2011) Programmable ligand detection system in plants through a synthetic signal transduction pathway. PLoS ONE, 6, e16292.
3. Arencibia, A.D., Vinagre, F., Estevez, Y., Bernal, A., Perez, J., Cavalcanti, J., Santana, I. and Hemerly, A.S. (2006) Gluconacetobacter diazotrophicus elicits a sugarcane defense response against a pathogenic bacteria Xanthomonas albilineans. Plant Signal Behav. 1, 265-273.
4. Arora, S., Patel, P.N., Vanza, M.J. and Rao, G.G. (2014) Isolation and characterization of endophytic bacteria colonizing halophyte and other salt tolerant plant species from coastal Gujarat. Afr. J. Microbiol. Res. 8, 1779-1788.
5. Assmus, B., Hutzler, P., Kirchhof, G., Amann, R., Lawrence, J.R. and Hartmann, A. (1995) In situ localization of Azospirillum brasilense in the rhizosphere of wheat using fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl. Environ. Microbiol. 61, 1013-1019.
6. Bacilio-Jiménez, M., Aguilar-Flores, S., Ventura-Zapata, E., Pérez-Campos, E., Bouquelet, S. and Zenteno, E. (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil, 249, 271-277.
7. Badri, D.V., Weir, T.L., Van Der Lelie, D. and Vivanco, J.M. (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr. Opin. Biotechnol. 20, 642-650.
8. Bais, H.P., Walker, T.S., Schweizer, H.P. and Vivanco, J.M. (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol. Biochem. 40, 983-995.
9. Bais, H.P., Fall, R. and Vivanco, J.M. (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134, 307-319.
10. Baldani, J.I. and Baldani, V.L. (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An. Acad. Bras. Ciênc. 77, 549-579.
11. Baldani, J.I., Baldani, V., Seldin, L. and Döbereiner, J. (1986) Characterization of Herbaspirillum seropedicae gen. nov., sp. nov., a root-associated nitrogen-fixing bacterium. International Journal of Systematic Bacteriology 36(1), 86-93.
12. Baldani, V.L.D., Baldani, J.I. and Döbereiner, J. (1987) Inoculation of field-grown wheat (Triticum aestivum) with Azospirillum spp. in Brazil. Biol. Fertil. Soils, 4, 37-40.
13. Baldani, V.L.D., Baldani, J.I., Olivares, F.L. and Döbereiner, J. (1992) Identification and ecology of Herbaspirillum seropedicae and closely related Pseudomonas rubrisubalbicans. Symbiosis, 13, 65-73.
14. Baldani, J.I., Oliveira, A.L.M., Guimarães, S.L., Baldani, V.L.D., Reis Jr, F.B., Silva, L.G., Reis, V.M., Teixeira, K.R.S. and Döbereiner, J. (2000) Biological nitrogen fixation (BNF) in non-leguminous plants: the role of endophytic diazotrophs. Curr. Plant Sci. Biotechnol. Agric. 38, 397-400.
15. Bashan, Y. (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol. Adv. 16, 729-770.
16. Berg, G., Eberl, L. and Hartmann, A. (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7, 1673-1685.
17. Berman-Frank, I., Lundgren, P. and Falkowski, P. (2003) Nitrogen fixation and photosynthetic oxygen evolution in Cyanobacteria. Res. Microbiol. 154, 157-164.
18. Bertalan, M., Albano, R., de Pádua, V., Rouws, L., Rojas, C., Hemerly, A., Teixeira, K., Schwab, S., Araujo, J., Oliveira, A., França, L., Magalhães, V., Alquéres, S., Cardoso, A., Almeida, W., Loureiro, M.M., Nogueira, E., Cidade, D., Oliveira, D., Simão, T., Macedo, J., Valadão, A., Dreschsel, M., Freitas, F., Vidal, M., Guedes, H., Rodrigues, E., Meneses, C., Brioso, P., Pozzer, L., Figueiredo, D., Montano, H., Junior, J., de Souza Filho, G., Martin, Q.F.V., Ferreira, B., Branco, A., Gonzalez, P., Guillobel, H., Lemos, M., Seibel, L., Macedo, J., Alves-Ferreira, M., Sachetto-Martins, G., Coelho, A., Santos, E., Amaral, G., Neves, A., Pacheco, A.B., Carvalho, D., Lery, L., Bisch, P., Rössle, S.C., Urményi, T., Rael, P.A., Silva, R., Rondinelli, E., von Krüger, W., Martins, O., Baldani, J.I. and Ferreira, P.C.G. (2009) Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics, 10, 450.
19. Boddey, R.M., Urquiaga, S., Reis, V.M. and Döbereiner, J. (1991) Biological nitrogen fixation associated with sugar cane. Plant Soil, 137, 111-117.
20. Boddey, R.M., Oliveira, O.C., Urquiaga, S., Reis, V.M., de Olivares, F.L., Baldani, V.L.D. and Döbereiner, J. (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. Plant Soil, 174, 195-209.
21. Bonfante, P. and Anca, I.A. (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu. Rev. Microbiol. 63, 363-383.
22. Bottini, R., Cassán, F. and Piccoli, P. (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biotechnol. 65, 497-503.
23. Buanafina, M.M.D.O., Langdon, T., Hauck, B., Dalton, S. and Morris, P. (2008) Expression of a fungal ferulic acid esterase increases cell wall digestibility of tall fescue (Festuca arundinacea). Plant Biotechnol. J. 6, 264-280.
24. Buanafina, M.M.D.O., Langdon, T., Hauck, B., Dalton, S., Timms-Taravella, E. and Morris, P. (2010) Targeting expression of a fungal ferulic acid esterase to the apoplast, endoplasmic reticulum or golgi can disrupt feruloylation of the growing cell wall and increase the biodegradability of tall fescue (Festuca arundinacea). Plant Biotechnol. J. 8, 316-331.
25. Budiharjo, A., Chowdhury, S.P., Dietel, K., Beator, B., Dolgova, O., Fan, B., Bleiss, W., Ziegler, J., Schmid, M., Hartmann, A. and Borriss, R. (2014) Transposon mutagenesis of the plant-associated Bacillus amyloliquefaciens ssp. plantarum FZB42 revealed that the nfrA and RBAM17410 genes are involved in plant-microbe-interactions. PLoS ONE, 9, 5.
26. Bulgarelli, D., Rott, M., Schlaeppi, K., van Themaat, E.V.L., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., Peplies, J., Gloeckner, F.O., Amann, R., Eickhorst, T. and Schulze-Lefert, P. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91-95.
27. Cai, T., Cai, W., Zhang, J., Zheng, H., Tsou, A.M., Xiao, L., Zhong, Z. and Zhu, J. (2009) Host legume-exuded antimetabolites optimize the symbiotic rhizosphere. Mol. Microbiol. 73, 507-517.
28. Cao, Q., Op den Camp, R., Seifi Kalhor, M., Bisseling, T. and Geurts, R. (2012) Efficiency of Agrobacterium rhizogenes-mediated root transformation of Parasponia and Trema is temperature dependent. Plant Growth Regul. 68, 459-465.
29. Compant, S., Clément, C. and 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, 669-678.
30. Conn, V.M., Walker, A.R. and Franco, C.M.M. (2008) Endophytic Actinobacteria induce defense pathways in Arabidopsis thaliana. Mol. Plant Microbe Interact. 21, 208-218.
31. Dames, J.F. and Ridsdale, C.J. (2012) What we know about arbuscular mycorhizal fungi and associated soil bacteria. Afr. J. Biotechnol. 11, 13753-13760.
32. Davis, S.C., Parton, W.J., Dohleman, F.G., Smith, C.M., Grosso, S.D., Kent, A.D. and DeLucia, E.H. (2010) Comparative biogeochemical cycles of bioenergy crops reveal nitrogen-fixation and low greenhouse gas emissions in a Miscanthus × giganteus agro-ecosystem. Ecosystems, 13, 144-156.
33. Dennis, P.G., Miller, A.J. and Hirsch, P.R. (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol. Ecol. 72, 313-327.
34. Döbereiner, J., Reis, V.M., Paula, M.A. and Olivares, F. (1993) Endophytic diazotrophs in sugar cane, cereals and tuber plants. Curr. Plant Sci. Biotechnol. Agric. 17, 671-676.
35. Dodds, P.N. and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548.
36. Dong, Z., Canny, M.J., McCully, M.E., Roboredo, M.R., Cabadilla, C.F., Ortega, E. and Rodes, R. (1994) A nitrogen-fixing endophyte of sugarcane stems (a new role for the apoplast). Plant Physiol. 105, 1139-1147.
37. Doty, S.L., Oakley, B., Xin, G., Kang, J.W., Singleton, G., Khan, Z., Vajzovic, A. and Staley, J.T. (2009) Diazotrophic endophytes of native black cottonwood and willow. Symbiosis, 47, 23-33.
38. Durbak, A., Yao, H. and McSteen, P. (2012) Hormone signaling in plant development. Curr. Opin. Plant Biol. 15, 92-96.
39. Eckert, B., Weber, O.B., Kirchhof, G., Halbritter, A., Stoffels, M. and Hartmann, A. (2001) Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int. J. Syst. Evol. Microbiol. 51, 17-26.
40. Egorshina, A.A., Khairullin, R.M., Sakhabutdinova, A.R. and Luk'yantsev, M.A. (2011) Involvement of phytohormones in the development of interaction between wheat seedlings and endophytic Bacillus subtilis strain 11BM. Russ. J. Plant Physiol. 59, 134-140.
41. Elbeltagy, A., Nishioka, K., Sato, T., Suzuki, H., Ye, B., Hamada, T., Isawa, T., Mitsui, H. and Minamisawa, K. (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. isolated from wild rice species. Appl. Environ. Microbiol. 67, 5285-5293.
42. Evangelisti, E., Rey, T. and Schornack, S. (2014) Cross-interference of plant development and plant-microbe interactions. Curr. Opin. Plant Biol. 20, 118-126.
43. Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.L., Wei, P., Cao, F., Zhu, S., Zhang, F., Mao, Y. and Zhu, J.K. (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229.
44. Finlay, R.D. (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59, 1115-1126.
45. Foster, K.R. and Bell, T. (2012) Competition, not cooperation, dominates interactions among culturable microbial species. Curr. Biol. 22, 1845-1850.
46. Fowler, M. and Beck, K. (1999) Refactoring: Improving the Design of Existing Code. Reading, MA: Addison-Wesley.
47. Fuentes-Ramírez, L.E., Caballero-Mellado, J., Sepúlveda, J. and Martínez-Romero, E. (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol. Ecol. 29, 117-128.
48. Gan, H.Y., Gan, H.M., Savka, M.A., Triassi, A.J., Wheatley, M.S., Smart, L.B., Fabio, E.S. and Hudson, A.O. (2014) Whole-genome sequences of 13 endophytic bacteria isolated from shrub willow (salix) grown in Geneva, New York]. Genome Announc. 2, e00288-e00314.
49. Gillis, M., Kersters, K., Hoste, B., Janssens, D., Kroppenstedt, R.M., Stephan, M.P., Teixeira, K.R.S., Dobereiner, J. and De Ley, J. (1989) Acetobacter diazotrophicus sp. nov., a nitrogen-fixing acetic acid bacterium associated with sugarcane. Int. J. Syst. Bacteriol. 39, 361-364.
50. Glick, B.R. (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169, 30-39.
51. Goldfarb, K.C., Karaoz, U., Hanson, C.A., Santee, C.A., Bradford, M.A., Treseder, K.K., Wallenstein, M.D. and Brodie, E.L. (2011) Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front. Microbiol. 2, 94, 1-10.
52. Greenberg, E.P. (1997) Quorum sensing in Gram-negative bacteria. ASM News, 63, 371-377.
53. Großkopf, T. and Soyer, O.S. (2014) Synthetic microbial communities. Curr. Opin. Microbiol. 18, 72-77.
54. Hardoim, P.R., van Overbeek, L.S. and Elsas, J.D.V. (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol. 16, 463-471.
55. Heaton, E.A., Flavell, R.B., Mascia, P.N., Thomas, S.R., Dohleman, F.G. and Long, S.P. (2008) Herbaceous energy crop development: recent progress and future prospects. Curr. Opin. Biotechnol. 19, 202-209.
56. Hildebrandt, U., Janetta, K. and Bothe, H. (2002) Towards growth of arbuscular mycorrhizal fungi independent of a plant host. Appl. Environ. Microbiol. 68, 1919-1924.
57. Hirsch, A.M. (2004) Plant-microbe symbioses: a continuum from commensalism to parasitism. Symbiosis, 37, 345-363.
58. Hottes, A.K., Freddolino, P.L., Khare, A., Donnell, Z.N., Liu, J.C. and Tavazoie, S. (2013) Bacterial adaptation through loss of function. PLoS Genet. 9, e1003617.
59. Hungria, M., Campo, R.J., Souza, E.M. and Pedrosa, F.O. (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil, 331, 413-425.
60. Hurek, T., Reinhold-Hurek, B., Van Montagu, M. and Kellenberger, E. (1994) Root colonization and systemic spreading of Azoarcus sp. strain BH72 in grasses. J. Bacteriol. 176, 1913-1923.
61. Iqbal, A. and Hasnain, S. (2013) Auxin producing Pseudomonas strains: biological candidates to modulate the growth of Triticum aestivum beneficially. Am. J. Plant Sci. 4, 1693-1700.
62. Isawa, T., Yasuda, M., Awazaki, H., Minamisawa, K., Shinozaki, S. and Nakashita, H. (2010) Azospirillum sp. strain B510 enhances rice growth and yield. Microbes Environ. 25, 58-61.
63. James, E.K. (2000) Nitrogen fixation in endophytic and associative symbiosis. Field Crops Res. 65, 197-209.
64. James, E.K. and Olivares, F.L. (1998) Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit. Rev. Plant Sci. 17, 77-119.
65. James, E.K., Reis, V.M., Olivares, F.L., Baldani, J.I. and Döbereiner, J. (1994) Infection of sugar cane by the nitrogen-fixing bacterium Acetobacter diazotrophicus. J. Exp. Bot. 45, 757-766.
66. James, E.K., Olivares, F.L., Baldani, J.I. and Döbereiner, J. (1997) Herbaspirillum, an endophytic diazotroph colonizing vascular tissue in leaves of Sorghum bicolor L. Moench. J. Exp. Bot. 48, 785-797.
67. Jarboe, L.R., Zhang, X., Wang, X., Moore, J.C., Shanmugam, K.T. and Ingram, L.O. (2010) Metabolic engineering for production of biorenewable fuels and chemicals: contributions of synthetic biology. BioMed Research International, 2010. Article ID 761042, doi:10.1155/2010/761042
68. Jones, D.L., Nguyen, C. and Finlay, R.D. (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil, 321, 5-33.
69. Jones, M.B., Finnan, J. and Hodkinson, T.R. (2014) Morphological and physiological traits for higher biomass production in perennial rhizomatous grasses grown on marginal land. Glob. Change Biol. Bioenergy, Doi: 10.1111/gcbb.12203.
70. Kachroo, A. and Robin, G.P. (2013) Systemic signaling during plant defense. Curr. Opin. Plant Biol. 16, 527-533.
71. Keymer, D.P. and Kent, A.D. (2013) Contribution of nitrogen fixation to first year Miscanthus × giganteus. Glob. Change Biol. Bioenergy, Glob. Change Biol. Bioenergy 6(5), 577-586.
72. Khan, Z. and Doty, S.L. (2009) Characterization of bacterial endophytes of sweet potato plants. Plant Soil, 322, 197-207.
73. Kim, S., Lowman, S., Hou, G., Nowak, J., Flinn, B. and Mei, C. (2012) Growth promotion and colonization of switchgrass (Panicum virgatum) cv. Alamo by bacterial endophyte Burkholderia phytofirmans strain PsJN. Biotechnol. Biofuels, 5, 37.
74. Kirchhof, G., Reis, V.M., Baldani, J.I., Eckert, B., Döbereiner, J. and Hartmann, A. (1997) Occurrence, physiological and molecular analysis of endophytic diazotrophic bacteria in gramineous energy plants. In Opportunities for Biological Nitrogen Fixation in Rice and Other Non-Legumes (Ladha, J.K., de Bruijn, F.J. & Malik, K.A. eds), pp. 45-55. the Netherlands: Springer.
75. Kirchhof, G., Baldani, J.I., Reis, V.M. and Hartmann, A. (1998) Molecular assay to identify Acetobacter diazotrophicus and detect its occurrence in plant tissues. Can. J. Microbiol. 44, 12-19.
76. Kirchhof, G., Eckert, B., Stoffels, M., Baldani, J.I., Reis, V.M. and Hartmann, A. (2001) Herbaspirillum frisingense sp. nov., a new nitrogen-fixing bacterial species that occurs in C4-fibre plants. Int. J. Syst. Evol. Microbiol. 51, 157-168.
77. Kloepper, J.W. and Ryu, C.-M. (2006) Bacterial endophytes as elicitors of induced systemic resistance. Soil Biol. 9, 33-52.
78. Kusari, P., Kusari, S., Lamshöft, M., Sezgin, S., Spiteller, M. and Kayser, O. (2014) Quorum quenching is an antivirulence strategy employed by endophytic bacteria. Appl. Microbiol. Biotechnol. 98(16), 7173-7183.
79. Lakshmanan, V., Kitto, S.L., Caplan, J.L., Hsueh, Y.-H., Kearns, D.B., Wu, Y.-S. and Bais, H.P. (2012) Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol. 160, 1642-1661.
80. Leite, M.C.B.S., de Farias, A.R.B., Freire, F.J., Andreote, F.D., Sobral, J.K. and Freire, M.B.G.S. (2014) Isolation, bioprospecting and diversity of salt-tolerant bacteria associated with sugarcane in soils of Pernambuco, Brazil. Rev. Bras. Eng. Agríc. Amb. 18, S73-S79.
81. van der Lelie, D., Taghavi, S., Monchy, S., Schwender, J., Miller, L., Ferrieri, R., Rogers, A., Wu, X., Zhu, W., Weyens, N., Vangronsveld, J. and Newman, L. (2009) Poplar and its bacterial endophytes: coexistence and harmony. Crit. Rev. Plant Sci. 28, 346-358.
82. Lery, L.M., Hemerly, A.S., Nogueira, E.M., von Krüger, W.M. and Bisch, P.M. (2011) Quantitative proteomic analysis of the interaction between the endophytic plant-growth-promoting bacterium Gluconacetobacter diazotrophicus and sugarcane. Mol. Plant Microbe Interact. 24, 562-576.
83. Lewandowski, I., Scurlock, J.M., Lindvall, E. and Christou, M. (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy, 25, 335-361.
84. Looger, L.L., Dwyer, M.A., Smith, J.J. and Hellinga, H.W. (2003) Computational design of receptor and sensor proteins with novel functions. Nature, 423, 185-190.
85. van Loon, L.C., Bakker, P.A. and Pieterse, C.M. (1998) Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36, 453-483.
86. Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., et al. (2012) Defining the core, Arabidopsis thaliana root microbiome. Nature, 488, 86-90.
87. Luo, S., Xu, T., Chen, L., Chen, J., Rao, C., Xiao, X., Wan, Y., Zeng, G., Long, F., Liu, C. and Liu, Y. (2012) Endophyte-assisted promotion of biomass production and metal-uptake of energy crop sweet sorghum by plant-growth-promoting endophyte Bacillus sp. SLS18. Appl. Microbiol. Biotechnol. 93, 1745-1753.
88. Magnani, G.S., Didonet, C.M., Cruz, L.M., Picheth, C.F., Pedrosa, F.O. and Souza, E.M. (2010) Diversity of endophytic bacteria in Brazilian sugarcane. Genet. Mol. Res. 9, 250-258.
89. Malik, K.A., Bilal, R., Mehnaz, S., Rasul, G., Mirza, M.S. and Ali, S. (1997) Association of nitrogen-fixing, plant-growth-promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil, 194, 37-44.
90. Mark, G.L., Dow, J.M., Kiely, P.D., Higgins, H., Haynes, J., Baysse, C., Abbas, A., Foley, T., Franks, A., Morrissey, J. and O'Gara, F. (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc. Natl Acad. Sci. USA, 102, 17454-17459.
91. Mastretta, C., Taghavi, S., Van Der Lelie, D., Mengoni, A., Galardi, F., Gonnelli, C., Barac, T., Boulet, J., Weyens, N. and Vangronsveld, J. (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int. J. Phytorem. 11, 251-267.
92. Mathesius, U. (2009) Comparative proteomic studies of root-microbe interactions. J. Proteom. 72, 353-366.
93. Mei, C. and Flinn, B.S. (2010) The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Pat. Biotechnol. 4, 81-95.
94. Mendes, R., Pizzirani-Kleiner, A.A., Welington, L.A. and Raaijmakers, J.M. (2007) Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. Appl. Environ. Microbiol. 73, 7259-7267.
95. Mitter, B., Petric, A., Shin, M.W., Chain, P.S., Hauberg-Lotte, L., Reinhold-Hurek, B., Nowak, J. and Sessitsch, A. (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 4, Article 120.
96. Miyamoto, T., Kawahara, M. and Minamisawa, K. (2004) Novel endophytic nitrogen-fixing clostridia from the grass Miscanthus sinensis as revealed by terminal restriction fragment length polymorphism analysis. Appl. Environ. Microbiol. 70, 6580-6586.
97. Monteiro, R.A., Balsanelli, E., Tuleski, T., Faoro, H., Cruz, L.M., Wassem, R., de Baura, V.A., Tadra-Sfeir, M.Z., Weiss, V., DaRocha, W.D., Muller-Santos, M., Chubatsu, L.S., Huergo, L.F., Pedrosa, F.O. and de Souza, E.M. (2012a) Genomic comparison of the endophyte Herbaspirillum seropedicae SmR1 and the phytopathogen Herbaspirillum rubrisubalbicans M1 by suppressive subtractive hybridization and partial genome sequencing. FEMS Microbiol. Ecol. 80, 441-451.
98. Monteiro, R.A., Alsanelli, E., Wassem, R., Marin, A.M., Brusamarello-Santos, L.C.C., Schmidt, M.A., Tadra-Sfeir, M.Z., Pankievicz, V.C.S., Cruz, L.M., Chubatsu, L.S., Pedrosa, F.O. and Souza, E.M. (2012b) Herbaspirillum-plant interactions: microscopical, histological and molecular aspects. Plant Soil, 356, 175-196.
99. Moran, N.A., McLaughlin, H.J. and Sorek, R. (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science, 323, 379-382.
100. Naveed, M., Hussain, B., Zahir, A., Mitter, B. and Sessitsch, A. (2014a) Drought stress amelioration in wheat through inoculation with Burkholderia phytofirmans strain PsJN. Plant Growth Regul. 73, 121-131.
101. Naveed, M., Mitter, B., Reichenauer, T.G., Wieczorek, K. and Sessitsch, A. (2014b) Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ. Exp. Bot. 97, 30-39.
102. Newman, M.A., Sundelin, T., Nielsen, J.T. and Erbs, G. (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 4, 139.
103. Nithya, A., Gothandam, K.M. and Babu, S. (2014) Alternative ecology of human pathogenic bacteria in fruits and vegetables. Plant Pathol. J. 13, 1-7.
104. Okon, Y. and Itzigsohn, R. (1995) The development of Azospirillum as a commercial inoculant for improving crop yields. Biotechnol. Adv. 13, 415-424.
105. Oldroyd, E.D.G., Murray, J.D., Poole, P.S. and Downie, J.A. (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119-144.
106. Olivares, F.L., Baldani, V.L.D., Reis, V.M., Baldani, J.I. and Döbereiner, J. (1996) Occurrence of the endophytic diazotrophs Herbaspirillum spp. in roots, stems, and leaves, predominantly of Gramineae. Biol. Fertil. Soils, 21, 197-200.
107. de Oliveira, Z.M., Floh, E.I., Ferrara, F.I. and Barbosa, H.R. (2011) Diazotrophyc rhizobacteria isolated from sugarcane can release amino acids in a synthetic culture medium. Biol. Fertil. Soils, 47, 957-962.
108. Onofre-Lemus, J., Hernández-Lucas, I., Girard, L. and Caballero-Mellado, J. (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl. Environ. Microbiol. 75, 6581-6590.
109. Pariona-Llanos, R., Ibañez de Santi Ferrara, F., Soto Gonzales, H.H. and Barbosa, H.R. (2010) Influence of organic fertilization on the number of culturable diazotrophic endophytic bacteria isolated from sugarcane. Eur. J. Soil Biol. 46, 387-393.
110. Paungfoo-Lonhienne, C., Lonhienne, T.G., Yeoh, A., Yun, K., Webb, I.R., Lakshmanan, P., Chan, C., Xin, L., Phaik-Eem, R.M.A., Schmidt, S. and Hugenholtz, P. (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microb. Biotechnol. 2, 142-154.
111. Pedrosa, F.O. (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet. 7, 1-10.
112. Pereira, J.A. and Baldani, J.I. (1995) Selection of Azospirillum spp. and Herbaspirillum seropedicae strains to inoculate rice and maize plants. In International Symposium on Sustainable Agriculture for the Tropics-the role of Biological Nitrogen Fixation, pp. 220-221.
113. Pieterse, C.M.J. (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell, 10, 1571-1580.
114. Puchta, H. and Fauser, F. (2014) Synthetic nucleases for genome engineering in plants: prospects for a bright future. Plant J. 78, 727-741.
115. Qin, S., Xing, K., Jiang, J.H., Xu, L.H. and Li, W.J. (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl. Microbiol. Biotechnol. 89, 457-473.
116. Rajesh, P.S. and Ravishankar, R.V. (2013) Quorum quenching activity in cell-free lysate of endophytic bacteria isolated from Pterocarpus santalinus Linn., and its effect on quorum sensing regulated biofilm in Pseudomonas aeruginosa PAO1. Microbiol. Res. 169(7-8), 561-568.
117. Ramey, B.E., Koutsoudis, M., von Bodman, S.B. and Fuqua, C. (2004) Biofilm formation in plant-microbe associations. Curr. Opin. Microbiol. 7, 602-609.
118. Ratón, T.D.L.M.O., Yano, R., Gámez, O.R., Floh, E.I.S., Díaz, M.D.J.S. and Barbosa, H.R. (2012) Isolation and characterisation of aerobic endospore forming Bacilli from sugarcane rhizosphere for the selection of strains with agriculture potentialities. World J. Microbiol. Biotechnol. 28, 1593-1603.
119. Reinhold-Hurek, B. and Hurek, T. (2011) Living inside plants: bacterial endophytes. Curr. Opin. Plant Biol. 14, 435-443.
120. Rogers, A., McDonald, K., Muehlbauer, M.F., Hoffman, A., Koenig, K., Newman, L., Taghavi, S. and Lelie, D. (2012) Inoculation of hybrid poplar with the endophytic bacterium Enterobacter sp. 638 increases biomass but does not impact leaf level physiology. GCB Bioenergy 4, 364-370.
121. Rosenblueth, M. and Martínez-Romero, E. (2006) Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 19, 827-837.
122. Rothballer, M., Eckert, B., Schmid, M., Fekete, A., Schloter, M., Lehner, A., Pollmann, S. and Hartmann, A. (2008) Endophytic root colonization of gramineous plants by Herbaspirillum frisingense. FEMS Microbiol. Ecol. 66, 85-95.
123. Rouws, L.F., Simões-Araújo, J.L., Hemerly, A.S. and Baldani, J.I. (2008) Validation of a Tn5 transposon mutagenesis system for Gluconacetobacter diazotrophicus through characterization of a flagellar mutant. Arch. Microbiol. 189, 397-405.
124. Ryan, R.P., Germaine, K., Franks, A., Ryan, D.J. and Dowling, D.N. (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278, 1-9.
125. Santi, C., Bogusz, D. and Franche, C. (2013) Biological nitrogen fixation in non-legume plants. Ann. Bot. 111, 743-767.
126. Serrano, L. (2007) Synthetic biology: promises and challenges. Mol. Syst. Biol. 3, 158.
127. Sessitsch, A., Hardoim, P., Döring, J., Weilharter, A., Krause, A., Woyke, T., Mitter, B., Hauberg-Lotte, L., Friedrich, F., Rahalkar, M., Hurek, T., Sarkar, A., Bodrossy, L., van Overbeek, L., Brar, D., van Elsas, J.D. and Reinhold-Hurek, B. (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant Microbe Interact. 25, 28-36.
128. Shidore, T., Dinse, T., Öhrlein, J., Becker, A. and Reinhold-Hurek, B. (2012) Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Environ. Microbiol. 14, 2775-2787.
129. Simmons, B.A., Loque, D. and Blanch, H.W. (2008) Next-generation biomass feedstocks for biofuel production. Genome Biol. 9, 242.
130. Smith, S.E. and Smith, F.A. (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62, 227-250.
131. Spaepen, S., Vanderleyden, J. and Remans, R. (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31, 425-448.
132. Steenhoudt, O. and Vanderleyden, J. (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol. Rev. 24, 487-506.
133. Stewart, E.J. (2012) Growing unculturable bacteria. J. Bacteriol. 194, 4151-4160.
134. Straub, D., Rothballer, M., Hartmann, A. and Ludewig, U. (2013a) The genome of the endophytic bacterium H. frisingense GSF30(T) identifies diverse strategies in the Herbaspirillum genus to interact with plants. Front. Microbiol. 4, 168.
135. Straub, D., Yang, H., Liu, Y., Tsap, T. and Ludewig, U. (2013b) Root ethylene signalling is involved in Miscanthus sinensis growth promotion by the bacterial endophyte Herbaspirillum frisingense GSF30T. J. Exp. Bot. 64, 4603-4615.
136. Sturz, A.V. and Kimpinski, J. (2004) Endoroot bacteria derived from marigolds (Tagetes spp.) can decrease soil population densities of root-lesion nematodes in the potato root zone. Plant Soil, 262, 241-249.
137. Sun, N. and Zhao, H. (2013) Transcription activator-like effector nucleases (TALENs): a highly efficient and versatile tool for genome editing. Biotechnol. Bioeng. 110, 1811-1821.
138. Suto, M., Takebayashi, M., Saito, K., Tanaka, M., Yokota, A. and Tomita, F. (2002) Endophytes as producers of xylanase [online]. J. Biosci. Bioeng. 93, 88-90.
139. Taghavi, S., Garafola, C., Monchy, S., Newman, L., Hoffman, A., Weyens, N., Barac, T., Vangronsveld, J. and Daniel van der Lelie, D. (2009) Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 75, 748-757.
140. Taghavi, S., Garafola, C., Monchy, S., Newman, L., Hoffman, A., Weyens, N., Barac, T., Vangronsveld, J. and van der Lelie, D. (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet. 6, e1000943.
141. Temme, K., Dehua, Z. and Voigt, C.A. (2012) Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca. Proc. Natl Acad. Sci. USA, 109, 7085-7090.
142. Theocharis, A., Bordiec, S., Fernandez, O., Paquis, S., Dhondt-Cordelier, S., Baillieul, F., Clément, C. and Barka, E.A. (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol. Plant Microbe Interact. 25, 241-249.
143. Tikhonovich, I.A. and Provorov, N.A. (2011) Microbiology is the basis of sustainable agriculture: an opinion. Ann. Appl. Biol. 159, 155-168.
144. Tilman, D. (1998) The greening of the green revolution. Nature, 396, 211-212.
145. Toft, C. and Andersson, S.V.G. (2010) Evolutionary microbial genomics: insights into bacterial host adaptation. Nat. Rev. Genet. 11, 465-475.
146. Tsavkelova, E.A., Klimova, S.Y., Cherdyntseva, T.A. and Netrusov, A.I. (2006) Hormones and hormone-like substances of microorganisms: A review. Appl. Biochem. Microbiol. 42, 229-235.
147. Tuck, G., Glendining, M.J., Smith, P., House, J.I. and Wattenbach, M. (2006) The potential distribution of bioenergy crops in Europe under present and future climate. Biomass Bioenergy, 30, 183-197.
148. Turner, T.R., Ramakrishnan, K., Walshaw, J., Heavens, D., Alston, M., Swarbreck, D., Osbourn, A., Grant, A. and Poole, P.S. (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J. 7, 2248-2258.
149. Umenhoffer, K., Fehér, T., Balikó, G., Ayaydin, F., Pósfai, J., Blattner, F.R. and Pósfai, G. (2010) Reduced evolvability of Escherichia coli MDS42, an IS-less cellular chassis for molecular and synthetic biology applications. Microb. Cell Fact. 9, 1-12.
150. Van Aken, B., Peres, C.M., Doty, S.L., Yoon, J.M. and Schnoor, J.L. (2004) Methylobacterium populi sp. nov., a novel aerobic, pink-pigmented, facultatively methylotrophic, methane-utilizing bacterium isolated from poplar trees (Populus deltoids × nigra DN34). Int. J. Syst. Evol. Microbiol. 54, 1191-1196.
151. Vartoukian, S.R., Palmer, R.M. and Wade, W.G. (2010) Strategies for culture of 'unculturable'bacteria. FEMS Microbiol. Lett. 309, 1-7.
152. Velázquez-Hernández, M.L., Baizabal-Aguirre, V.M., Cruz-Vázquez, F., Trejo-Contreras, M.J., Fuentes-Ramírez, L.E., Bravo-Patiño, A. and Valdez-Alarcón, J.J. (2011) Gluconacetobacter diazotrophicus levansucrase is involved in tolerance to NaCl, sucrose and desiccation, and in biofilm formation. Arch. Microbiol. 193, 137-149.
153. Videira, S.S., Oliveira, D.M., Morais, R.F., Borges, W.L., Baldani, V.L.D. and Baldani, J.I. (2012) Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field. Plant Soil, 356, 51-66.
154. Walker, T.S., Bais, H.P., Grotewold, E. and Vivanco, J.M. (2003) Root exudation and rhizosphere biology. Plant Physiol. 132, 44-51.
155. Werner, J.J., Knights, D., Garciac, M.L., Scalfone, N.B., Smith, S., Yarasheski, K., Cummings, T.A., Beerse, A.R., Knight, R. and Angenenta, L.T. (2011) Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc. Natl Acad. Sci. USA, 108, 4158-4163.
156. Weyens, N., van der Lelie, D., Taghavi, S., Newman, L. and Vangronsveld, J. (2009a) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol. 27, 591-598.
157. Weyens, N., van der Lelie, D., Taghavi, S. and Vangronsveld, J. (2009b) Phytoremediation: plant-endophyte partnerships take the challenge. Curr. Opin. Biotechnol. 20, 248-254.
158. Wirthmueller, L., Maqbool, A. and Banfield, M.J. (2013) On the front line: structural insights into plant-pathogen interactions. Nat. Rev. Microbiol. 11, 761-776.
159. Yang, J., Kloepper, J.W. and Ryu, C.M. (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14, 1-4.
160. Ye, B., Saito, A. and Minamisawa, K. (2005) Effect of inoculation with anaerobic nitrogen-fixing consortium on salt tolerance of Miscanthus sinensis. Soil Sci. Plant Nutr. 51, 243-249.
161. Yuan, Z.-C., Haudecoeur, E., Faure, D., Kerr, K.F. and Nester, E.W. (2008) Comparative transcriptome analysis of Agrobacterium tumefaciens in response to plant signal salicylic acid, indole-3-acetic acid and gamma-amino butyric acid reveals signalling cross-talk and Agrobacterium-plant co-evolution. Cell. Microbiol. 10, 2339-2354.
162. Zhang, N., Wang, D., Liu, Y., Li, S., Shen, Q. and Zhang, R. (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil, 374, 689-700.
163. Zhao, L. (2010) Genomics: the tale of our other genome. Nature, 465, 879-880.
164. Zinniel, D.K., Lambrecht, P., Harris, N.B., Feng, Z., Kuczmarski, D., Higley, P. and Vidaver, A.K. (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl. Environ. Microbiol. 68, 2198-2208.
165. Zuccaro, A., Lahrmann, U., Güldener, U., Langen, G., Pfiffi, S., Biedenkopf, D., Wong, W., Samans, B., Grimm, C., Basiewicz, M., Murat, C., Martin, F. and Kogel, K.H. (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog. 7, e1002290.