Diversity and plant growth-promoting functions of diazotrophic/N-scavenging bacteria isolated from the soils and rhizospheres of two species of Solanum
Autoři:
Mónica Yorlady Alzate Zuluaga aff001; Karina Maria Lima Milani aff001; Leandro Simões Azeredo Gonçalves aff002; André Luiz Martinez de Oliveira aff001
Působiště autorů:
Departamento de Bioquímica e Biotecnologia, Universidade Estadual de Londrina, Londrina, Paraná, Brazil
aff001; Departamento de Agronomia, Universidade Estadual de Londrina, Londrina, Paraná, Brazil
aff002
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227422
Souhrn
Studies of the interactions between plants and their microbiome have been conducted worldwide in the search for growth-promoting representative strains for use as biological inputs for agriculture, aiming to achieve more sustainable agriculture practices. With a focus on the isolation of plant growth-promoting (PGP) bacteria with ability to alleviate N stress, representative strains that were found at population densities greater than 104 cells g-1 and that could grow in N-free semisolid media were isolated from soils under different management conditions and from the roots of tomato (Solanum lycopersicum) and lulo (Solanum quitoense) plants that were grown in those soils. A total of 101 bacterial strains were obtained, after which they were phylogenetically categorized and characterized for their basic PGP mechanisms. All strains belonged to the Proteobacteria phylum in the classes Alphaproteobacteria (61% of isolates), Betaproteobacteria (19% of isolates) and Gammaproteobacteria (20% of isolates), with distribution encompassing nine genera, with the predominant genus being Rhizobium (58.4% of isolates). Strains isolated from conventional horticulture (CH) soil composed three bacterial genera, suggesting a lower diversity for the diazotrophs/N scavenger bacterial community than that observed for soils under organic management (ORG) or secondary forest coverture (SF). Conversely, diazotrophs/N scavenger strains from tomato plants grown in CH soil comprised a higher number of bacterial genera than did strains isolated from tomato plants grown in ORG or SF soils. Furthermore, strains isolated from tomato were phylogenetically more diverse than those from lulo. BOX-PCR fingerprinting of all strains revealed a high genetic diversity for several clonal representatives (four Rhizobium species and one Pseudomonas species). Considering the potential PGP mechanisms, 49 strains (48.5% of the total) produced IAA (2.96–193.97 μg IAA mg protein-1), 72 strains (71.3%) solubilized FePO4 (0.40–56.00 mg l-1), 44 strains (43.5%) solubilized AlPO4 (0.62–17.05 mg l-1), and 44 strains produced siderophores (1.06–3.23). Further, 91 isolates (90.1% of total) showed at least one PGP trait, and 68 isolates (67.3%) showed multiple PGP traits. Greenhouse trials using the bacterial collection to inoculate tomato or lulo plants revealed increases in plant biomass (roots, shoots or both plant tissues) elicited by 65 strains (54.5% of the bacterial collection), of which 36 were obtained from the tomato rhizosphere, 15 were obtained from the lulo rhizosphere, and 14 originated from samples of soil that lacked plants. In addition, 18 strains showed positive inoculation effects on both Solanum species, of which 12 were classified as Rhizobium spp. by partial 16S rRNA gene sequencing. Overall, the strategy adopted allowed us to identify the variability in the composition of culturable diazotroph/N-scavenger representatives from soils under different management conditions by using two Solanum species as trap plants. The present results suggest the ability of tomato and lulo plants to enrich their belowground microbiomes with rhizobia representatives and the potential of selected rhizobial strains to promote the growth of Solanum crops under limiting N supply.
Klíčová slova:
Phylogenetics – Pseudomonas – Tomatoes – Solanum – Agricultural soil science – Diazo compounds – Burkholderia – Rhizobium
Zdroje
1. Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact. 2014;13. doi: 10.1186/1475-2859-13-13
2. Pieterse CMJ, de Jonge R, Berendsen RL. The soil-borne supremacy. Trends Plant Sci. 2016;21: 171–173. doi: 10.1016/j.tplants.2016.01.018 26853594
3. Armada E, Leite MFA, Medina A, Azcón R, Kuramae EE. Native bacteria promote plant growth under drought stress condition without impacting the rhizomicrobiome. FEMS Microbiol Ecol. 2018;94: 1–13. doi: 10.1093/femsec/fiy092 29771325
4. Ji SH, Kim JS, Lee CH, Seo HS, Chun SC, Oh J, et al. Enhancement of vitality and activity of a plant growth-promoting bacteria (PGPB) by atmospheric pressure non-thermal plasma. Sci Rep. 2019;9: 1–16. doi: 10.1038/s41598-018-37186-2
5. Baez-Rogelio A, Morales-García YE, Quintero-Hernández V, Muñoz-Rojas J. Next generation of microbial inoculants for agriculture and bioremediation. Microb Biotechnol. 2017;10: 19–21. doi: 10.1111/1751-7915.12448 27790851
6. Ogata-Gutiérrez K, Chumpitaz-Segovia C, Lirio-Paredes J, Finetti-Sialer MM, Zúñiga-Dávila D. Characterization and potential of plant growth promoting rhizobacteria isolated from native Andean crops. World J Microbiol Biotechnol. 2017;33: 1–13. doi: 10.1007/s11274-016-2144-y
7. Hinsinger P, Bengough AG, Vetterlein D, Young IM. Rhizosphere: Biophysics, biogeochemistry and ecological relevance. Plant Soil. 2009;321: 117–152. doi: 10.1007/s11104-008-9885-9
8. Bashan Y, de-Bashan LE, Prabhu SR, Hernandez JP. Advances in plant growth-promoting bacterial inoculant technology: Formulations and practical perspectives (1998–2013). Plant Soil. 2014;378: 1–33. doi: 10.1007/s11104-013-1956-x
9. de Souza R, Ambrosini A, Passaglia LMP. Plant growth-promoting bacteria as inoculants in agricultural soils. Genetics and Molecular Biology. 2015. doi: 10.1590/S1415-475738420150053 26537605
10. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A. The importance of the microbiome of the plant holobiont. New Phytol. 2015;206: 1196–1206. doi: 10.1111/nph.13312 25655016
11. White L, Ge X, Brozel V, Subramanian S. Root isoflavonoids and hairy root transformation influence key bacterial taxa in the soybean rhizosphere. Environ Microbiol. 2017;19: 1391–1406. doi: 10.1111/1462-2920.13602 27871141
12. Musilova L, Ridl J, Polivkova M, Macek T, Uhlik O. Effects of secondary plant metabolites on microbial populations: Changes in community structure and metabolic activity in contaminated environments. Int J Mol Sci. 2016;17. doi: 10.3390/ijms17081205 27483244
13. Lareen A, Burton F, Schäfer P. Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol. 2016;90: 575–587. doi: 10.1007/s11103-015-0417-8 26729479
14. Singh BK, Dawson LA, Macdonald CA, Buckland SM. Impact of biotic and abiotic interaction on soil microbial communities and functions: A field study. Appl Soil Ecol. 2009;41: 239–248. doi: 10.1016/j.apsoil.2008.10.003
15. Agler MT, Ruhe J, Kroll S, Morhenn C, Kim S, Weigel D, et al. Microbial hub taxa link host and abiotic factors to pant microbiome variation. PLoS Biol. 2016;14: 1–31. doi: 10.1371/journal.pbio.1002352 26788878
16. Santoyo G, Hernández-pacheco C, Hernández-salmerón J, Hernández-león R. The role of abiotic factors modulating the plant-microbe-soil interactions: Toward sustainable agriculture. A review. Spanish J Agric Res. 2017;15: 1–15. doi: 10.5424/sjar/2017151-9990
17. De-la-peña C, Loyola-vargas VM. Biotic interactions in the rhizosphere: A diverse cooperative enterprise for plant productivity. Plant Physiol. 2014;166: 701–719. doi: 10.1104/pp.114.241810 25118253
18. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science. 2011;332: 1097–1100. doi: 10.1126/science.1203980 21551032
19. Sanchez-Canizares C, Jorrı B, Poole PS, Tkacz A. Understanding the holobiont: The interdependence of plants and their microbiome. Curr Opin Microbiol. 2017;38: 188–196. doi: 10.1016/j.mib.2017.07.001 28732267
20. Yang Y, Wang N, Guo X, Zhang Y, Ye B. Comparative analysis of bacterial community structure in the rhizosphere of maize by highthroughput pyrosequencing. PLoS One. 2017;12: 1–11. doi: 10.1371/journal.pone.0178425 28542542
21. Ahmad F, Ahmad I, Khan MS. Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res. 2008;163: 173–181. doi: 10.1016/j.micres.2006.04.001 16735107
22. Compant S, Samad A, Faist H, Sessitsch A. A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J Adv Res. 2019;19: 29–37. doi: 10.1016/j.jare.2019.03.004 31341667
23. Olanrewaju OS, Glick BR, Babalola OO. Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol. Springer Netherlands; 2017;33: 0. doi: 10.1007/s11274-017-2364-9 28986676
24. Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda M del C, Glick BR. Plant growth-promoting bacterial endophytes. Microbiol Res. Elsevier GmbH.; 2016;183: 92–99. doi: 10.1016/j.micres.2015.11.008 26805622
25. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol. 2013;64: 807–38. doi: 10.1146/annurev-arplant-050312-120106 23373698
26. Koskey G, Mburu SW, Njeru EM, Kimiti JM, Ombori O, Maingi JM. Potential of native rhizobia in enhancing nitrogen fixation and yields of climbing beans (Phaseolus vulgaris L.) in contrasting environments of eastern Kenya. Front Plant Sci. 2017;8: 1–12. doi: 10.3389/fpls.2017.00001
27. Baldani JI, Reis VM, Videira SS, Boddey LH, Baldani VLD. The art of isolating nitrogen-fixing bacteria from non-leguminous plants using N-free semi-solid media: a practical guide for microbiologists. Plant Soil. 2014;384: 413–431. doi: 10.1007/s11104-014-2186-6
28. Cheng HR, Jiang N. Extremely rapid extraction of DNA from bacteria and yeasts. Biotechnol Lett. 2006;28: 55–59. doi: 10.1007/s10529-005-4688-z 16369876
29. Koskey G, Mburu SW, Kimiti JM, Ombori O, Maingi JM, Njeru EM. Genetic characterization and diversity of Rhizobium isolated from root nodules of mid-altitude climbing bean (Phaseolus vulgaris L.) varieties. Front Microbiol. 2018;9: 1–12. doi: 10.3389/fmicb.2018.00001
30. Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN, Martinez-Romero E. Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants Pa. 2006;29: 315–332. doi: 10.1016/j.syapm.2005.12.002
31. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73: 5261–5267. doi: 10.1128/AEM.00062-07 17586664
32. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33: 1870–1874. doi: 10.1093/molbev/msw054 27004904
33. Versalovic J, Schneider M, Bruijn FJD, Lupski JR. Microbial DNA typing by automated repetitive sequence-based PCR. Methods in Molecular and Celluar Biology. 1994. pp. 25–40.
34. Rademaker JL., Bruijn F. Characterization and classification of microbes by Rep-PCR genomic fingerprinting and computer assisted pattern analysis. In: Caetano-Anólles G, Gresshoff P., editors. DNA markers: protocols, applications and overviews. Hoboken: John Wiley & Sons; 1997. pp. 151–171.
35. Mohammed M, Jaiswal SK, Dakora FD. Distribution and correlation between phylogeny and functional traits of cowpea (Vigna unguiculata L. Walp.)-nodulating microsymbionts from Ghana and South Africa. Sci Rep. 2018;8: 1–19. doi: 10.1038/s41598-017-17765-5
36. Agnol RFD, Bournaud C, Faria SM, Béna G, Moulin L, Hungria M. Genetic diversity of symbiotic Paraburkholderia species isolated from nodules of Mimosa pudica (L.) and Phaseolus vulgaris (L.) grown in soils of the Brazilian Atlantic Forest (Mata Atlântica). FEMS Microbiol Ecol. 2017;93: 1–15. doi: 10.1093/femsec/fix027 28334155
37. Sarwar M, Kremer RJ. Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol. 1995;20: 282–285. doi: 10.1111/j.1472-765X.1995.tb00446.x
38. Bradford MM. A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;254: 248–254.
39. Mehta S, Nautiyal CS. An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol. 2001;43: 51–56. doi: 10.1007/s002840010259 11375664
40. Murphy J, Riley JP. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta. 1962;27: 31–36. doi: 10.1016/S0003-2670(00)88444-5
41. Schwyn B, Neilands JB. Universal assay for the detection and determination of siderophores. Anal Biochem. 1987;160: 47–56. doi: 10.1016/0003-2697(87)90612-9 2952030
42. Payne SM. Detection, isolation, and characterization of siderophores. Methods Enzymol. 1994;235: 329–344. doi: 10.1016/0076-6879(94)35151-1 8057905
43. Dutta J, Thakur D. Evaluation of multifarious plant growth promoting traits, antagonistic potential and phylogenetic affiliation of rhizobacteria associated with commercial tea plants grown in Darjeeling, India. PLoS One. 2017;12: 1–24. doi: 10.1371/journal.pone.0182302 28771547
44. Heimpel GE, Yang Y, Hill JD, Ragsdale DW. Environmental consequences of invasive species: Greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. plo. 2013;8: 1–7. doi: 10.1371/journal.pone.0072293 23977273
45. Kumar A, Singh J, Singh V, Srivastava R. Biocatalysis and agricultural biotechnology recent advances of PGPR based approaches for stress tolerance in plants for sustainable agriculture. Biocatal Agric Biotechnol. 2019;20: 1–10. doi: 10.1016/j.bcab.2019.101271
46. Billah M, Khan M, Bano A, Hassan TU, Munir A, Gurmani AR. Phosphorus and phosphate solubilizing bacteria: Keys for sustainable agriculture. Geomicrobiol J. 2019;36: 904–916. doi: 10.1080/01490451.2019.1654043
47. Hurek T, Reinhold-hurek B, Grimm B, Fendrik I, Niemann E-G. Occurrence of effective nitrogen-scavenging bacteria in the rhizosphere of kallar grass. Plant Soil. 1988;110: 339–348.
48. Kruasuwan W, Thamchaipenet A. Diversity of culturable plant growth-promoting bacterial endophytes associated with sugarcane roots and their effect of growth by co-inoculation of diazotrophs and actinomycetes. J Plant Growth Regul. 2016;35: 1074–1087. doi: 10.1007/s00344-016-9604-3
49. Wright SF, Weaver RW. Enumeration and identification of nitrogen-fixing bacteria from forage grass roots. Appl an Environ Microbiol. 1981;42: 97–101.
50. Goes KCGP, Fisher ML de C, Cattelan AJ, Nogueira MA, Carvalho CGP, Oliveira ALM. Biochemical and molecular characterization of high population density bacteria isolated from sunflower. J Microbiol Biotechnol. 2012;22: 437–447. doi: 10.4014/jmb.1109.09007 22534289
51. Videira SS, de Oliveira DM, de Morais RF, Borges WL, Baldani VLD, Baldani JI. Genetic diversity and plant growth promoting traits of diazotrophic bacteria isolated from two Pennisetum purpureum Schum. genotypes grown in the field. Plant Soil. 2012;356: 51–66. doi: 10.1007/s11104-011-1082-6
52. Stefani FOP, Bell TH, Marchand C, De La Providencia IE, El Yassimi A, St-Arnaud M, et al. Culture-dependent and -independent methods capture different microbial community fractions in hydrocarbon-contaminated soils. PLoS One. 2015;10: 1–16. doi: 10.1371/journal.pone.0128272 26053848
53. Lee SA, Park J, Chu B, Kim JM, Joa JH, Sang MK, et al. Comparative analysis of bacterial diversity in the rhizosphere of tomato by culture-dependent and -independent approaches. J Microbiol. 2016;54: 823–831. doi: 10.1007/s12275-016-6410-3 27888459
54. Wang S, Liu J, Sun J, Sun Y, Liu J, Jia N. Diversity of culture-independent bacteria and antimicrobial activity of culturable endophytic bacteria isolated from different Dendrobium stems. Sci Rep. 2019;9: 1–12. doi: 10.1038/s41598-018-37186-2
55. Zheng T. Rhizosphere effects on soil microbial community structure and enzyme activity in a successional subtropical forest.
56. Bever JD, Platt TG, Morton ER. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol. 2012;66: 265–283. doi: 10.1146/annurev-micro-092611-150107 22726216
57. Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizosphere microbiome and plant health. Trends Plant Sci. 2012;17: 478–486. doi: 10.1016/j.tplants.2012.04.001 22564542
58. Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL. Plant community richness and microbial interactions structure bacterial communities in soil. Ecology. 2015;96: 134–142. doi: 10.1890/13-1648.1 26236898
59. Nicolitch O, Colin Y, Turpault M, Uroz S. Soil type determines the distribution of nutrient mobilizing bacterial communities in the rhizosphere of beech trees. Soil Biol Biochem. 2016;103: 429–445. doi: 10.1016/j.soilbio.2016.09.018
60. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbiots. Nat Rev Microbiol. 2018;16: 291–303. doi: 10.1038/nrmicro.2017.171 29379215
61. Broughton WJ. Control of specificity in legume-Rhizobium associations. J Appl Bacteriol. 1978;45: 165–194.
62. Denison RF, Kiers ET. Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett. 2004;237: 187–193. doi: 10.1016/j.femsle.2004.07.013 15321661
63. Keller KR, Lau JA. When mutualisms matter: rhizobia effects on plant communities depend on host plant population and soil nitrogen availability. J Ecol. 2018;106: 1046–1056. doi: 10.1111/ijlh.12426
64. Burghardt L., Epstein B, Tiffin P. Legacy of prior host and soil selection on rhizobial fitness in planta. Evolution. 2019;73: 2013–2023. doi: 10.1111/evo.13807 31334838
65. Berge O, Lodhi A, Santaella C, Roncato M, Christen R, Heulin T, et al. Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol. 2009;59: 367–372. doi: 10.1099/ijs.0.000521-0 19196780
66. Singh RK, Mishra RPN, Jaiswal HK. Role of rhizobial endophytes as nitrogen fixer in promoting plant growth and productivity of Indian cultivated upland. In: Wang Y-P, Lin M, Tian Z-X, Elmerich C, Newton WE, editors. Biological nitrogen fixation, sustainable agriculture and the environment. Springer Netherlands; 2005. pp. 289–291.
67. Mehboob I, Naveed M, Zahir ZA. Rhizobial association with non-legumes: mechanisms and applications. CRC Crit Rev Plant Sci. 2009;28: 432–456. doi: 10.1080/07352680903187753
68. Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, et al. Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil. 1997;194: 99–114. doi: 10.1023/a:1004269902246
69. Antoun H, Beauchamp CJ, Goussard N, Chabot R, Lalande R, Plant S, et al. Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on non-legumes: effect on radishes (Raphanus sativus L.). Plant Soil. 1998;204: 57–67. doi: 10.1023/A:1004326910584
70. Chabot R, Antoun H, Cescas MP. Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar. phaseoli. Plant Soil. 1996;39: 311–321. doi: 10.1128/JB.184.15.4071
71. Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF. Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol. 1996;42: 279–283. doi: 10.1139/m96-040 8868235
72. Kim JS, Dungan RS, Kwon SW, Weon HY. The community composition of root-associated bacteria of the tomato plant. World J Microbiol Biotechnol. 2006;22: 1267–1273. doi: 10.1007/s11274-006-9171-z
73. Poudel R, Jumpponen A, Kennelly MM, Rivard CL, Gomez-Montano L, Garrett KA. Rootstocks shape the rhizobiome: rhizosphere and endosphere bacterial communities in the grafted tomato system. Appl Environ Microbiol. 2019;85. doi: 10.1128/AEM.01765-18 30413478
74. Romero FM, Marina M, Pieckenstain FL. The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Microbiol Lett. 2014;351: 187–194. doi: 10.1111/1574-6968.12377 24417185
75. Ottesen AR, González Peña A, White JR, Pettengill JB, Li C, Allard S, et al. Baseline survey of the anatomical microbial ecology of an important food plant: Solanum lycopersicum (tomato). BMC Microbiol. 2013;13: 114. doi: 10.1186/1471-2180-13-114 23705801
76. Tian B, Zhang C, Ye Y, Wen J, Wu Y, Wang H, et al. Beneficial traits of bacterial endophytes belonging to the core communities of the tomato root microbiome. Agric Ecosyst Environ. 2017;247: 149–156. doi: 10.1016/j.agee.2017.06.041
77. Caballero-Mellado J, Onofre-Lemus J, Estrada-De Los Santos P, Martinez-Aguilar L. The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol. 2007;73: 5308–5319. doi: 10.1128/AEM.00324-07 17601817
78. Miranda-sánchez F, Rivera J, Vinuesa P. Diversity patterns of Rhizobiaceae communities inhabiting soils, root surfaces and nodules reveal a strong selection of rhizobial partners by legumes. 2016;18: 2375–2391. doi: 10.1111/1462-2920.13061
79. Stepkowski T, Banasiewicz J, Granada CE, Andrews M, Passaglia LMP. Phylogeny and phylogeography of rhizobial symbionts nodulating legumes of the tribe Genisteae. Genes (Basel). 2018;9: 1–25. doi: 10.3390/genes9030163 29538303
80. Smyth EM, Mccarthy J, Nevin R, Khan MR, Dow JM, Gara FO, et al. In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol. 2011;111: 683–692. doi: 10.1111/j.1365-2672.2011.05079.x 21672102
81. Valenzuela-aragon B, Parra-cota FI, Santoyo G, Arellano-wattenbarger GL, Santos-villalobos SDL. Plant-assisted selection: a promising alternative for in vivo identification of wheat (Triticum turgidum L. subsp. Durum) growth promoting bacteria. Plant Soil. 2019;435: 367–384.
82. Zahir HNAZA, Khaliq MAA. Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils. 2002;35: 231–237. doi: 10.1007/s00374-002-0462-8
83. Ait-kaki A, Kacem-chaouche N. In vitro and in vivo characterization of plant growth promoting Bacillus strains isolated from extreme environments of eastern Algeria. Appl Biochem Biotechnol. 2014;172: 1735–1746. doi: 10.1007/s12010-013-0617-0 24258791
84. Passari AK, Mishra VK, Gupta VK, Yadav MK, Saikia R, Singh BP. In vitro and in vivo plant growth promoting activities and DNA fingerprinting of antagonistic endophytic actinomycetes associates with medicinal plants. PLoS One. 2015;10: 1–18. doi: 10.1371/journal.pone.0139468 26422789
85. Sukumar P, Legué V, Vayssières A, Martin F, Tuskan GA, Kalluri UC. Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ. 2013;36: 909–919. doi: 10.1111/pce.12036 23145472
86. Casanova-sáez R, Voß U. Auxin metabolism controls developmental decisions in land plants. Trends Plant Sci. 2019;24: 741–754. doi: 10.1016/j.tplants.2019.05.006 31230894
87. Ambreetha S, Chinnadurai C, Marimuthu P, Balachandar D. Plant-associated Bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture. Rhizosphere. 2018;5: 57–66. doi: 10.1016/j.rhisph.2017.12.001
88. Shen J, Lixing Y, Junling Zhang. Haigang L, Zhaohai B, Xinping Chen. Weifeng Z, Fusuo Z. Phosphorus dynamics: from soil to plant. Plant Physiol. 2011;156: 997–1005. doi: 10.1104/pp.111.175232 21571668
89. Richardson AE, Simpson RJ. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 2011;156: 989–996. doi: 10.1104/pp.111.175448 21606316
90. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus. 2013;2: 587. doi: 10.1186/2193-1801-2-587 25674415
91. Neilands JB. Siderophores: Structure and function of microbial iron transport compounds. J Biol Chem. 1995;270: 26723–26726. doi: 10.1074/jbc.270.45.26723 7592901
92. Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P. Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res. 2016;23: 3984–3999. doi: 10.1007/s11356-015-4294-0 25758420
93. Kumar P, Thakur S, Dhingra GK, Singh A, Pal MK, Harshvardhan K, et al. Inoculation of siderophore producing rhizobacteria and their consortium for growth enhancement of wheat plant. Biocatal Agric Biotechnol. 2018;15: 264–269. doi: 10.1016/j.bcab.2018.06.019
94. Illmer P, Barbato A, Schinner F. Solubilization of hardly-soluble AlPO4 with P-solubilizing microorganisms. Soil Biol Biochem. 1995;27: 265–270.
95. Cai H, Bai Y, Guo C. Comparative genomics of 151 plant-associated bacteria reveal putative mechanisms underlying specific interactions between bacteria and plant hosts. Genes Genomics. The Genetics Society of Korea; 2018;40: 864. doi: 10.1007/s13258-018-0693-1 30047115
96. Naveed M, Mitter B, Yousaf S. The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils. 2014;50: 249–262. doi: 10.1007/s00374-013-0854-y
97. Drogue B, Sanguin H, Chamam A, Mozar M, Llauro C, Panaud O, et al. Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front Plant Sci. 2014;5: 1–14. doi: 10.3389/fpls.2014.00607 25414716
98. Mulas D, Díaz-Alcántara C, Mulas R, Marcano I, Barquero M, Serrano P, et al. Inoculants based in autochthonous microorganisms, a strategy to optimize agronomic performance of biofertilizers. In: Rodelas-González M, Gonzalez-Lopez J, editors. Beneficial Plant-microbial interactions: ecology and applications. Boca Raton: CRC Press; 2013. pp. 300–328. doi: 10.1201/b15251-14
99. Symanczik S, Gisler M, Thonar C, Schlaeppi K, Van der Heijden M, Kahmen A, et al. Application of mycorrhiza and soil from a permaculture system improved phosphorus acquisition in naranjilla. Front Plant Sci. 2017;8: 1–12. doi: 10.3389/fpls.2017.00001
100. Gonzalez O, Osorio W. Determination of mycorrhizal dependency of lulo. Acta Biol Colomb. 2008;13: 163–173.
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