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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References
Bar-Yosef, B. In Plant roots, the hidden half. (eds Waisel, Y., Eschel, A., Kafkafi V.) 529–557 (Marcel Dekker, New York, NY; 1991).
www.Fertilizer.org. Fertilizer demand and crops. International Industry Assoc. Paris, France (1999).
Holford, I.C.R. Soil phosphorus: its measurements, and its uptake by plants. Aust. J. Soil Res. 35, 227–239 (1997).
Sharpley, A.N. Soil phosphorus dynamics: agronomic and environmental impacts. Ecol. Eng. 5, 261–279 (1995).
Loneragan, J.F. Plant nutrition in the 20th and perspectives for the 21st century. Plant Soil 196, 163–174 (1997).
Schachtman, D.P., Reid, R.J. & Ayling, S.L. Phosphorus uptake by plants: from soil to cells. Plant Physiol. 116, 447–453 (1998).
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).
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).
Dinkelaker, B., Hengeler, B. & Marshner, H. Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183–200 (1995).
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).
Marschner, H. Mineral nutrition of higher plants . (Academic Press, London; 1995).
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).
Tyler, G. Inability to solubilize phosphate in limestone soils—key factor controlling calcifuge habit of plants. Plant Soil 145, 65–70 (1992).
Pate, J.S. The mycorrhizal association: just one of many nutrient-acquiring specializations in natural ecosystems. Plant Soil 159, 1–10 (1994).
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).
Murashige, T. & Skoog, F. A revised medium for a rapid growth and bioassay with tobacco tissue culture. Physiol. Plant. 15, 473–497 (1962).
Srere, P. Citrate synthase. Methods Enzymol. 13, 3–11 (1969).
Picha, H.D. Organic acid determination in sweet potatoes by HPLC. J. Agric. Food Chem. 33, 743–745 (1985).
Murphy, J. & Riley, J.P. A modified single method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962).
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).
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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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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DOI: https://doi.org/10.1038/74531
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