Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system

Nature Biotechnology volume 30, pages 889–893 (2012)Cite this article

Subjects

Abstract

High crop yields depend on the continuous input of orthophosphate (PO4−3)-based fertilizers and herbicides1,2. Two major challenges for agriculture are that phosphorus is a nonrenewable resource and that weeds have developed broad herbicide resistance3,4,5. One strategy to overcome both problems is to engineer plants to outcompete weeds and microorganisms for limiting resources, thereby reducing the requirement for both fertilizers and herbicides. Plants and most microorganisms are unable to metabolize phosphite (PO3−3), so we developed a dual fertilization and weed control system by generating transgenic plants that can use phosphite as a sole phosphorus source. Under greenhouse conditions, these transgenic plants require 30–50% less phosphorus input when fertilized with phosphite to achieve similar productivity to that obtained by the same plants using orthophosphate fertilizer and, when in competition with weeds, accumulate 2–10 times greater biomass than when fertilized with orthophosphate.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Transgenic Arabidopsis plants that express a phosphite oxidoreductase can use phosphite as a phosphorus source.
Figure 2: Effect of phosphite fertilization on WT and transgenic tobacco plants in a low-phosphate nonsterile soil.
Figure 3: Effectiveness of the PTXD/phosphite system for weed control in a nonsterile soil.

Similar content being viewed by others

Accession codes

Primary accessions

NCBI Reference Sequence

References

  1. Tilman, D. et al. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).

    Article  CAS  Google Scholar 

  2. Gianessi, L.P. & Reigner, N.P. The value of herbicides in US crop production. Weed Technol. 21, 559–566 (2007).

    Article  Google Scholar 

  3. Dawson, C.J. & Hilton, J. Fertiliser availability in a resource-limited world: production and recycling of nitrogen and phosphorus. Food Policy 36, S14–S22 (2011).

    Article  Google Scholar 

  4. Cordell, D., Drangert, J.-O. & White, S. The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292–305 (2009).

    Article  Google Scholar 

  5. Powles, S.B. & Yu, Q. Evolution in action: plants resistant to herbicides. Annu. Rev. Plant Biol. 61, 317–347 (2010).

    Article  CAS  Google Scholar 

  6. Gilbert, N. The disappearing nutrient. Nature 461, 716–718 (2009).

    Article  CAS  Google Scholar 

  7. Cakmak, I. Plant nutrition research: priorities to meet human needs for food in sutainable ways. Plant Soil 247, 3–24 (2002).

    Article  CAS  Google Scholar 

  8. Hinsinger, P. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237, 173–195 (2001).

    Article  CAS  Google Scholar 

  9. Syers, J.K., Johnston, A.E. & Curtis, D. Efficiency of soil and fertilizer phosphorus use: reconciling changing concepts of soil phosphorus behavior with agronomic information. Fertilizer and Plant Nutrition Bulletin 18 (Food and Agriculture Organization of the United Nations, 2008).

  10. Carpenter, S.R. Phosphorus control is critical to mitigating eutrophication. Proc. Natl. Acad. Sci. USA 105, 11039–11040 (2008).

    Article  CAS  Google Scholar 

  11. Downing, J.A., Watson, S.B. & McCauley, E. Predicting cyanobacterial dominance in lakes. Rapid communication. Can. J. Fish. Aquat. Sci. 58, 1905–1908 (2001).

    Article  Google Scholar 

  12. Abelson, P.H. A potential phosphate crisis. Science 283, 2015 (1999).

    Article  CAS  Google Scholar 

  13. Ruthbaum, H.P. & Baille, W.J.H. The use of red phosphorus as a fertilizer. Part 4. Phosphite and phosphate retention in soil. N. Z. J. Sci. 7, 446–451 (1964).

    Google Scholar 

  14. Morton, S. et al. Analysis of reduced phosphorus in samples of environmental interest. Environ. Sci. Technol. 39, 4369–4376 (2005).

    Article  CAS  Google Scholar 

  15. Pasek, M. Rethinking early earth phosphorus geochemistry. Proc. Natl. Acad. Sci. USA 105, 853–858 (2008).

    Article  CAS  Google Scholar 

  16. White, A.K. & Metcalf, W.W. Microbial metabolism of reduced phosphorus compounds. Annu. Rev. Microbiol. 61, 379–400 (2007).

    Article  CAS  Google Scholar 

  17. Schroetter, S., Angeles-Wedler, D., Kreuzig, R. & Schnug, E. Effects of phosphite on phosphorus supply and growth of corn (Zea mays). Landbauforschung Völkenrode 56, 87–99 (2006).

    CAS  Google Scholar 

  18. Ouimette, D.G. & Coffey, M.D. Phosphonate levels in avocado (Persea amercana) seedlings and soil following treatment with Fosetyl-Al or potassium phosphonate. Plant Dis. 73, 212–215 (1989).

    Article  CAS  Google Scholar 

  19. Carswell, C. et al. The fungicide phosphonate disrupts the phosphate-starvation response in Brassica nigra seedlings. Plant Physiol. 110, 105–110 (1996).

    Article  CAS  Google Scholar 

  20. Carswell, M.C., Grant, B.R. & Plaxton, W.C. Disruption of the phosphate-starvation response of oilseed rape suspension cells by the fungicide Phosphonate. Planta 203, 67–74 (1997).

    Article  CAS  Google Scholar 

  21. Förster, H. et al. Effect of phosphite on tomato and pepper plants and on susceptibility of pepper to Phytophthora root and crown rot in hydroponic culture. Plant Dis. 82, 1165–1170 (1998).

    Article  Google Scholar 

  22. Ticconi, C.A., Delatorre, C.A. & Abel, S. Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol. 127, 963–972 (2001).

    Article  CAS  Google Scholar 

  23. Varadarajan, D.K. et al. Phosphite, an analogue of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol. 129, 1232–1240 (2002).

    Article  CAS  Google Scholar 

  24. McDonald, A.E., Grant, B.R. & Plaxton, W.C. Phosphite (phosphorus acid): its relevance in the environment and agriculture and influence on plant phosphate starvation response. J. Plant Nutr. 24, 1505–1519 (2001).

    Article  CAS  Google Scholar 

  25. Saindrenan, P., Barchietto, T. & Gilbert, B. Modification of the phosphite induced resistance response in leaves of cowpea infected with Phytophthora cryptogea by α-aminooxyacetate. Plant Sci. 58, 245–252 (1988).

    Article  CAS  Google Scholar 

  26. Costas, A.M.G., White, A.K. & Metcalf, W.W. Purification and characterization of a novel phosphorus-oxidizing enzyme from Pseudomonas stutzeri WM88. J. Biol. Chem. 276, 17429–17436 (2001).

    Article  CAS  Google Scholar 

  27. Metcalf, W.W. & Wolfe, R.S. Molecular genetic analysis of phosphite and hypophosphite oxidation by Pseudomonas stutzeri WM88. J. Bacteriol. 180, 5547–5558 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Rao, I.M., Arulanantham, A.R. & Terry, N. Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. II. Diurnal changes in sugar phosphates, adenylates, and nicotinamide nucleotides. Plant Physiol. 90, 820–826 (1989).

    Article  CAS  Google Scholar 

  29. Lee, T.-M. The effects of phosphite on phosphate starvation responses of Ulva lactuca (Ulvales, Chlorophyta). J. Phycol. 41, 975–982 (2005).

    Article  CAS  Google Scholar 

  30. Martinez-Trujillo, M. et al. Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol. Biol. Rep. 22, 63–70 (2004).

    Article  CAS  Google Scholar 

  31. Sambrook, J. & Russell, D.W. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory, 2001).

  32. Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Delta Delta C (T)] method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

  33. Horsch, R.B. et al. A simple and general method for transferring genes into plants. Science 227, 1229–1231 (1985).

    Article  CAS  Google Scholar 

  34. Abramoff, M.D., Magelhaes, P.J. & Ram, S.J. Image processing with ImageJ. Biophotonics Int. 11, 36–42 (2004).

    Google Scholar 

  35. Wrobel, K. et al. Phosphorus and osmium as elemental tags for the determination of global DNA methylation- a novel application of high performance liquid chromatography inductively coupled plasma mass spectrometry in epigenetic studies. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 878, 609–614 (2010).

    Article  CAS  Google Scholar 

  36. Hesse, P.R. Soil phosphorus: its measurements and its uptake by plants. Aust. J. Soil Res. 35, 227–239 (1971).

    Google Scholar 

Download references

Acknowledgements

We thank O. Martínez for advice in statistical analysis; M.A. Leyva, A. Vera and J.L. Cabrera for technical support; K. Wrobel and K. Wrobel for the phosphite detection method; V. Limones for assistance in Tobacco transformation and C. Castro and E. Alva in Arabidopsis greenhouse experiments. We are grateful to A. Estrada, J.D. Frier and Universidad Autónoma Chapingo for providing Brachypodium distachyon, Amaranthus hybridus and Ipomoea purpurea and Brachiaria plantaginea seeds, respectively; and C. Morales for assistance in photosynthesis measurements. We thank S. Gillmore and V. Albert for critical reading this manuscript. This work was supported in part by grant from the Howard Hughes Medical Institute (grant 55005946) to L.H.-E. D.L.L.-A. is indebted to CONACyT, México, for a PhD fellowship (no. 207308). pWM302 was a gift from W.W. Metcalf.

Author information

Authors and Affiliations

  1. Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Guanajuato, México

    Damar Lizbeth López-Arredondo & Luis Herrera-Estrella

Authors
  1. Damar Lizbeth López-Arredondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luis Herrera-Estrella
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.L.L.-A. and L.H.-E. designed experiments, analyzed data and wrote the paper. D.L.L.-A. performed experiments.

Corresponding author

Correspondence to Luis Herrera-Estrella.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–11 (PDF 28014 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

López-Arredondo, D., Herrera-Estrella, L. Engineering phosphorus metabolism in plants to produce a dual fertilization and weed control system. Nat Biotechnol 30, 889–893 (2012). https://doi.org/10.1038/nbt.2346

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nbt.2346

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing