Advertisement

Effects of commercial microbial biostimulants on soil and root microbial communities and sugarcane yield

  • Shelby BergEmail author
  • Paul G. Dennis
  • Chanyarat Paungfoo-Lonhienne
  • Jay Anderson
  • Nicole Robinson
  • Richard Brackin
  • Adam Royle
  • Lawrence DiBella
  • Susanne Schmidt
Original Paper
  • 111 Downloads

Abstract

Ameliorating biological attributes of agricultural soils is desirable, and one avenue is introducing beneficial microbes via commercial biostimulant products. Although gaining popularity with farmers, scientific evaluation of such products in field-grown crops is often lacking. We tested two microbial products, Soil-Life™ and Nutri-Life Platform®, in a commercial sugarcane crop by profiling bacterial and fungal communities in soil and roots using high throughput phylogenetic marker gene sequencing. The products, one predominantly consisting of Lactobacillus and the other of Trichoderma, were applied as a mixture as per manufacturers’ instructions. Additives included in the formulations were not listed, and plots that did not receive the product mixture were the controls. The compositions of bacterial communities of soil and sugarcane roots, sampled 2, 5 and 25 weeks after application, were unaffected by the products. Soil fungal communities were also unaffected, but sugarcane roots had a greater relative abundance of three unidentified taxa in genera Marasmius, Fusarium and Talaromyces in the treated plots. Sugarcane yield was similar across all treatments that included a 25% lower nitrogen fertiliser rate. Further research must examine if the altered root fungal community is a consistent feature of the tested products, and if it conveys benefits. We conclude that putative biostimulants can be evaluated by analysing the composition of microbial communities. DNA profiling should be complemented by cost-benefit analysis to build a public information base documenting the effects of microbial biostimulants. Such knowledge will assist manufacturers in product development and farmers in making judicious decisions on product selection, to ensure that the anticipated benefits of microbial biostimulants are realised for broad acre cropping.

Keywords

Microbial biostimulants Crop probiotics Beneficial microbes Root microbial communities Soil microbial communities Sugarcane 

Notes

Acknowledgements

We thank Terrain Natural Resource Management for funding this project, as well as Melissa Royle and Minka Ibanez for sample collection. Shelby Berg gratefully acknowledges financial support from Sugar Research Australia (PhD top-up stipend and operating funds) and the Australian Government Research Training Program.

Data availability statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Author contributions

CP-L and SS designed the study in collaboration with AR and LD. AR was responsible for field sampling and CP-L performed the DNA extractions. CP-L and SB performed bioinformatics analyses, PGD and SB performed statistical analyses and all authors contributed to writing the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. ActivFert (2017) Products: soil-life soil activator. ActivFert Natures Balance. https://docs.wixstatic.com/ugd/845181_f3a8f92dbf1b4298ac4cb8d7f621125e.pdf. Accessed 6 November 2017
  2. Alves GC, Videira SS, Urquiaga S, Reis VM (2015) Differential plant growth promotion and nitrogen fixation in two genotypes of maize by several Herbaspirillum inoculants. Plant Soil 387:307–321.  https://doi.org/10.1007/s11104-014-2295-2 CrossRefGoogle Scholar
  3. Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: Statistics Reference Online 1–15. doi:  https://doi.org/10.1002/9781118445112.stat07841
  4. Baldani JI, Pot B, Kirchhof G, Falsen E, Baldani VLD, Olivares FL, Hoste B, Kersters K, Hartmann M, Gillis M, Doberneiger J (1996) Emended description of Herbaspirillum; inclusion of [Pseudomonas] rubrisubalbicans, a mild plant pathogen, as Herbaspirillum rubrisubalbicans comb. nov.; and classification of a group of clinical isolates (EF group 1) as Herbaspirillum species 3. Int J Syst Bacteriol 46:802–810.  https://doi.org/10.1099/00207713-46-3-802 CrossRefPubMedGoogle Scholar
  5. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778.  https://doi.org/10.1093/jxb/eri197 CrossRefPubMedGoogle Scholar
  6. Bashan Y, de Bashan LE, Prabhu SR, Hernandez JP (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998-2013). Plant Soil 378:1–33.  https://doi.org/10.1007/s11104-013-1956-x CrossRefGoogle Scholar
  7. Bashan Y, Kloepper JW, de Bashan LE, Nannipieri P (2016) A need for disclosure of the identity of microorganisms, constituents, and application methods when reporting tests with microbe-based or pesticide-based products. Biol Fertil Soils 52:283–284.  https://doi.org/10.1007/s00374-016-1091-y CrossRefGoogle Scholar
  8. Batista L, Irisarri P, Rebuffo M, Cuitino MJ, Sanjuan J, Mnoza JS (2015) Nodulation competitiveness as a requisite for improved rhizobial inoculants of Trifolium pratense. Biol Fertil Soils 51:11–20.  https://doi.org/10.1007/s00374-014-0946-3 CrossRefGoogle Scholar
  9. Bauoin E, Nazaret S, Mougel C, Ranjard M, Moënne-Loccoz Y (2009) Impact of inoculation with the phytostimulatory PGPR Azospirillum lipoferum CRT1 on the genetic structure of the rhizobacterial community of field-grown maize. Soil Biol Biochem 41:409–413.  https://doi.org/10.1016/j.soilbio.2008.10.015 CrossRefGoogle Scholar
  10. Baveye PC, Baveye J, Gowdy J (2016) Soil “ecosystem” services and natural capital: critical appraisal of research on uncertain ground. Front Environ Sci 4:1–49.  https://doi.org/10.3389/fenvs.2016.00041 CrossRefGoogle Scholar
  11. Bensch K (2016) Mycobank database: fungal database, nomenclature and species bank. International Mycological Association. http://www.mycobank.org/. Accessed 3 July 2018
  12. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18.  https://doi.org/10.1007/s00253-009-2092-7 CrossRefPubMedGoogle Scholar
  13. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350.  https://doi.org/10.1007/s11274-011-0979-9 CrossRefPubMedGoogle Scholar
  14. Boddey RM, Urquiaga S, Alves BJR, Reis V (2003) Endophytic nitrogen fixation in sugarcane: present knowledge and future applications. Plant Soil 252:139–149.  https://doi.org/10.1023/A:1024152126541 CrossRefGoogle Scholar
  15. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11.  https://doi.org/10.1038/ncomms1046 CrossRefGoogle Scholar
  16. Bothe H, Schmitz O, Yates MG, Newton WE (2010) Nitrogen fixation and hydrogen metabolism in Cyanobacteria. Microbiol Mol Biol Rev 74:529–551.  https://doi.org/10.1128/MMBR.00033-10 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Brackin R, Schmidt S, Walter D, Bhuiyan S, Buckley S, Anderson J (2017) Soil biological health—what is it and how can we improve it? Proc Aust Soc Sugar Cane Technol 39:141–154Google Scholar
  18. Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ (2014) Interactions in multispecies biofilms: do they actually matter? Trends Microbiol 22:84–91.  https://doi.org/10.1016/j.tim.2013.12.004 CrossRefPubMedGoogle Scholar
  19. Çakmakçi 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 38:1482–1487.  https://doi.org/10.1016/j.soilbio.2005.09.019 CrossRefGoogle Scholar
  20. Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41.  https://doi.org/10.1007/s11104-014-2131-8 CrossRefGoogle Scholar
  21. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Busham FD, Costello EK, Fierer N, Peña 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, Turnbaough PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth0510-335 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chen YX, Zhou T, Penttinen P, Zou L, Wang K, Cui YQ, Heng NN, Xu KW (2015) Symbiotic matching, taxonomic position, and field assessment of symbiotically efficient rhizobia isolated from soybean root nodules in Sichuan, China. Biol Fertil Soils 51:707–718.  https://doi.org/10.1007/s00374-015-1019-y CrossRefGoogle Scholar
  23. Chiarini L, Bevivino A, Dalmastri C, Nacamulli C, Tabacchioni S (1998) Influence of plant development, cultivar and soil type on microbial colonization of maize roots. Appl Soil Ecol 8:11–18.  https://doi.org/10.1016/S0929-1393(97)00071-1 CrossRefGoogle Scholar
  24. Chin-A-Woeng TFC, Lugtenberg BJJ (2008) Root colonisation following seed inoculation. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 13–33CrossRefGoogle Scholar
  25. Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729.  https://doi.org/10.1046/j.1462-2920.2003.00471.x CrossRefPubMedGoogle Scholar
  26. Cóndor Golec AF, González Pérez P, Lokare C (2007) Effective microorganisms: myth or reality? Rev Peru Biol 14:315–319.  https://doi.org/10.15381/rpb.v14i2.1837 CrossRefGoogle Scholar
  27. Cote CK, Heffron JD, Bozue JA, Welkos SL (2015) Bacillus anthracis and other Bacillus species. In: Tang Y-W, Sussman M, Liu D, Poxton I, Schwartzman J (eds) Molecular medical microbiology, 2nd edn. Academic Press, London, pp 1789–1844Google Scholar
  28. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Anderson GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072.  https://doi.org/10.1128/AEM.03006-05 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Díaz-Zorita M, Canigia MVF, Bravo OÁ, Berger A, Satorre EH (2015) Field evaluation of extensive crops inoculated with Azospirillum sp. In: Cassán FB, Okon Y, Creus CM (eds) Handbook for Azospirillum: technical issues and protocols. Springer, Cham, pp 435–445Google Scholar
  30. do Amaral FP, Pankievicz VCS, ACM A, de Souza EM, Pedrosa F, Stacey G (2016) Differential growth responses of Brachypodium distachyon genotypes to inoculation with plant growth promoting rhizobacteria. Plant Mol Biol 90:689–697.  https://doi.org/10.1007/s11103-016-0449-8 CrossRefPubMedGoogle Scholar
  31. Doran JW (2002) Soil health and global sustainability: translating science into practice. Agric Ecosyst Environ 88:119–127.  https://doi.org/10.1016/S0167-8809(01)00246-8 CrossRefGoogle Scholar
  32. Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:3–11.  https://doi.org/10.1016/S0929-1393(00)00067-6 CrossRefGoogle Scholar
  33. Doumbou CL, Hamby Salove MK, Crawford DL, Beaulieu C (2002) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85–102.  https://doi.org/10.7202/706219ar CrossRefGoogle Scholar
  34. Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36:232–244.  https://doi.org/10.3109/10408411003766806 CrossRefPubMedGoogle Scholar
  35. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189.  https://doi.org/10.1016/j.apsoil.2007.02.005 CrossRefGoogle Scholar
  38. Egamberdiyeva D, Höflich G (2003) Influence of growth-promoting bacteria on the growth of wheat in different soils and temperatures. Soil Biol Biochem 35:973–978.  https://doi.org/10.1016/S0038-0717(03)00158-5 CrossRefGoogle Scholar
  39. Elmer WH (1987) Effects of inoculum densities of Fusarium oxysporum f. sp. apii in organic soil on disease expression in celery. Plant Dis 71:1086–1089CrossRefGoogle Scholar
  40. EPPO (2012a) Principles of efficacy evaluation for microbial plant protection products. EPPO Bulletin. http://pp1.eppo.org/list.php. Accessed 6 November 2017
  41. EPPO (2012b) Introduction to the efficacy evaluation of plant protection products. EPPO Bulletin. http://pp1.eppo.org/list.php. Accessed 6 November 2017
  42. EPPO (2012c) Number of efficacy trials. EPPO Bulletin. http://pp1.eppo.org/list.php.
  43. Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase: bacterial traits required in rhizosphere, rhizoplane and/or endophytic competence by beneficial bacteria. In: Maheshwari DK (ed) Bacterial metabolites in sustainable agroecosystem. Springer, Cham, pp 183–258CrossRefGoogle Scholar
  44. Ferreira Gregorio AP, Da Silva IR, Sedarati MR, Hedger JN (2006) Changes in production of lignin degrading enzymes during interactions between mycelia of the tropical decomposer Basidiomycetes, Marasmiellus troyanus and Marasmius pallescens. Mycol Res 110:161–168CrossRefGoogle Scholar
  45. Figueiredo GGO, Lopes VR, Fendrich RC, Szilagyi-Zecchin VJ (2017) Interaction between beneficial bacteria and sugarcane. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer Nature, Singapore, pp 1–28Google Scholar
  46. Finkel OM, Castrillo G, Herrera Paredes S, González IS, Dangl JL (2017) Understanding and exploiting plant beneficial microbes. Curr Opin Plant Biol 38:155–163.  https://doi.org/10.1016/j.pbi.2017.04.018 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM (2010) Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217.  https://doi.org/10.1016/j.apsoil.2010.04.007 CrossRefGoogle Scholar
  48. Fravel D, Olivain C, Alabouvette C (2003) Fusarium oxysporum and its biocontrol. New Phytol 157:493–502.  https://doi.org/10.1046/j.1469-8137.2003.00700.x CrossRefGoogle Scholar
  49. Fu SF, Sun PF, Lu HY, Wei JY, Xiao HS, Fang WT, Cheng BY, Chou JY (2016) Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spatulata Lab. Fungal Biol 120:433–448.  https://doi.org/10.1016/j.funbio.2015.12.006 CrossRefPubMedGoogle Scholar
  50. Gamalero E, Glick BR (2011) Mechanisms used by plant growth-promoting bacteria. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 17–46CrossRefGoogle Scholar
  51. Garcia MM, Pereira LC, Braccini AL, Angelotti P, Suzukawa AK, Marteli DCV, Felber PH, Bianchessi PA, Dametto IB (2017) Effects of Azospirillum brasilense on growth and yield components of maize grown at nitrogen limiting conditions. Rev Fac Cienc Agrar 40:353–362CrossRefGoogle Scholar
  52. Gerbaldo GA, Barberis C, Pascual L, Dalcero A, Barberis L (2012) Antifungal activity of two Lactobacillus strains with potential probiotic properties. FEMS Microbiol Lett 332:27–33.  https://doi.org/10.1111/j.1574-6968.2012.02570.x CrossRefPubMedGoogle Scholar
  53. Ghorbanpour M, Omidvari M, Abbaszadeh-Dahaji P, Omidvar R, Kariman K (2018) Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol Control 117:147–157.  https://doi.org/10.1016/j.biocontrol.2017.11.006 CrossRefGoogle Scholar
  54. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15.  https://doi.org/10.6064/2012/963401 CrossRefGoogle Scholar
  55. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877.  https://doi.org/10.1104/pp.017004.872 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Hallenbeck PC, Liu Y (2016) Recent advances in hydrogen production by photosynthetic bacteria. Int J Hydrog Energy 41:4446–4454.  https://doi.org/10.1016/j.ijhydene.2015.11.090 CrossRefGoogle Scholar
  57. Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools , techniques , and challenges. Genome Res 19:1141–1152.  https://doi.org/10.1101/gr.085464.108 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Higa T, Parr JF (1994) Beneficial and effective microorganisms for a sustainable agriculture and environment. Int Nat Farming Res Cent 1:1–16Google Scholar
  59. Houlden A, Timms-Wilson TM, Day MJ, Bailey MJ (2008) Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiol Ecol 65:193–201.  https://doi.org/10.1111/j.1574-6941.2008.00535.x CrossRefPubMedGoogle Scholar
  60. Huang X, Zhou X, Zhang J, Cai Z (2019) Highly connected taxa located in the microbial network are prevalent in the rhizosphere soil of healthy plant. Biol Fertil Soils 55:299–312.  https://doi.org/10.1007/s00374-019-01350-1 CrossRefGoogle Scholar
  61. James EK, Olivares FL (1997) Infection and colonization of sugar cane and other graminaceous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119.  https://doi.org/10.1016/S0735-2689(98)00357-8 CrossRefGoogle Scholar
  62. Jog R, Nareshkumar G, Rajkumar S (2016) Enhancing soil health and plant growth promotion by actinomycetes. In: Subramaniam G, Arumugam S, Rajendran V (eds) Plant growth promoting actinobacteria: a new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, Singapore, pp 33–45CrossRefGoogle Scholar
  63. Kim J (2005) Antifungal activity of lactic acid bacteria isolated from Kimchi against Aspergillus fumigatus. Mycobiology 33:210–214.  https://doi.org/10.4489/MYCO.2005.33.4.210 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Kobayashi M, Haque M (1971) Contribution to nitrogen fixation and soil fertility by photosynthetic bacteria. Plant Soil 35:443–456CrossRefGoogle Scholar
  65. Koch E (1999) Evaluation of commercial products for microbial control of soil-borne plant diseases. Crop Prot 18:119–125.  https://doi.org/10.1016/S0261-2194(98)00102-1 CrossRefGoogle Scholar
  66. Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad BUM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068.  https://doi.org/10.1111/j.1469-8137.2005.01376.x CrossRefPubMedGoogle Scholar
  67. König H, Fröhlich J (2009) Lactic acid bacteria. In: König H, Gottfried U, Fröhlich J (eds) Biology of microorganisms on grapes, in must and in wine, 2nd edn. Springer International Publishing, Cham, pp 3–42Google Scholar
  68. Kubicek CP, Komon-Zelazowska M, Druzhinina IS (2008) Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B 9:753–763.  https://doi.org/10.1631/jzus.B0860015 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Lamont JR, Wilkins O, Bywater-Ekegard M, Smith DL (2017) From yoghurt to yield: potential applications of lactic acid bacteria in plant production. Soil Biol Biochem 111:1–9. doi:  https://doi.org/10.1016/j.soilbio.2017.03.015 CrossRefGoogle Scholar
  70. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280.  https://doi.org/10.1007/s004420100716 CrossRefPubMedGoogle Scholar
  71. Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, Pallen MJ (2012) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 30:434–439.  https://doi.org/10.1038/nbt.2198 CrossRefPubMedGoogle Scholar
  72. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Anton Leeuw Int J G 86:1–25.  https://doi.org/10.1023/B:ANTO.0000024903.10757.6e CrossRefGoogle Scholar
  73. Mandeel Q, Baker R (1991) Mechanisms involved in biological control of Fusarium wilt in cucumber with strains of nonpathogenic Fusarium oxysporum. Phytopathology 81:462–469CrossRefGoogle Scholar
  74. Mehnaz S (2013) Microbes—friends and foes of sugarcane. J Basic Microbiol 53:954–971.  https://doi.org/10.1002/jobm.201200299 CrossRefPubMedGoogle Scholar
  75. Mendes R, Pizzirani-Kleiner AA, Araujo WL, Raaijmakers JM (2007) Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. Appl Environ Microbiol 73:7259–7267.  https://doi.org/10.1128/AEM.01222-07 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Murray JD (2011) Invasion by invitation: rhizobial infection in legumes. Mol Plant-Microbe Interact 24:631–639.  https://doi.org/10.1094/MPMI-08-10-0181 CrossRefPubMedGoogle Scholar
  77. Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2014) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50:249–262.  https://doi.org/10.1007/s00374-013-0854-y CrossRefGoogle Scholar
  78. Nielsen UN, Wall DH, Six J (2015) Soil biodiversity and the environment. Annu Rev Environ Resour 40:63–90.  https://doi.org/10.1146/annurev-environ-102014-021257 CrossRefGoogle Scholar
  79. Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2014) Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biol 118:683–694.  https://doi.org/10.1016/j.funbio.2014.04.010 CrossRefPubMedGoogle Scholar
  80. Nutri-Tech Solutions (2017) Nutri-life platform: new and improved blend. Nutri-Tech. https://shop.nutri-tech.com.au/products/platform. Accessed 6 November 2017
  81. Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1–12.  https://doi.org/10.3389/fpls.2016.01110 CrossRefGoogle Scholar
  82. Paungfoo-Lonhienne C, Yeoh YK, Kasinadhuni NRP, Lonhienne TGA, Robinson N, Hugenholtz P, Ragan MA, Schmidt S (2015) Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere. Sci Rep 5:1–6.  https://doi.org/10.1038/srep08678 CrossRefGoogle Scholar
  83. Paungfoo-Lonhienne C, Lonhienne TGA, Yeoh YK, Donose BC, Webb RI, Parsons J, Liao W, Sagulenko E, Lakshmanan P, Hugenholtz P, Schmidt S, Ragan MA (2016) Crosstalk between sugarcane and a plant-growth promoting Burkholderia species. Sci Rep 6:1–14.  https://doi.org/10.1038/srep37389 CrossRefGoogle Scholar
  84. Pedula RO, Schultz N, Monteiro RC, Pereira W, de Araujo AP, Urquiaga S, Reis VM (2016) Growth analysis of sugarcane inoculated with diazotrophic bacteria and nitrogen fertilization. Afr J Agric Res 11:2786–2795.  https://doi.org/10.5897/AJAR2016.11141 CrossRefGoogle Scholar
  85. Philip D (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930CrossRefGoogle Scholar
  86. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils:403–415.  https://doi.org/10.1007/s00374-015-0996-1 CrossRefGoogle Scholar
  87. Qiao J, Yu X, Liang X, Liu Y, Borriss R, Liu Y (2017) Addition of plant-growth-promoting Bacillus subtilis PTS-394 on tomato rhizosphere has no durable impact on composition of root microbiome. BMC Microbiol 17:1–12.  https://doi.org/10.1186/s12866-017-1039-x CrossRefGoogle Scholar
  88. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.-R-project.org/Google Scholar
  89. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361.  https://doi.org/10.1007/s11104-008-9568-6 CrossRefGoogle Scholar
  90. Raynaud X, Nunan N (2014) Spatial ecology of bacteria at the microscale in soil. PLoS One 9:e87217.  https://doi.org/10.1371/journal.pone.0087217 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Reis VM, Teixeira KRDS (2015) Nitrogen fixing bacteria in the family Acetobacteraceae and their role in agriculture. J Basic Microbiol 55:931–949.  https://doi.org/10.1002/jobm.201400898 CrossRefPubMedGoogle Scholar
  92. Research and Markets (2017) Global agricultural microbial market—forecasts from 2017 to 2022. Research and Markets. https://www.researchandmarkets.com/research/w9mfnj/global/. Accessed 6 November 2017
  93. Robinson N, Vogt J, Lakshmanan P, Schmidt S (2013) Nitrogen physiology of sugarcane. In: Moore PH, Botha FC (eds) Sugarcane: physiology, biochemistry, and functional biology. John Wiley & Sons, New York, pp 169–195CrossRefGoogle Scholar
  94. Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria : a critical review. Life Sci Med Res 1–30Google Scholar
  95. Sarabia M, Jakobsen I, Grønlund M, Carreon-Abud Y, Larsen J (2018) Rhizosphere yeasts improve P uptake of a maize arbuscular mycorrhizal association. Appl Soil Ecol 125:18–25.  https://doi.org/10.1016/j.apsoil.2017.12.012 CrossRefGoogle Scholar
  96. Singh S, Srivastava K, Sharma S, Sharma AK (2014) Mycorrhizal inoculum production. In: Solaiman Z, Abbott L, Varma A (eds) Mycorrhizal fungi: use in sustainable agriculture and land restoration. Springer, Berlin, pp 67–80CrossRefGoogle Scholar
  97. Singh RK, Singh P, Li HB, Yang LT, Li YR (2017) Soil–plant–microbe interactions: use of nitrogen-fixing bacteria for plant growth and development in sugarcane. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives. Springer Nature, Singapore, pp 35–59CrossRefGoogle Scholar
  98. Steenhoudt O, Vandereyden J (2000) Azospirillum, a free-living nitrogen fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506.  https://doi.org/10.1111/j.1574-6976.2000.tb00552.x CrossRefPubMedGoogle Scholar
  99. Tabassum B, Khan A, Tariq M, Ramzan M, Khan MSI, Shahid N, Aaliya K (2017) Bottlenecks in commercialisation and future prospects of PGPR. Appl Soil Ecol 121:102–117CrossRefGoogle Scholar
  100. Thokchom E, Thakuria D, Kalita MC, Sharma CK, Talukdar NC (2017) Root colonization by host-specific rhizobacteria alters indigenous root endophyte and rhizosphere soil bacterial communities and promotes the growth of mandarin orange. Eur J Soil Biol 79:48–56.  https://doi.org/10.1016/j.ejsobi.2017.02.003 CrossRefGoogle Scholar
  101. Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 2013:1–11.  https://doi.org/10.1155/2013/863240 CrossRefGoogle Scholar
  102. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355.  https://doi.org/10.1111/j.1469-8137.2004.01159.x CrossRefGoogle Scholar
  103. Valverde A, Burgos A, Fiscella T, Rivas R, Velazquez E, Rodriguez-Barrueco C, Cervantes E, Chamber M, Igual JM (2006) Differential effects of coinoculations with Pseudomonas jessenii PS06 (a phosphate-solubilizing bacterium) and Mesorhizobium ciceri C-2/2 strains on the growth and seed yield of chickpea under greenhouse and field conditions. In: Velazquez E, Rodriguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Springer, Dordrecht, pp 43–50Google Scholar
  104. van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254.  https://doi.org/10.1007/s10658-007-9165-1 CrossRefGoogle Scholar
  105. Vargas LK, Volpiano CG, Lisboa BB, Giongo A, Beneduzi A, Passaglia LMP (2017) Potential of rhizobia as plant growth-promoting rhizobacteria. In: Zaidi A, Khan MS, Musarrat J (eds) Microbes for legume improvement, 2nd edn. Springer, Cham, pp 153–174CrossRefGoogle Scholar
  106. Wei X, Hu Y, Razavi BS, Zhou J, Shen J, Nannipieri P, We J, Ge T (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biol Biochem 131:62–70CrossRefGoogle Scholar
  107. Xue C, Hao Y, Pu X, Penton CR, Wang Q, Zhao M, Zhang B, Ran W, Huang Q, Shen Q, Tiedje JM (2019) Effect of LSU and ITS genetic markers and reference databases on analyses of fungal communities. Biol Fertil Soils 55:79–88CrossRefGoogle Scholar
  108. Yamagiwa Y, Inagaki Y, Ichinose Y, Toyoda K, Hyakumachi M, Shiraishi T (2011) Talaromyces wortmannii FS2 emits β-caryphyllene, which promotes plant growth and induces resistance. J Gen Plant Pathol 77:336–341.  https://doi.org/10.1007/s10327-011-0340-z CrossRefGoogle Scholar
  109. Yeoh YK, Paungfoo-Lonhienne C, Dennis PG, Robinson RMA, Schmidt S, Hugenholtz P (2015) The core root microbiome of sugarcanes cultivated under varying nitrogen fertiliser application. Environ Microbiol 18:1338–1351.  https://doi.org/10.1111/1462-2920.12925 CrossRefGoogle Scholar
  110. Yeoh YK, Dennis PG, Paungfoo-Lonhienne C, Weber L, Brackin R, Ragan MA, Schmidt S, Hugenholtz P (2017) Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat Commun 8:215.  https://doi.org/10.1038/s41467-017-00262-8 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Yilmaz N, Visagie CM, Houbraken J, Frisvad JC, Samson RA (2014) Polyphasic taxonomy of the genus Talaromyces. Stud Mycol 78:175–341.  https://doi.org/10.1016/j.simyco.2014.08.001 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Zhang Y, Burris RH, Ludden PW, Roberts GP (1997) Regulation of nitrogen fixation in Azospirillum brasilense. FEMS Microbiol Lett 152:195–204.  https://doi.org/10.1111/j.1574-6968.1997.tb10428.x CrossRefPubMedGoogle Scholar
  113. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273.  https://doi.org/10.1111/j.1365-313X.2008.03593.x CrossRefPubMedGoogle Scholar
  114. Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620.  https://doi.org/10.1093/bioinformatics/btt593 CrossRefPubMedGoogle Scholar
  115. Zhou X, Zhang J, Pan D, Ge X, Jin X, Chen S, Wu F (2018) p-Coumaric can alter the composition of cucumber rhizosphere microbial communities and induce negative plant-microbial interactions. Biol Fertil Soils 54:363–372.  https://doi.org/10.1007/s00374-018-1265-x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Shelby Berg
    • 1
    Email author
  • Paul G. Dennis
    • 2
  • Chanyarat Paungfoo-Lonhienne
    • 1
    • 3
  • Jay Anderson
    • 1
  • Nicole Robinson
    • 1
  • Richard Brackin
    • 1
  • Adam Royle
    • 4
  • Lawrence DiBella
    • 4
  • Susanne Schmidt
    • 1
  1. 1.School of Agriculture and Food SciencesThe University of QueenslandBrisbaneAustralia
  2. 2.School of Earth and Environmental SciencesThe University of QueenslandBrisbaneAustralia
  3. 3.Sustainable Organic Solutions Pty. Ltd.BrisbaneAustralia
  4. 4.Herbert Cane Productivity Services Ltd.InghamAustralia

Personalised recommendations