Skip to main content
Log in

Effects of Penicillium bilaii on maize growth are mediated by available phosphorus

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Inoculation with Penicillium bilaii has been reported to increase plant growth, which is attributed to increase availability of phosphorus (P), but similar effects have been observed with no P limitation, suggesting that other mechanisms may be involved. The aim of this work was to evaluate the interaction between available soil P and P. bilaii inoculation on plant growth.

Methods

Maize plants (Zea mays) inoculated with P. bilaii and non-inoculated were grown in pot experiments in three soils with different inherent P availability, and in a low P availability soil with different additions of mineral P, both with and without supplementation of all other macro and micronutrients.

Results

We found a positive interaction between P bilaii and available P, when other nutrients were applied, with P bilaii inoculation resulting in increased root growth and thus nutrient uptake and plant growth. By contrast, when other nutrients were not supplied, little effect on plant growth or P uptake was observed, except for root length that tended to decrease in inoculated plants with P addition.

Conclusions

The effects of P. bilaii inoculation were related to root growth and function, but were dependent on the nutrient status in the soil environment.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Asea P, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilization by to Penicillium species in solution culture and soil. Soil Biol Biochem 20:459–464

    Article  CAS  Google Scholar 

  • Barry DAJ, Miller MH (1989) Phosphorus nutritional requirement of maize seedlings for maximum yield. Agron J 81:95–99

    Article  Google Scholar 

  • Beckie HJ, Schlechte D, Moulin AP, Gleddie SC, Pulkinen DA (1998) Response of alfalfa to inoculation with Penicillium bilaii (Provide). Can J Plant Sci 78:91–102

    Article  Google Scholar 

  • Bünemann EK, Augstburger S, Frossard E (2016) Dominance of either physicochemical or biological phosphorus cycling processes in temperate forest soils of contrasting phosphate availability. Soil Biol Biochem 101:85–95

    Article  Google Scholar 

  • Campbell CR (2009) Reference sufficiency ranges for plant analysis in the southern region of the United States. Southern Cooperative Series Bulletin #394. North Carolina Department of Agriculture and Consumer Services Agronomic Division. NC, USA

  • Chambers JW (1992) Influence of a commercial fungal inoculant (PB-50) on plant nutrient availability and crop growth. M.Sc. thesis, University of Manitoba, Winnipeg

  • Chambers JW, Yeomans JC (1991) The influence of PB-50 on crop availability of phosphorus from soil and fertilizer as determined by 32P dilution. In: In Proceedings of the 34th Annual Meeting, Manitoba Society of Soil Science. Winnipeg, Manitoba, Canada: University of Manitoba, pp 75–87

  • Cunningham JE, Kuiack C (1992) Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium bilaii. Appl Environ Microbiol 58:1451–1458

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Oliveira Mendes G, de Freitas ALM, Pereira OL, da Silva IR, Vassilev NB, Costa MD (2014) Mechanisms of phosphate solubilization by fungal isolates when exposed to different P sources. Ann Microbiol 64:239–249

    Article  Google Scholar 

  • Downey J, van Kessel C (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji. Biol Fertil Soils 10:194–196

    Article  Google Scholar 

  • Gleddie SC (1992) Response of pea to inoculation with the phosphate –solubilizing fungus Penicillium bilaiae. MSc thesis. University of Saskatchewan, Saskatoon, SK

  • Gleddie SC, Hnatowich GL, Polonenko DR (1991) A summary of wheat response to Provide@ (Penicillium biluji) in western Canada. In: In Proc Alberta Soil Science Workshop. Lethbridge, Alberta

  • Gómez-Muñoz B, Magid J, Jensen LS (2017a) Nitrogen turnover, crop use efficiency and soil fertility in a long-term field experiment amended with different qualities of urban and agricultural waste. Agric Ecosyst Environ 240:300–313

    Article  Google Scholar 

  • Gómez-Muñoz B, Pittroff SM, de Neergaard A, Jensen LS, Nicolaisen MH, Magid J (2017b) Penicillium bilaii effects on maize growth and P uptake from soil and localized sewage sludge in a rhizobox experiment. Biol Fertil Soils:1–13

  • Gulden RH, Vessey JK (2000) Penicillium bilaii inoculation increases root-hair production in field pea. Can J Plant Sci 80:801–804

    Article  Google Scholar 

  • Haling RE, Yang Z, Shadwell N, Culvenor RA, Stefanski A, Ryan MH, Sandral GA, Kidd DR, Lambers H, Simpson RJ (2016) Growth and root dry matter allocation by pasture legumes and a grass with contrasting external critical phosphorus requirements. Plant Soil 407:67–79

    Article  CAS  Google Scholar 

  • Heisinger KG (1998) Effect of Penicillium bilaii on root morphology and architecture of pea (Pisum sativum L.). M.Sc. Thesis. University of Manitoba, Winnipeg

  • Hnatowich GL, Gleddie SC, Polonenko DR (1990) Wheat response to PB-50 (Penicillium bilaji), a phosphate-solubilizing inoculant. In: Havlin JL, Jacobsen JS (eds) Proc. Great Plains Soil Fert. Conf. Denver, CO, Kansas State University, Manhattan, KS., pp 82–87

  • Illmer P, Schinner F (1995) Solubilization of inorganic calcium phosphates - Solubilization mechanisms. Soil Biol Biochem 27:257–263

    Article  CAS  Google Scholar 

  • Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere microorganisms and plant phosphorus uptake. In: Sims JT, Sharpley AN (eds) Phosphorus, agriculture and the environment. American Society for Agronomy, Madison, pp 437–494

  • Karamanos RE, Flore NA, Harapiak JT (2010) Re-visiting use of Penicillium bilaii with phosphorus fertilization of hard red spring wheat. Can J Plant Sci 90:265–277

    Article  Google Scholar 

  • Keyes DO (1990) Penicillium bilaii: Interactions with crops. M.Sc. thesis. University of Alberta, Edmonton

  • Kucey RMN (1983) Phosphate-solubilizing bacteria and fungi in various cultivated and virgin Alberta soils. Can J Soil Sci 63:671–678

    Article  CAS  Google Scholar 

  • Kucey RMN (1987) Increased phosphorus uptake by wheat and field beans inoculated with a phosphorus-solubilizing Penicillium bilaji strain and with vesicular-arbuscular mycorrhizal fungi. Appl Environ Microbiol 53:2699–2703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kucey RMN, Leggett ME (1989) Increased yields and phosphorus uptake by westar canola (Brassica napus L .) inoculated with a phophate-solubilizaing isolate of Penicillium bilaji. Can J Soil Sci 39:425–432

    Article  Google Scholar 

  • Leggett ME, Newlands NK, Greenshields D, West L, Inman S, Koivunen ME (2015) Maize yield response to a phosphorus-solubilizing microbial inoculant in field trials. J Agric Sci 153:1464–1478

    Article  CAS  Google Scholar 

  • Lekfeldt JDS, Rex M, Mercl F, Kulhánek M, Tlustoš P, Magid J, de Neergaard A (2016) Effect of bioeffectors and recycled P-fertiliser products on the growth of spring wheat. Chem Biol Technol Agric 3. https://doi.org/10.1186/s40538-016-0074-4

  • López-Rayo S, Laursen KH, Lekfeldt JDS, Grazie FD, Magid J (2016) Long-term amendment of urban and animal wastes equivalent to more than 100 years of application had minimal effect on plant uptake of potentially toxic elements. Agric Ecosyst Environ 231:44–53

    Article  Google Scholar 

  • Marschner P (2008) The role of rhizosphere microorganisms in relation to P uptake by plants. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Springer, Heidelberg, pp 165–176

    Chapter  Google Scholar 

  • McLaughlin MJ, Alston AM (1986) The relative contribution of plant residues and fertiliser to the phosphorus nutrition of wheat in a pasture/cereal system. Aust J Soil Res 24:517–526

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria

  • Reuter DJ, Robinson JB (1997) Plant analysis: an interpretation manual. CSIRO Publishing, Collingwood

    Book  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culnover RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560

    Article  CAS  Google Scholar 

  • Sánchez-Esteva S, Gómez-Muñoz B, Jensen LS, de Neergaard A, Magid J (2016) The effect of Penicillium bilaii on wheat growth and phosphorus uptake as affected by soil pH, soil P and application of sewage sludge. Chem Biol Technol Agric 3:21

  • Schütz L, Gattinger A, Meier M, Müller A, Boller T, Mäder P, Mathimaran N (2018) Improving crop yield and nutrient use efficiency via biofertilization-a global meta-analysis. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.02204

  • Tarafdar JC, Rao AV, Praveen-Kumar (1995) Role of phosphatase-producing fungi on the growth and nutrition of clusterbean (Cyamopsis tetragonoloba (L.) Taub.). J Arid Environ 29:331–337

    Article  Google Scholar 

  • Thonar C, Lekfeldt JDS, Cozzolino V, Kundel D, Kulhánek M, Mosimann C, Neumann G, Piccolo A, Rex M, Symanczik S, Walder F, Weinmann M, de Neergaard A, Mäder P (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

    Article  Google Scholar 

  • Tinker C, Nye PH (2000) Solute movement in the rhizosphere, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Regent Instruments Inc. (2005) Winrhizo 2005 a, b basic, reg & pro for washed root measurement (user’s guide) Québec, Canada

  • Van der Paauw F (1971) An effective water extraction method for the determination of plant-available soil phosphorus. Plant Soil 34:467–481

    Article  Google Scholar 

  • Vessey JK, Heisinger KG (2001) Effect of Penicillium bilaii inoculation and phosphorus fertilisation on root and shoot parameters of field-grown pea. Can J Plant Sci 81:361–366

    Article  Google Scholar 

  • Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fertil Soils 40:36–43

    Article  CAS  Google Scholar 

  • Wang Y, Thorup-Kristensen K, Jensen LS, Magid J (2016) Vigorous root growth is a better indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility. Front Plant Sci 7:1–9

    PubMed  PubMed Central  Google Scholar 

  • Whitelaw MA, Harden TJ, Bender GL (1997) Plant growth promotion of wheat inoculated with Penicillium radicum sp. nov. Aust J Soil Res 35:291–300

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Lene Vigh, Lena Asta Byrgesen and Ayse Gül Özcetin for their support with sample analysis. This study was supported by Innovation Foundation Denmark (grant number 1308-00016B to the project “Microbial biofertilizers for enhanced crop availability of phosphorus pools in soil and waste, MiCroP”).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Magid.

Additional information

Responsible Editor: Matthew G. Bakker.

Electronic supplementary material

ESM 1

(DOCX 2.44 mb)

ESM 2

(DOCX 28.0 kb)

ESM 3

(DOCX 22.9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gómez-Muñoz, B., Jensen, L.S., de Neergaard, A. et al. Effects of Penicillium bilaii on maize growth are mediated by available phosphorus. Plant Soil 431, 159–173 (2018). https://doi.org/10.1007/s11104-018-3756-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3756-9

Keywords

Navigation