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Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate

Abstract

Phosphorus (P) is one of the most important nutrients limiting agricultural production worldwide. In acid and alkaline soils, which make up over 70% of the world's arable land, P forms insoluble compounds that are not available for plant use. To reduce P deficiencies and ensure plant productivity, nearly 30 million tons of P fertilizer are applied every year. Up to 80% of the applied P fertilizer is lost because it becomes immobile and unavailable for plant uptake. Therefore, the development of novel plant varieties more efficient in the use of P represents the best alternative to reduce the use of P fertilizers and achieve a more sustainable agriculture. We show here that the ability to use insoluble P compounds can be significantly enhanced by engineering plants to produce more organic acids. Our results show that when compared to the controls, citrate-overproducing plants yield more leaf and fruit biomass when grown under P-limiting conditions and require less P fertilizer to achieve optimal growth.

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Figure 1: Growth and productivity of CSb tobacco plants subjected to different P treatments.
Figure 2: Accumulation of biomass in CSb lines grown under limiting P conditions.
Figure 3: Height and total foliar area of transgenic and control plants grown in alkaline soil at suboptimal P fertilization.
Figure 4: P level in leaves of CSb and control lines.
Figure 5: Fruit dry weight of CSb-4, CSb-18, and control lines grown at two levels (22 and 44 p.p.m.) of hydroxyapatite in an alkaline soil.
Figure 6: Effect of citrate on the biomass accumulation of tobacco plants grown in media containing an insoluble source of phosphate.

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References

  1. Bar-Yosef, B. In Plant roots, the hidden half. (eds Waisel, Y., Eschel, A., Kafkafi V.) 529–557 (Marcel Dekker, New York, NY; 1991).

    Google Scholar 

  2. www.Fertilizer.org. Fertilizer demand and crops. International Industry Assoc. Paris, France (1999).

  3. Holford, I.C.R. Soil phosphorus: its measurements, and its uptake by plants. Aust. J. Soil Res. 35, 227–239 (1997).

    Article  CAS  Google Scholar 

  4. Sharpley, A.N. Soil phosphorus dynamics: agronomic and environmental impacts. Ecol. Eng. 5, 261–279 (1995).

    Article  Google Scholar 

  5. Loneragan, J.F. Plant nutrition in the 20th and perspectives for the 21st century. Plant Soil 196, 163–174 (1997).

    Article  CAS  Google Scholar 

  6. Schachtman, D.P., Reid, R.J. & Ayling, S.L. Phosphorus uptake by plants: from soil to cells. Plant Physiol. 116, 447–453 (1998).

    Article  CAS  Google Scholar 

  7. Hoffland, E., Findenegg, G.R. & Nelemans, J.A. Solubilization of rock phosphate by rape. 2. Local root exudation of organic acids as a response to P starvation. Plant Soil 113, 161–165 (1989).

    Article  CAS  Google Scholar 

  8. Dinkelaker, B., Romheld, B. & Marshner, H. Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupine (Lupinus albus L.). Plant Cell Environ. 12, 285–292 (1989).

    Article  Google Scholar 

  9. Dinkelaker, B., Hengeler, B. & Marshner, H. Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183–200 (1995).

    Article  Google Scholar 

  10. Zhang, F.S., Ma, J. & Cao, Y.P. Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish ( Rhaganus sativus L.) and rape (Brassica napus L.). Plant Soil 196, 261–264 (1997).

    Article  CAS  Google Scholar 

  11. Marschner, H. Mineral nutrition of higher plants . (Academic Press, London; 1995).

    Google Scholar 

  12. de la Fuente, J.M., Ramirez-Rodriguez, V., Cabrera-Ponce, J.L. & Herrera-Estrella, L. Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276, 1566–1568 (1997).

    Article  CAS  Google Scholar 

  13. Tyler, G. Inability to solubilize phosphate in limestone soils—key factor controlling calcifuge habit of plants. Plant Soil 145, 65–70 (1992).

    Article  CAS  Google Scholar 

  14. Pate, J.S. The mycorrhizal association: just one of many nutrient-acquiring specializations in natural ecosystems. Plant Soil 159, 1–10 (1994).

    Article  CAS  Google Scholar 

  15. Bolan, N.S. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134, 189–207 (1991).

    Article  CAS  Google Scholar 

  16. Murashige, T. & Skoog, F. A revised medium for a rapid growth and bioassay with tobacco tissue culture. Physiol. Plant. 15, 473–497 (1962).

    Article  CAS  Google Scholar 

  17. Srere, P. Citrate synthase. Methods Enzymol. 13, 3–11 (1969).

    Article  CAS  Google Scholar 

  18. Picha, H.D. Organic acid determination in sweet potatoes by HPLC. J. Agric. Food Chem. 33, 743–745 (1985).

    Article  CAS  Google Scholar 

  19. Murphy, J. & Riley, J.P. A modified single method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962).

    Article  CAS  Google Scholar 

  20. Phillips J.M. & Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–161 (1970).

    Article  Google Scholar 

Download references

Acknowledgements

We thank Fernanda Nieto, Verenice Ramirez, Omar Ocampo, and Victor Olalde for CS antibodies, mycorrhizal inoculum and technical advice. Drs. Gabriela Olmedo and June Simpson for critical reading of this manuscript. This work was supported in part by grants of the HHMI (75191-526901), the Rockefeller Foundation (AS 9644), and the European Commission (ERBIC-18C-960089) to L.H.E. J.L.B. is a CONACYT fellow No. 113732.

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Correspondence to Luis Herrera-Estrella.

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López-Bucio, J., de la Vega, O., Guevara-García, A. et al. Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18, 450–453 (2000). https://doi.org/10.1038/74531

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