Interactions of plant growth-promoting rhizobacteria and soil factors in two leguminous plants

Abstract

Although the rhizomicrobiome has been extensively studied, little is known about the interactions between soil properties and the assemblage of plant growth-promoting microbes in the rhizosphere. Herein, we analysed the composition and structure of rhizomicrobiomes associated with soybean and alfalfa plants growing in different soil types using deep Illumina 16S rRNA sequencing. Soil pH, P and K significantly affected the composition of the soybean rhizomicrobiome, whereas soil pH and N had a significant effect on the alfalfa rhizomicrobiome. Plant biomass was influenced by plant species, the composition of the rhizomicrobiome, soil pH, N, P and plant growth stage. The beta diversity of the rhizomicrobiome was the second most influential factor on plant growth (biomass). Rhizomicrobes associated with plant biomass were identified and divided into four groups: (1) positively associated with soybean biomass; (2) negatively associated with soybean biomass; (3) positively associated with alfalfa biomass; and (4) negatively associated with alfalfa biomass. Genera assemblages among the four groups differentially responded to soil properties; Group 1 and Group 2 were significantly correlated with soil pH and P, whereas Group 3 and Group 4 were significantly correlated with soil N, K and C. The influence of soil properties on the relative abundance of plant biomass-associated rhizomicrobes differed between soybean and alfalfa. The results suggest the rhizomicrobiome has a pronounced influence on plant growth, and the rhizomicrobiome assemblage and plant growth-associated microbes are differentially structured by soil properties and leguminous plant species.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adhikari M, Yadav DR, Kim SW, Um YH, Kim HS, Lee SC, Song JY, Kim HG, Lee YS (2017) Biological control of bacterial fruit blotch of watermelon pathogen (Acidovorax citrulli) with rhizosphere associated bacteria. Plant Pathol J 33(2):170–183. https://doi.org/10.5423/PPJ.OA.09.2016.0187

    PubMed  PubMed Central  Google Scholar 

  2. Ali B, Sabri AN, Hasnain S (2010) Rhizobacterial potential to alter auxin content and growth of Vigna radiata (L.) World J Microb Biot 26(8):1379–1384. https://doi.org/10.1007/s11274-010-0310-1

    CAS  Article  Google Scholar 

  3. Anandham R, Gandhi PI, Madhaiyan M, Sa T (2008) Potential plant growth promoting traits and bioacidulation of rock phosphate by thiosulfate oxidizing bacteria isolated from crop plants. J Basic Microbiol 48(6):439–447. https://doi.org/10.1002/jobm.200700380

    CAS  Article  PubMed  Google Scholar 

  4. Anderson M, Habiger J (2012) Characterization and identification of productivity-associated rhizobacteria in wheat. Appl Environ Microbiol 78(12):4434–4446. https://doi.org/10.1128/AEM.07466-11

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x

    CAS  Article  PubMed  Google Scholar 

  6. Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends Plant Sci 19(2):90–98. https://doi.org/10.1016/j.tplants.2013.11.006

    CAS  Article  PubMed  Google Scholar 

  7. Brodhagen M, Henkels MD, Loper JE (2004) Positive autoregulation and signaling properties of pyoluteorin, an antibiotic produced by the biological control organism Pseudomonas fluorescens Pf-5. Appl Environ Microbiol 70(3):1758–1766. https://doi.org/10.1128/AEM.70.3.1758-1766.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Bano A, Muqarab R (2017) Plant defence induced by PGPR against Spodoptera litura in tomato (Solanum lycopersicum L.) Plant Biol 19(3):406–412. https://doi.org/10.1111/plb.12535

    CAS  Article  PubMed  Google Scholar 

  9. Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18. https://doi.org/10.1007/s00253-009-2092-7

    CAS  Article  PubMed  Google Scholar 

  10. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x

    CAS  Article  PubMed  Google Scholar 

  11. Cakmakçi R, Dönmez F, Aydın A, Şahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38(6):1482–1487. https://doi.org/10.1016/j.soilbio.2005.09.019

    Article  Google Scholar 

  12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8(4):790–803. https://doi.org/10.1038/ismej.2013.196

    CAS  Article  PubMed  Google Scholar 

  14. Chapelle E, Mendes R, Bakker PA, Raaijmakers JM (2016) Fungal invasion of the rhizosphere microbiome. ISME J 10(1):265–268. https://doi.org/10.1038/ismej.2015.82

    CAS  Article  PubMed  Google Scholar 

  15. Cheng J, Zhang MY, Wang WX, Manikprabhu D, Salam N, Zhang TY, Wu YY, Li WJ, Zhang YX (2015) Luteimonas notoginsengisoli sp. nov., isolated from rhizosphere soil. Int J Syst Evol Microbiol 66:946–950. https://doi.org/10.1099/ijsem.0.000816

    Article  PubMed  Google Scholar 

  16. Coats VC, Pelletreau KN, Rumpho ME (2014) Amplicon pyrosequencing reveals the soil microbial diversity associated with invasive Japanese barberry (Berberis thunbergii DC.) Mol Ecol 23(6):1318–1332. https://doi.org/10.1111/mec.12544

    CAS  Article  PubMed  Google Scholar 

  17. Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221(2):297–303. https://doi.org/10.1007/s00425-005-1523-7

    CAS  Article  PubMed  Google Scholar 

  18. Dastager SG, Deepa CK, Pandey A (2010) Isolation and characterization of novel plant growth promoting Micrococcus sp NII-0909 and its interaction with cowpea. Plant Physiol Biochem 48(12):987–992. https://doi.org/10.1016/j.plaphy.2010.09.006

    CAS  Article  PubMed  Google Scholar 

  19. Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal-resistant, potentially plant growth-promoting bacteria. FEMS Microbiol Ecol 52(2):153–162. https://doi.org/10.1016/j.femsec.2004.11.005

    Article  PubMed  Google Scholar 

  20. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72(3):313–327. https://doi.org/10.1111/j.1574-6941.2010.00860.x

    CAS  Article  PubMed  Google Scholar 

  21. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694. https://doi.org/10.1111/j.1365-3040.2009.02028.x

    CAS  Article  PubMed  Google Scholar 

  22. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. https://doi.org/10.1093/bioinformatics/btq461

    CAS  Article  PubMed  Google Scholar 

  23. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Edwards J, Johnson C, Santos-Medellin C, Lurie E, Podishetty NK, Bhatnagar S, Eisen JA, Sundaresan V (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A 112(8):E911–E920. https://doi.org/10.1073/pnas.1414592112

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Fan X, Yu T, Li Z, Zhang XH (2014) Luteimonas abyssi sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 64(Pt 2):668–674. https://doi.org/10.1099/ijs.0.056010-0

    CAS  Article  PubMed  Google Scholar 

  26. Gaiero JR, McCall CA, Thompson KA, Day NJ, Best AS, Dunfield KE (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100(9):1738–1750. https://doi.org/10.3732/ajb.1200572

    Article  PubMed  Google Scholar 

  27. Galleguillos C, Aguirre C, Miguel Barea J, Azcon R (2000) Growth promoting effect of two Sinorhizobium meliloti strains (a wild type and its genetically modified derivative) on a non-legume plant species in specific interaction with two arbuscular mycorrhizal fungi. Plant Sci 159(1):57–63. https://doi.org/10.1016/S0168-9452(00)00321-6

    CAS  Article  PubMed  Google Scholar 

  28. Gamalero E, Glick BR (2015) Bacterial modulation of plant ethylene levels. Plant Physiol 169(1):13–22. https://doi.org/10.1104/pp.15.00284

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Goldstein AH (1995) Recent progress in understanding the molecular genetics and biochemistry of calcium phosphate solubilization by gram negative bacteria. Biol Agric Hortic 12(2):185–193. https://doi.org/10.1080/01448765.1995.9754736

    Article  Google Scholar 

  30. Hahm MS, Sumayo M, Hwang YJ, Jeon SA, Park SJ, Lee JY, Ahn JH, Kim BS, Ryu CM, Ghim SY (2012) Biological control and plant growth promoting capacity of rhizobacteria on pepper under greenhouse and field conditions. J Microbiol 50(3):380–385. https://doi.org/10.1007/s12275-012-1477-y

    Article  PubMed  Google Scholar 

  31. Hariprasad P, Niranjana S (2009) Isolation and characterization of phosphate solubilizing rhizobacteria to improve plant health of tomato. Plant Soil 316(1–2):13–24. https://doi.org/10.1007/s11104-008-9754-6

    CAS  Article  Google Scholar 

  32. Huang X, Liu L, Wen T, Zhang J, Wang F, Cai Z (2016) Changes in the soil microbial community after reductive soil disinfestation and cucumber seedling cultivation. Appl Microbiol Biotechnol 100(12):5581–5593. https://doi.org/10.1007/s00253-016-7362-6

    CAS  Article  PubMed  Google Scholar 

  33. Hutsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165(4):397–407. https://doi.org/10.1002/1522-2624(200208)165:4<397::AID-JPLN397>3.0.CO;2-C

    CAS  Article  Google Scholar 

  34. Jin ZX, Wang C, Chen W, Chen X, Li X (2007) Induction of oxalate decarboxylase by oxalate in a newly isolated Pandoraea sp. OXJ-11 and its ability to protect against Sclerotinia sclerotiorum infection. Can J Microbiol 53(12):1316–1322. https://doi.org/10.1139/W07-103

    CAS  Article  PubMed  Google Scholar 

  35. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321(1–2):5–33. https://doi.org/10.1007/s11104-009-9925-0

    CAS  Article  Google Scholar 

  36. Joo ES, Cha S, Kim MK, Jheong W, Seo T, Srinivasan S (2015) Flavisolibacter swuensis sp. nov. isolated from soil. J Microbiol 53(7):442–447. https://doi.org/10.1007/s12275-015-5241-y

    CAS  Article  PubMed  Google Scholar 

  37. Kai M, Effmert U, Piechulla B (2016) Bacterial-plant-interactions: approaches to unravel the biological function of bacterial volatiles in the rhizosphere. Front Microbiol 7:108. https://doi.org/10.3389/fmicb.2016.00108

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286(5776):885–886. https://doi.org/10.1038/286885a0

    CAS  Article  Google Scholar 

  39. Lee JJ, Kang MS, Kim GS, Lee CS, Lim S, Lee J, Roh SH, Kang H, Ha JM, Bae S, Jung HY, Kim MK (2016) Flavisolibacter tropicus sp. nov., isolated from tropical soil. Int J Syst Evol Microbiol 66(9):3413–3419. https://doi.org/10.1099/ijsem.0.001207

    Article  PubMed  Google Scholar 

  40. Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37(7):1325–1334. https://doi.org/10.1007/s10529-015-1814-4

    Article  PubMed  Google Scholar 

  41. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918

    CAS  Article  PubMed  Google Scholar 

  42. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Lunt HA, Swanson CLW, Jacobson HGM (1950) The Morgan soil testing system. Bulletin 541. Connecticut Agricultural Experiment Station, New Haven

    Google Scholar 

  44. Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963. https://doi.org/10.1093/bioinformatics/btr507

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8(8):1577–1587. https://doi.org/10.1038/ismej.2014.17

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Nagpal S, Haque MM, Mande SS (2016) Vikodak-A modular framework for inferring functional potential of microbial communities from 16S metagenomic datasets. PLoS One 11(2):e0148347

    Article  PubMed  PubMed Central  Google Scholar 

  47. Navarrete AA, Tsai SM, Mendes LW, Faust K, de Hollander M, Cassman NA, Raes J, van Veen JA, Kuramae EE (2015) Soil microbiome responses to the short-term effects of Amazonian deforestation. Mol Ecol 24(10):2433–2448. https://doi.org/10.1111/mec.13172

    CAS  Article  PubMed  Google Scholar 

  48. Nuccio EE, Anderson-Furgeson J, Estera KY, Pett-Ridge J, De Valpine P, Brodie EL, Firestone MK (2016) Climate and edaphic controllers influence rhizosphere community assembly for a wild annual grass. Ecology 97(5):1307–1318. https://doi.org/10.1890/15-0882.1

    Article  PubMed  Google Scholar 

  49. Ofek M, Hadar Y, Minz D (2012) Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS One 7(7):e40117. https://doi.org/10.1371/journal.pone.0040117

  50. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests M (2007) The vegan package. Community ecology package. http://r-forge.r-project.org/projects/vegan/. Accessed 5 September 2007

  51. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290. https://doi.org/10.1093/bioinformatics/btg412

    CAS  Article  PubMed  Google Scholar 

  52. Paungfoo-Lonhienne C, Lonhienne TG, Yeoh YK, Webb RI, Lakshmanan P, Chan CX, Lim PE, Ragan MA, Schmidt S, Hugenholtz P (2014) A new species of Burkholderia isolated from sugarcane roots promotes plant growth. Microb Biotechnol 7(2):142–154. https://doi.org/10.1111/1751-7915.12105

    CAS  Article  PubMed  Google Scholar 

  53. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110(16):6548–6553. https://doi.org/10.1073/pnas.1302837110

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Picard C, Di Cello F, Ventura M, Fani R, Guckert A (2000) Frequency and biodiversity of 2, 4-diacetylphloroglucinol-producing bacteria isolated from the maize rhizosphere at different stages of plant growth. Appl Environ Microbiol 66(3):948–955. https://doi.org/10.1128/AEM.66.3.948-955.2000

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Piccoli P, Bottini R (2013) Terpene production by bacteria and its involvement in plant growth promotion, stress alleviation, and yield increase. In: de Bruijn FJ (ed) Molecular Microbial Ecology of the Rhizosphere, vol 1 & 2. Wiley, Hoboken, pp 335–343

    Google Scholar 

  56. Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016) The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Physiol Biochem 99:39–48. https://doi.org/10.1016/j.plaphy.2015.12.002

    CAS  Article  PubMed  Google Scholar 

  57. Poupin MJ, Timmermann T, Vega A, Zuniga A, Gonzalez B (2013) Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PLoS One 8(7):e69435. https://doi.org/10.1371/journal.pone.0069435

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Reeder J, Knight R (2010) Rapid denoising of pyrosequencing amplicon data: exploiting the rank-abundance distribution. Nat Methods 7(9):668–669. https://doi.org/10.1038/nmeth0910-668b

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Schreiter S, Ding GC, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K (2014) Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front Microbiol 5:144. https://doi.org/10.3389/fmicb.2014.00144

    Article  PubMed  PubMed Central  Google Scholar 

  60. Schulz B, Boyle C, Draeger S, Römmert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106(9):996–1004. https://doi.org/10.1017/s0953756202006342

    CAS  Article  Google Scholar 

  61. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  62. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Sorty AM, Meena KK, Choudhary K, Bitla UM, Minhas PS, Krishnani KK (2016) Effect of plant growth promoting bacteria associated with halophytic weed (Psoralea corylifolia L) on germination and seedling growth of wheat under saline conditions. Appl Biochem Biotechnol 180(5):872–882. https://doi.org/10.1007/s12010-016-2139-z

    CAS  Article  PubMed  Google Scholar 

  64. Staff PO (2015) Correction: Rhizodeposition of nitrogen and carbon by mungbean (Vigna radiata L.) and its contribution to intercropped oats (Avena nuda L.) PLoS One 10(5):e0128503. https://doi.org/10.1371/journal.pone.0128503

    Article  Google Scholar 

  65. Sun HM, Zhang T, Yu LY, Sen K, Zhang YQ (2015) Ubiquity, diversity and physiological characteristics of geodermatophilaceae in Shapotou National Desert Ecological Reserve. Front Microbiol 6:1059. https://doi.org/10.3389/fmicb.2015.01059

    PubMed  PubMed Central  Google Scholar 

  66. Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5(1):51–58. https://doi.org/10.1080/17429140903125848

    CAS  Article  Google Scholar 

  67. Tian F, Wang Y, Zhu X, Chen L, Duan Y (2014) Effect of Sinorhizobium fredii strain Sneb183 on the biological control of soybean cyst nematode in soybean. J Basic Microbiol 54(11):1258–1263. https://doi.org/10.1002/jobm.201301014

    Article  PubMed  Google Scholar 

  68. Trda L, Fernandez O, Boutrot F, Heloir MC, Kelloniemi J, Daire X, Adrian M, Clement C, Zipfel C, Dorey S, Poinssot B (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201(4):1371–1384. https://doi.org/10.1111/nph.12592

    CAS  Article  PubMed  Google Scholar 

  69. Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moenne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dye F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. https://doi.org/10.3389/fpls.2013.00356

    Article  PubMed  PubMed Central  Google Scholar 

  70. Velazquez-Becerra C, Macias-Rodriguez LI, Lopez-Bucio J, Flores-Cortez I, Santoyo G, Hernandez-Soberano C, Valencia-Cantero E (2013) The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro. Protoplasma 250(6):1251–1262. https://doi.org/10.1007/s00709-013-0506-y

    CAS  Article  PubMed  Google Scholar 

  71. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255(2):571–586. https://doi.org/10.1023/A:1026037216893

    CAS  Article  Google Scholar 

  72. Xiao X, Chen W, Zong L, Yang J, Jiao S, Lin Y, Wang E, Wei G (2017) Two cultivated legume plants reveal the enrichment process of the microbiome in the rhizocompartments. Mol Ecol 26(6):1641–1651. https://doi.org/10.1111/mec.14027

    CAS  Article  PubMed  Google Scholar 

  73. Yang SJ, Zhang XH, Cao ZY, Zhao KP, Wang S, Chen MX, XF H (2014) Growth-promoting Sphingomonas paucimobilis ZJSH1 associated with Dendrobium officinale through phytohormone production and nitrogen fixation. Microb Biotechnol 7(6):611–620. https://doi.org/10.1111/1751-7915.12148

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. Yoon MH, Im WT (2007) Flavisolibacter ginsengiterrae gen. nov., sp. nov. and Flavisolibacter ginsengisoli sp. nov., isolated from ginseng cultivating soil. Int J Syst Evol Microbiol 57(Pt 8):1834–1839. https://doi.org/10.1099/ijs.0.65011-0

    CAS  Article  PubMed  Google Scholar 

  75. Zhang H, Kim M-S, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu C-M, Allen R, Melo IS (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226(4):839–851. https://doi.org/10.1007/s00425-007-0530-2

    CAS  Article  PubMed  Google Scholar 

  76. Zhang YQ, Chen J, Liu HY, Zhang YQ, Li WJ, LY Y (2011) Geodermatophilus ruber sp. nov., isolated from rhizosphere soil of a medicinal plant. Int J Syst Evol Microbiol 61(Pt 1):190–193. https://doi.org/10.1099/ijs.0.020610-0

    CAS  Article  PubMed  Google Scholar 

  77. Zhao K, Penttinen P, Zhang X, Ao X, Liu M, Yu X, Chen Q (2014) Maize rhizosphere in Sichuan, China, hosts plant growth promoting Burkholderia cepacia with phosphate solubilizing and antifungal abilities. Microbiol Res 169(1):76–82. https://doi.org/10.1016/j.micres.2013.07.003

    CAS  Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by National Key Research and Development Program (2016YFD0200308) and National Natural Science Foundation of China (41671261, 31370142).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Weimin Chen or Gehong Wei.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

ESM 1

(PDF 818 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xiao, X., Fan, M., Wang, E. et al. Interactions of plant growth-promoting rhizobacteria and soil factors in two leguminous plants. Appl Microbiol Biotechnol 101, 8485–8497 (2017). https://doi.org/10.1007/s00253-017-8550-8

Download citation

Keywords

  • Plant growth-promoting rhizobacteria
  • Illumina sequencing
  • Plant-microbial interactions
  • Rhizosphere
  • Leguminous plants