[en] The use of plant biostimulants, also known as bioeffectors (BEs), has attracted increasing attention as an environmentally friendly strategy for more sustainable crop production. BEs are substances or microorganisms that are applied to plants or the surrounding soil to stimulate natural processes to enhance nutrient uptake, stress tolerance, and plant growth. Here, we tested the effectiveness of five BEs to enhance maize growth and phosphorus (P) uptake from various recycled P fertilizers in a series of pot and field experiments. First, the impact of two bacterial BEs and one soil-specific plant-based BE on crop performance was assessed in a 4-week screening experiment conducted in two arable, P-deficient soils of differing soil pH (a silty clay loam of pH 7.1 and a silty loam of pH 7.8) amended with recycled P-fertilizers (rock phosphate, biogas digestate, green waste compost, composted dairy manure, and chicken manure pellets). Then, for each soil type, the plant growth-promoting effect of the most promising BE–fertilizer combinations was re-assessed in an 8-week experiment. In addition, over a period of up to 3 years, three field experiments were conducted with maize in which up to two bacterial BEs were used either alone or in combination with a plant-based BE. Our experiments show that while BEs in combination with specific P-fertilizers can promote maize growth within the first weeks of growth under controlled conditions, the observed effects vanished in the long term, both in pots and under field conditions. In a tracing experiment, in which we tested the persistence of one bacterial BE over a period of 5 weeks, we observed a drastic decrease in colony-forming units already 2 weeks after inoculation. As previously shown in other studies, our data indicate that the plant growth-promoting effects of BEs found under controlled conditions are not directly transferable to field conditions. It is suggested that the drastic decline in inoculated bacterial strains in the tracing experiment is the reason for the decline in plant growth effect.
Adesemoye A. O. Kloepper J. W. (2009). Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl. Microbiol. Biotechnol. 85, 1–12. doi: 10.1007/s00253-009-2196-0
Ali S. Moon Y.-S. Hamayun M. Khan M. A. Bibi K. Lee I.-J. (2022). Pragmatic role of microbial plant biostimulants in abiotic stress relief in crop plants. J. Plant Interact. 17, 705–718. doi: 10.1080/17429145.2022.2091801
Backer R. Rokem J. S. Ilangumaran G. Lamont J. Praslickova D. Ricci E. et al. (2018). Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 9, 1473. doi: 10.3389/fpls.2018.01473
Berg G. Kusstatscher P. Abdelfattah A. Cernava T. Smalla K. (2021). Microbiome modulation—toward a better understanding of plant microbiome response to microbial inoculants. Front. Microbiol. 12, 650610. doi: 10.3389/fmicb.2021.650610
Bradáčová K. Kandeler E. Berger N. Ludewig U. Neumann G. (2020). Microbial consortia inoculants stimulate early growth of maize depending on nitrogen and phosphorus supply. Plant Soil Environ. 66, 105–112. doi: 10.17221/382/2019-PSE
Cordell D. Drangert J.-O. White S. (2009). The story of phosphorus: global food security and food for thought. Global Environ. Change 19, 292–305. doi: 10.1016/j.gloenvcha.2008.10.009
Dobbelaere S. Croonenborghs A. Thys A. Ptacek D. Vanderleyden J. Dutto P. et al. (2001). Responses of agronomically important crops to inoculation with Azospirillum. Funct. Plant Biol. 28, 871–879. doi: 10.1071/PP01074
Dobbss L. B. Canellas L. P. Olivares F. L. Aguiar N. O. Peres L. E. P. Azevedo M. et al. (2010). Bioactivity of chemically transformed humic matter from vermicompost on plant root growth. J. Agric. Food Chem. 58, 3681–3688. doi: 10.1021/jf904385c
Du Jardin P. (2015). Plant biostimulants: Definition, concept, main categories and regulation. Scientia Hortic. 196, 3–14. doi: 10.1016/j.scienta.2015.09.021
Dunbabin V. Armstrong R. Officer S. Norton R. (2009). Identifying fertiliser management strategies to maximise nitrogen and phosphorus acquisition by wheat in two contrasting soils from Victoria, Australia. Soil Res. 47, 74–90. doi: 10.1071/SR08107
Hawkes C. V. Connor E. W. (2017). Translating phytobiomes from theory to practice: ecological and evolutionary considerations. Phytobiomes 1, 57–69. doi: 10.1094/PBIOMES-05-17-0019-RVW
Herrmann M. N. Wang Y. Hartung J. Hartmann T. Zhang W. Nkebiwe P. M. et al. (2022). A global network meta-analysis of the promotion of crop growth, yield, and quality by bioeffectors. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.816438
Jindo K. Olivares F. L. Malcher D. J. d. P. Sánchez-Monedero M. A. Kempenaar C. et al. (2020). From lab to field: Role of humic substances under open-field and greenhouse conditions as biostimulant and biocontrol agent. Front. Plant Sci. 11, 426. doi: 10.3389/fpls.2020.00426
Koskella B. Taylor T. B. (2018). Multifaceted impacts of bacteriophages in the plant microbiome. Annu. Rev. Phytopathol. 56, 361–380. doi: 10.1146/annurev-phyto-080417-045858
Kumar M. Mishra S. Dixit V. Kumar M. Agarwal L. Chauhan P. S. et al. (2016). Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signaling Behav. 11, e1071004. doi: 10.1080/15592324.2015.1071004
Lenth R. P. Bolker B. Buerkner P. Giné-Vázquez I. Herve M. Jung M. et al. (2023). H. emmeans: Estimated Marginal Means, aka Least-Squares Means.
Li J. Wang J. Liu H. Macdonald C. A. Singh B. K. (2022). Application of microbial inoculants significantly enhances crop productivity: a meta-analysis of studies from 2010 to 2020. J. Sustain. Agric. Environ. 1, 216–225. doi: 10.1002/sae2.12028
Lori M. Symnaczik S. Mäder P. De Deyn G. Gattinger A. (2017). Organic farming enhances soil microbial abundance and activity—A meta-analysis and meta-regression. PloS One 12, e0180442. doi: 10.1371/journal.pone.0180442
Lynch J. P. Brown K. M. (2001). Topsoil foraging–an architectural adaptation of plants to low phosphorus availability. Plant Soil 237, 225–237. doi: 10.1023/A:1013324727040
Ma Y. Freitas H. Dias M. C. (2022). Strategies and prospects for biostimulants to alleviate abiotic stress in plants. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1024243
Mäder P. Kaiser F. Adholeya A. Singh R. Uppal H. S. Sharma A. K. et al. (2011). Inoculation of root microorganisms for sustainable wheat–rice and wheat–black gram rotations in India. Soil Biol. Biochem. 43, 609–619. doi: 10.1016/j.soilbio.2010.11.031
Mallon C. A. Le Roux X. Van Doorn G. Dini-Andreote F. Poly F. Salles J. (2018). The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader’s niche. ISME J. 12, 728–741. doi: 10.1038/s41396-017-0003-y
Monda H. Cozzolino V. Vinci G. Drosos M. Savy D. Piccolo A. (2018). Molecular composition of the Humeome extracted from different green composts and their biostimulation on early growth of maize. Plant and Soil 429, 407–424.
Mosimann C. Oberhänsli T. Ziegler D. Nassal D. Kandeler E. Boller T. et al. (2017). Tracing of two pseudomonas strains in the root and rhizoplane of maize, as related to their plant growth-promoting effect in contrasting soils. Front. Microbiol. 7. doi: 10.3389/fmicb.2016.02150
Mpanga I. K. Nkebiwe P. M. Kuhlmann M. Cozzolino V. Piccolo A. Geistlinger J. et al. (2019). The form of N supply determines plant growth promotion by P-solubilizing microorganisms in maize. Microorganisms 7, 38. doi: 10.3390/microorganisms7020038
Mukherjee A. Patel J. S. (2020). Seaweed extract: biostimulator of plant defense and plant productivity. Int. J. Environ. Sci. Technol. 17, 553–558. doi: 10.1007/s13762-019-02442-z
Murphy J. Riley J. P. (1962). A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36. doi: 10.1016/S0003-2670(00)88444-5
Otto S. Harms H. Wick L. Y. (2017). Effects of predation and dispersal on bacterial abundance and contaminant biodegradation. FEMS Microbiol. Ecol. 93. doi: 10.1093/femsec/fiw241
Owen D. Williams A. P. Griffith G. W. Withers P. J. (2015). Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl. Soil Ecol. 86, 41–54. doi: 10.1016/j.apsoil.2014.09.012
Pinheiro J. Bates D. R Core Team. (2022). nlme: Nonlinear Mixed Effects Models.
R Core Team. (2022). R: a language and environment for statistical computing. R Foundation for Statistical Computing.
Richardson A. E. Simpson R. J. (2011). Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 156, 989–996. doi: 10.1104/pp.111.175448
Rivett D. W. Jones M. L. Ramoneda J. Mombrikotb S. B. Ransome E. Bell T. (2018). Elevated success of multispecies bacterial invasions impacts community composition during ecological succession. Ecol. Lett. 21, 516–524. doi: 10.1111/ele.12916
Rose M. T. Patti A. F. Little K. R. Brown A. L. Jackson W. R. Cavagnaro T. R. (2014). A meta-analysis and review of plant-growth response to humic substances: practical implications for agriculture. Adv. Agron. 124, 37–89. doi: 10.1016/B978-0-12-800138-7.00002-4
Rubin R. L. van Groenigen K. J. Hungate B. A. (2017). Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant Soil 416, 309–323. doi: 10.1007/s11104-017-3199-8
RStudio Team. (2020). RStudio: Integrated Development Environment for R RStudio. PBC, Boston, MA
Schütz L. Gattinger A. Meier M. Müller A. Boller T. Mäder P. et al. (2018). Improving crop yield and nutrient use efficiency via biofertilization—A global meta-analysis. Front. Plant Sci. 8, 2204. doi: 10.3389/fpls.2017.02204
Sible C. N. Seebauer J. R. Below F. E. (2021). Plant biostimulants: A categorical review, their implications for row crop production, and relation to soil health indicators. Agronomy 11, 1297. doi: 10.3390/agronomy11071297
Smil V. (2000). Phosphorus in the environment: natural flows and human interferences. Annu. Rev. Energy Environ. 25, 53–88. doi: 10.1146/annurev.energy.25.1.53
Thonar C. Lekfeldt J. D. S. Cozzolino V. Kundel D. Kulhánek M. Mosimann C. et al. (2017). Potential of three microbial bio-effectors to promote maize growth and nutrient acquisition from alternative phosphorous fertilizers in contrasting soils. Chem. Biol. Technol. Agric. 4, 1–16. doi: 10.1186/s40538-017-0088-6
Tilman D. Cassman K. G. Matson P. A. Naylor R. Polasky S. (2002). Agricultural sustainability and intensive production practices. Nature 418, 671–677. doi: 10.1038/nature01014
Tilman D. Fargione J. Wolff B. D'antonio C. Dobson A. Howarth R. et al. (2001). Forecasting agriculturally driven global environmental change. Science 292, 281–284. doi: 10.1126/science.1057544
Vermeulen S. J. Campbell B. M. Ingram J. S. (2012). Climate change and food systems. Annu. Rev. Environ. Resour. 37, 195–222. doi: 10.1146/annurev-environ-020411-130608
Weinmann M. Neumann G. (2020). “Bio-effectors to optimize the mineral nutrition of crop plants,” in Achieving sustainable crop nutrition (Cambridge: Burleigh Dodds Science Publishing), 589–690. doi: 10.19103/AS.2019.0062.27
Wickham H. ggplot2: Elegant Graphics for Data Analysis. 2016
Wozniak E. Blaszczak A. Wiatrak P. Canady M. (2020). Biostimulant Mode of Action: Impact of Biostimulant on Whole‐Plant Level. The Chemical Biology of Plant Biostimulants, 205–227.
Yang F. Tang C. Antonietti M. (2021). Natural and artificial humic substances to manage minerals, ions, water, and soil microorganisms. Chem. Soc. Rev. 50, 6221–6239. doi: 10.1039/D0CS01363C
Yang T. Wei Z. Friman V. P. Xu Y. Shen Q. Kowalchuk G. A. et al. (2017). Resource availability modulates biodiversity-invasion relationships by altering competitive interactions. Environ. Microbiol. 19, 2984–2991. doi: 10.1111/1462-2920.13708
Zhao X. Yuan X. Xing Y. Dao J. Zhao D. Li Y. et al. (2023). A meta-analysis on morphological, physiological and biochemical responses of plants with PGPR inoculation under drought stress. Plant Cell Environ. 46, 199–214. doi: 10.1111/pce.14466