Preferential association of endophytic bradyrhizobia with different rice cultivars and its implications for rice endophyte evolution

Applied and Environmental Microbiology

Volumn 81, Issue 9, 2015, Pages 3049-3061

  Piromyou, Pongdet ^a   Greetatorn, Teerana ^a   Teamtisong, Kamonluck ^a   Okubo, Takashi ^b   Shinoda, Ryo ^b   Nuntakij, Achara ^c   Tittabutr, Panlada ^a   Boonkerd, Nantakorn ^a   Minamisawa, Kiwamu ^b   Teaumroong, Neung ^a  

^a SURANAREE UNIVERSITY OF TECHNOLOGY   (Thailand)

^b TOHOKU UNIVERSITY   (Japan)

^c Department of Agriculture   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; CROPS;

AESCHYNOMENE AMERICANA; LEGUMINOUS PLANTS; PLANT COLONIZATION; RICE (ORYZA SATIVA); RICE CULTIVARS; SELECTIVE MEDIUM; SYSTEM SUPPORTS; THAI RICE CULTIVARS;

STRAIN;

BACTERIUM; COLONIZATION; CROP ROTATION; CULTIVAR; ENDOPHYTE; GROWTH RATE; LEGUME; NODULATION; OLIGOTROPHIC ENVIRONMENT; PLANTATION; RICE; SYMBIOSIS;

AESCHYNOMENE AMERICANA; AESCHYNOMENE EVENIA; AESCHYNOMENE INDICA; BACTERIA (MICROORGANISMS); BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; BRADYRHIZOBIUM SP.; FABACEAE; MACROPTILIUM ATROPURPUREUM; ORYZA SATIVA; PHOTORHIZOBIUM; VIGNA RADIATA;

BRADYRHIZOBIACEAE; ENDOPHYTE; FABACEAE; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; NODULATION; ORYZA; PHYSIOLOGY; PLANT DEVELOPMENT; SYMBIOSIS;

BRADYRHIZOBIACEAE; ENDOPHYTES; FABACEAE; ORYZA; PLANT DEVELOPMENT; PLANT ROOT NODULATION; SYMBIOSIS;

EID: 84927784735     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04253-14     Document Type: Article

References (50)

1. Okubo T, Fukushima S, Itakura M, Oshima K, Longtonglang A, Teaumroong N, Mitsui H, Hattori M, Hattori R, Hattori T. 2013. Soil oligotrophic bacterium Agromonas oligotrophica (Bradyrhizobium oligotrophicum) is a nitrogen-fixing symbiont of Aeschynomene indica as suggested by genome analysis. Appl Environ Microbiol 79:2542-2551. http://dx.doi.org/10.1128/AEM.00009-13.
2. Chaintreuil C, Giraud E, Prin Y, Lorquin J, Bâ A, Gillis M, de Lajudie P, Dreyfus B. 2000. Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl Environ Microbiol 66: 5437-5447. http://dx.doi.org/10.1128/AEM.66.12.5437-5447.2000.
3. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R. 1998. Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57-67. http://dx.doi.org/10.1023/A:1004326910584.
4. Stephens J, Rask H. 2000. Inoculant production and formulation. Field Crops Res 65:249-258. http://dx.doi.org/10.1016/S0378-4290(99)00090-8.
5. Abbasi MK, Majeed A, Sadiq A, Khan SR. 2008. Application of Bradyrhizobium japonicum and phosphorus fertilization improved growth, yield and nodulation of soybean in the sub-humid hilly region of Azad Jammu and Kashmir, Pakistan. Plant Prod Sci 11:368-376. http://dx.doi.org/10.1626/pps.11.368.
6. Saito A, Mitsui H, Hattori R, Minamisawa K, Hattori T. 1998. Slowgrowing and oligotrophic soil bacteria phylogenetically close to Bradyrhizobium japonicum. FEMS Microbiol Ecol 25:277-286. http://dx.doi.org/10.1111/j.1574-6941.1998.tb00480.x.
7. Crist DK, Wyza RE, Mills K, Bauer W, Evans W. 1984. Preservation of Rhizobium viability and symbiotic infectivity by suspension in water. Appl Environ Microbiol 47:895-900.
8. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, 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. http://dx.doi.org/10.1128/AEM.67.11.5285-5293.2001.
9. Lima AS, Nóbrega RSA, Barberi A, da Silva K, Ferreira DF, de Souza Moreira FM. 2009. Nitrogen-fixing bacteria communities occurring in soils under different uses in the Western Amazon Region as indicated by nodulation of siratro (Macroptilium atropurpureum). Plant Soil 319:127-145. http://dx.doi.org/10.1007/s11104-008-9855-2.
10. Tong Z, Sadowsky MJ. 1994. A selective medium for the isolation and quantification of Bradyrhizobium japonicum and Bradyrhizobium elkanii strains from soils and inoculants. Appl Environ Microbiol 60:581-586.
11. Baldwin E, Nisperos M, Chen X, Hagenmaier R. 1996. Improving storage life of cut apple and potato with edible coating. Postharvest Biol Technol 9:151-163. http://dx.doi.org/10.1016/S0925-5214(96)00044-0.
12. Sadowsky MJ, Tully RE, Cregan PB, Keyser HH. 1987. Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotypespecific nodulation of soybean. Appl Environ Microbiol 53:2624-2630.
13. Versalovic J, Schneider M, De Bruijn F, Lupski JR. 1994. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5:25-40.
14. Cole MA, Elkan GH. 1973. Transmissible resistance to penicillin G, neomycin, and chloramphenicol in Rhizobium japonicum. Antimicrob Agents Chemother 4:248-253. http://dx.doi.org/10.1128/AAC.4.3.248.
15. Lorquin J, Molouba F, Dreyfus BL. 1997. Identification of the carotenoid pigment canthaxanthin from photosynthetic bradyrhizobium strains. Appl Environ Microbiol 63:1151-1154.
16. Prakamhang J, Minamisawa K, Teamtaisong K, Boonkerd N, Teaumroong N. 2009. The communities of endophytic diazotrophic bacteria in cultivated rice (Oryza sativa L.). Appl Soil Ecol 42:141-149. http://dx.doi.org/10.1016/j.apsoil.2009.02.008.
17. Piromyou P, Buranabanyat B, Tantasawat P, Tittabutr P, Boonkerd N, Teaumroong N. 2011. Effect of plant growth promoting rhizobacteria (PGPR) inoculation on microbial community structure in rhizosphere of forage corn cultivated in Thailand. Eur J Soil Biol 47:44-54. http://dx.doi.org/10.1016/j.ejsobi.2010.11.004.
18. Allardet-Servent A, Michaux-Charachon S, Jumas-Bilak E, Karayan L, Ramuz M. 1993. Presence of one linear and one circular chromosome in the Agrobacterium tumefaciens C58 genome. J Bacteriol 175:7869-7874.
19. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696-704. http://dx.doi.org/10.1080/10635150390235520.
20. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
21. Kumar S, Nei M, Dudley J, Tamura K. 2008. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299-306. http://dx.doi.org/10.1093/bib/bbn017.
22. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning, a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
24. Manassila M, Nuntagij A, Kotepong S, Boonkerd N, Teaumroong N. 2007. Characterization and monitoring of selected rhizobial strains isolated from tree legumes in Thailand. Afr J Biotechnol 6:1393-1402.
25. Mae T, Ohira K. 1981. The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22:1067-1074.
26. Somasegaran P, Hoben HJ. 1994. Handbook for rhizobia: methods in legume-Rhizobium technology. Springer-Verlag, New York, NY.
27. Noisangiam R, Teamtisong K, Tittabutr P, Boonkerd N, Toshiki U, Minamisawa K, Teaumroong N. 2012. Genetic diversity, symbiotic evolution, and proposed infection process of Bradyrhizobium strains isolated from root nodules of Aeschynomene americana L. in Thailand. Appl Environ Microbiol 78:6236-6250. http://dx.doi.org/10.1128/AEM.00897-12.
28. Steel RG, Torrey JH. 1980. Principles and procedures of statistics, a biometrical approach. McGraw-Hill, New York, NY.
29. Duncan DB. 1955. Multiple range and multiple F tests. Biometrics 11:1-42. http://dx.doi.org/10.2307/3001478.
30. Ikeda S, Sasaki K, Okubo T, Yamashita A, Terasawa K, Bao Z, Liu D, Watanabe T, Murase J, Asakawa S. 2014. Low nitrogen fertilization adapts rice root microbiome to low nutrient environment by changing biogeochemical functions. Microbes Environ 29:50-59. http://dx.doi.org/10.1264/jsme2.ME13110.
31. Guong VT, Rosling A, Alström S, Chai B, Högberg N. 2012. Different crop rotation systems as drivers of change in soil bacterial community structure and yield of rice, Oryza sativa. Biol Fertility Soils 48:217-225. http://dx.doi.org/10.1007/s00374-011-0618-5.
32. Yanni YG, Rizk R, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D. 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. http://dx.doi.org/10.1023/A:1004269902246.
33. Webster G, Gough C, Vasse J, Batchelor C, O'Callaghan K, Kothari S, Davey M, Dénarié J, Cocking E. 1997. Interactions of rhizobia with rice and wheat. Plant Soil 194:115-122. http://dx.doi.org/10.1023/A:1004283819084.
34. Yanni YG, Rizk RY, El-Fattah FKA, Squartini A, Corich V, Giacomini A, de Bruijn F, Rademaker J, Maya-Flores J, Ostrom P. 2001. The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Funct Plant Biol 28:845-870. http://dx.doi.org/10.1071/PP01069.
35. Prévost D, Gauvin-Trudel C, Juge C. 2012. Diversity of Bradyrhizobium populations associated to soybean-maize rotations in Québec, Eastern Canada, and their potential to improve growth of both plant species. Appl Soil Ecol 59:29-38. http://dx.doi.org/10.1016/j.apsoil.2012.03.018.
36. Sasaki K, Ikeda S, Ohkubo T, Kisara C, Sato T, Minamisawa K. 2013. Effects of plant genotype and nitrogen level on bacterial communities in rice shoots and roots. Microbes Environ 28:391-395. http://dx.doi.org/10.1264/jsme2.ME12212.
37. Mornico D, Miché L, Béna G, Nouwen N, Verméglio A, Vallenet D, Smith AA, Giraud E, Médigue C, Moulin L. 2011. Comparative genomics of Aeschynomene symbionts: insights into the ecological lifestyle of nod-independent photosynthetic bradyrhizobia. Genes 3:35-61. http://dx.doi.org/10.3390/genes3010035.
38. Giraud E, Hannibal L, Fardoux J, Verméglio A, Dreyfus B. 2000. Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc Natl Acad Sci U S A 97:14795-14800. http://dx.doi.org/10.1073/pnas.250484097.
39. Cannon SB, Ilut D, Farmer AD, Maki SL, May GD, Singer SR, Doyle JJ. 2010. Polyploidy did not predate the evolution of nodulation in all legumes. PLoS One 5:e11630. http://dx.doi.org/10.1371/journal.pone.0011630.
40. Okubo T, Fukushima S, Minamisawa K. 2012. Evolution of Bradyrhizobium-Aeschynomene mutualism: living testimony of the ancient world or highly evolved state? Plant Cell Physiol 53:2000-2007. http://dx.doi.org/10.1093/pcp/pcs150.
41. Chaintreuil C, Arrighi JF, Giraud E, Miché L, Moulin L, Dreyfus B, Munive-Hernández JA, Villegas-Hernandez MC, Béna G. 2013. Evolution of symbiosis in the legume genus Aeschynomene. New Phytol 200: 1247-1259. http://dx.doi.org/10.1111/nph.12424.
42. Masuda S, Eda S, Sugawara C, Mitsui H, Minamisawa K. 2010. The cbbL gene is required for thiosulfate-dependent autotrophic growth of Bradyrhizobium japonicum. Microbes Environ 25:220-223. http://dx.doi.org/10.1264/jsme2.ME10124.
43. Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D, Chaintreuil C, Prin Y, Nouwen N. 2010. Large-scale transposon mutagenesis of photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant Microbe Interact 23:760-770. http://dx.doi.org/10.1094/MPMI-23-6-0760.
44. Gourion B, Delmotte N, Bonaldi K, Nouwen N, Vorholt JA, Giraud E. 2011. Bacterial RuBisCO is required for efficient Bradyrhizobium/Aeschynomene symbiosis. PLoS One 6:e21900. http://dx.doi.org/10.1371/journal.pone.0021900.
45. Okubo T, Tsukui T, Maita H, Okamoto S, Oshima K, Fujisawa T, Saito A, Futamata H, Hattori R, Shimomura Y. 2012. Complete genome sequence of Bradyrhizobium sp. S23321: insights into symbiosis evolution in soil oligotrophs. Microbes Environ 27:306-315. http://dx.doi.org/10.1264/jsme2.ME11321.
46. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 1991. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697-703.
47. Nzoué A, Miché L, Klonowska A, Laguerre G, de Lajudie P, Moulin L. 2009. Multilocus sequence analysis of bradyrhizobia isolated from Aeschynomene species in Senegal. Syst Appl Microbiol 32:400-412. http://dx.doi.org/10.1016/j.syapm.2009.06.002.
48. Vinuesa P, Silva C, Werner D, Martínez-Romero E. 2005. Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 34:29-54. http://dx.doi.org/10.1016/j.ympev.2004.08.020.
49. Scott HN, Laible PD, Hanson DK. 2003. Sequences of versatile broadhost-range vectors of the RK2 family. Plasmid 50:74-79.
50. Wilson KJ, Sessitsch A, Corbo JC, Giller KE, Akkermans AD, Jefferson RA. 1995. β-Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other Gram-negative bacteria. Microbiology 141: 1691-1705.