Improving phosphorus efficiency in cereal crops: Is breeding for reduced grain phosphorus concentration part of the solution?

Frontiers in Plant Science

Volumn 4, Issue NOV, 2013, Pages

  Rose, Terry J ^a   Liu, Lei ^a   Wissuwa, Matthias ^b  

^a SOUTHERN CROSS UNIVERSITY   (Australia)

^b JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

Author keywords

Grain phosphorus; Nutrient use efficiency; Phosphorus cycle; Phosphorus utilization efficiency; Sustainable agriculture

Indexed keywords

EID: 84899620100     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00444     Document Type: Article

References (46)

1. Barraclough, P. B., Howarth, J. R., Jones, J., Lopez-Bellido, R., Parmar, S., Shepherd, C. E., et al. (2010). Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement. Eur. J. Agron. 33, 1-11. doi: 10.1016/j.eja.2010.01.005
2. Batten, G. D. (1992). A review of phosphorus efficiency in wheat. Plant Soil 146, 163-168. doi: 10.1007/BF00012009
3. Bi, J., Liu, Z., Lin, Z., Alim, A., Rehmani, M. I. A., Li, G., et al. (2012). Phosphorus accumulation in grains of japonica rice as affected by nitrogen fertilizer. Plant Soil 369, 231-240. doi: 10.1007/s11104-012-1561-4
4. Bolland, M. D. A., and Baker, M. J. (1988). High phosphorus concentrations in seed of wheat and annual medic are related to higher rates of dry matter production of seedlings and plants. Aust. J. Exp. Agric. 28, 765-770. doi: 10.1071/EA9880765
5. Bregitzer, P., and Raboy, V. (2006). Effects of four independent low-phytate mutations on barley agronomic performance. Crop Sci. 46, 1318-1322. doi: 10.2135/cropsci2005.09-0301
6. Bregitzer, P., Raboy, V., Obert D. E., Windes, J. M., and Whitmore, J. C. (2007). Registration of 'Herald' barley. Crop Sci. 47, 441-442. doi: 10.2135/cropsci2006.07.0480
7. Burnett, V. F., Newton, P. J., and Coventry, D. R. (1997). Effect of seed source and seed phosphorus content on the growth and yield of wheat in north-eastern Victoria. Aust. J. Exp. Agric. 37, 191-197. doi: 10.1071/EA96082
8. Calvo, M. S., and Uribarri, J. (2013). Contributions to total phosphorus intake: all sources considered. Semin. Dial. 26, 54-61. doi: 10.1111/sdi.12042
9. Carpenter, S. R., Caraco, N. F., Correll, D. L., Howarth, R. W., Sharpley, A. N., and Smith, V. H. (1998). Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. Appl. 8, 559-568. doi: 10.1890/1051-0761(1998)008[0559:NPOSWW]2.0.CO;2
10. Cordell, D., Drangert, J., and White, S. (2009). The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292-305. doi: 10.1016/j.gloenvcha.2008.10.009
11. Correll, D. L. (1998). The role of phosphorus in the eutrophication of receiving water: a review. J. Environ. Qual. 27, 261-266. doi: 10.2134/jeq1998.00472425002700020004x
12. de Marco, D. G. (1990). Effect of seed weight, and seed phosphorus and nitrogen concentrations on the early growth of wheat seedlings. Austr. J. Exp. Agric. 30, 545-549. doi: 10.1071/EA9900545
13. Derrick, J. W., and Ryan, M. H. (1998). Influence of seed phosphorus content on seedling growth in wheat: implications for organic and conventional farm management in South East Australia. Biol. Agric. Hortic. 16, 223-237.
14. Holm, J., Björck, I., Ostrowska, S., Eliasson, A. C., Asp N. G., Larsson, K., et al. (1983). Digestibility of amylose-lipid complexes in-vitro and in-vivo. Starch 35, 294-297. doi: 10.1002/star.19830350902
15. Kim, S. I., and Tai, T. H. (2011). Identification of genes necessary for wild-type levels of seed phytic acid in Arabidopsis thaliana using a reverse genetics approach. Mol. Genet. Genomics 286, 119-133. doi: 10.1007/s00438-011-0631-2
16. Kullenberg, D., Taylor, L. A., Schneider, M., and Massing, U. (2012). Health effects of dietary phospholipids. Lipids Health Dis. 11, 3. doi: 10.1186/1476-511X-11-3
17. Kumar, V., Sinha, A. K., Makkar, H. P. S., and Becker, K. (2010). Dietary roles of phytate and phytase in human nutrition: a review. Food Chem. 120, 945-959. doi: 10.1016/j.foodchem.2009.11.052
18. Liu, L., Waters, D. L. E., Rose, T. J., Bao, J., and King, G. J. (2013). Phospholipids in rice: significance in grain quality and health benefits: a review. Food Chem. 139, 1133-1145. doi: 10.1016/j.foodchem.2012.12.046
19. Lott, J. N. A., Bojarski, M., Kolasa, J., Batten, G. D., and Campbell, L. C. (2009). A review of the phosphorus content of dry cereal and legume crops of the world. Int. J. Agric. Resour. Govern. Ecol. 8, 351-370. doi: 10.1504/IJARGE.2009.032640
20. Lott, J. N. A., Kolasa, J., Batten, G. D., and Campbell, L. C. (2011). The critical role of phosphorus in world production of cereal grains and legume seeds. Food Sec. 3, 451-462. doi: 10.1007/s12571-011-0144-1
21. MacDonald, G. K., Bennett, E. M., Potter, P. A., and Ramankutty, N. (2011). Agronomic phosphorus imbalances across the world's croplands. Proc. Natl. Acad. Sci. U.S.A. 108, 3086-3091. doi: 10.1073/pnas.1010808108
22. McLaughlin, M. J., McBeath, T. M., Smernik, R., Stacey, S. P., Ajiboye, B., and Guppy, C. (2011). The chemical nature of P accumulation in agricultural soils-implications for fertiliser management and design: an Australian perspective. Plant Soil 349, 69-87. doi: 10.1007/s11104-011-0907-7
23. Meis, S. J., Fehr, W. R., and Schnebly, S. R. (2003). Seed source effect on field emergence of soybean lines with reduced phytate and raffinose saccharides. Crop Sci. 43, 1336-1339. doi: 10.2135/cropsci2003.1336
24. Noack, S. R., McLaughlin, M. J., Smernik, R. J., McBeath, T. M., and Armstrong, R. D. (2012). Crop residue phosphorus: speciation and potential bio-availability. Plant Soil 359, 375-385. doi: 10.1007/s11104-012-1216-1215
25. Ockenden, I., Dorsch, J. A., Reid, M. M., Lin, L., Grant, L. K., Raboy, V., et al. (2004). Characterization of the storage of phosphorus, inositol phosphate and cations in grain tissues of four barley (Hordeum vulgare L.) low phytic acid genotypes. Plant Sci. 167, 1131-1142. doi: 10.1016/j.plantsci.2004.06.008
26. Raboy, V. (2007). The ABCs of low-phytate crops. Nat. Biotech. 25, 874-875. doi: 10.1038/nbt0807-874
27. Raboy, V. (2009). Approaches and challenges to engineering seed phytate and total phosphorus. Plant Sci. 177, 281-296. doi: 10.1016/j.plantsci.2009.06.012
28. Richardson, A. E., Hocking, P. J., Simpson, R. J., and George, T. S. (2009). Plant mechanisms to optimise access to soil phosphorus. Crop Past. Sci. 60, 124-143. doi: 10.1071/CP07125
29. Richardson, A. E., Lynch, J. P., Ryan, P. R., Delhaize, E., Smith, F. A., Smith, S. E., et al. (2011). Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349, 121-156. doi: 10.1007/s11104-011-0950-4
30. Robinson, W. D., Carson, I., Ying, S., Ellis, K., and Plaxton, W. C. (2012). Eliminating the purple acid phosphatase AtPAP26 in Arabidopsis thaliana delays leaf senescence and impairs phosphorus remobilization. New Phytol. 196, 1024-1029. doi: 10.1111/nph.12006
31. Rose, T. J., Pariasca-Tanaka, J., Rose, M. T., Fukuta, Y., and Wissuwa, M. (2010). Genotypic variation in grain phosphorus concentration; and opportunities to improve P-use efficiency in rice. Field Crops Res. 119, 154-160. doi: 10.1016/j.fcr.2010.07.004
32. Rose, T. J., Pariasca-Tanaka, J., Rose, M. T., Mori, A., and Wissuwa, M. (2012). Seeds of doubt: re-assessing the impact of grain P concentrations on seedling vigor. J. Soil Sci. Plant Nutr. 175, 799-804. doi: 10.1002/jpln.201200140
33. Rose, T. J., Rengel, Z., Ma, Q., and Bowden, J. W. (2007). Differential accumulation patterns of phosphorus and potassium by canola cultivars compared to wheat. J. Plant Nutr. Soil Sci. 170, 404-411. doi: 10.1002/jpln.200625163
34. Rose, T. J., Rengel, Z., Ma, Q., and Bowden, J. W. (2008). Post-flowering supply of P, but not K, is required for maximum canola seed yields. Eur. J. Agron. 28, 371-379. doi: 10.1016/j.eja.2007.11.003
35. Rose, T. J., Rose, M. T., Pariasca-Tanaka, J., Heuer, S., and Wissuwa, M. (2011). The frustration with utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive? Front. Plant Nutr. 2:73. doi: 10.3389/fpls.2011.00073
36. Rose, T. J., and Wissuwa, M. (2012). "Rethinking internal phosphorus utilization efficiency (PUE): a new approach is needed to improve PUE in grain crops, " in Advances in Agronomy, Vol. 80, ed. D. L. Sparks (New York: American Society of Agronomy and Academic Press), 183-215.
37. Rouached, H., Stefanovic, A., Secco, D., Arpat, A. B., Gout, E., Bligny, R., et al. (2011). Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J. 65, 557-570. doi: 10.1111/j.1365-313X.2010.04442.x
38. Takeda, E., Sakamoto, K., Yokota, K., Shinohara, M., Taketani, Y., Morita, K., et al. (2002). Phosphorus supply per capita from food in Japan between 1960 and 1995. J. Nutr. Sci. Vitaminol. 48, 102-108. doi: 10.3177/jnsv.48.102
39. Takeda, E., Yamamoto, H., Yamanaka-Okumura, H., and Taketani, Y. (2012). Dietary phosphorus in bone health and quality of life. Nutr. Rev. 70, 311-321. doi: 10.1111/j.1753-4887.2012.00473.x
40. Veneklaas, E. J., Lambers, H., Bragg, J., Finnegan, P. M., Lovelock, C. E., Plaxton, W. C., et al. (2012). Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 195, 306-320. doi: 10.1111/j.1469-8137.2012.04190.x
41. Wardyn, B. M., and Russell, W. K. (2004). Resource allocation in a breeding program for phosphorus concentration in maize grain. Crop Sci. 44, 753-757. doi: 10.2135/cropsci2004.0753
42. Welch, A. A., Fransen, H., Jenab, M., Boutron-Ruault, M. C., Tumino, R., Agnoli, C., et al. (2009). Variation in intakes of calcium, phosphorus, magnesium, iron and potassium in 10 countries in the European Prospective Investigation into Cancer and Nutrition study. Eur. J. Clin. Nutr. 63, S101-S121. doi: 10.1038/ejcn.2009.77
43. White, P. J., and Veneklaas, E. J. (2012). Nature and nurture: the importance of seed phosphorus content. Plant Soil 357, 1-8. doi: 10.1007/s11104-012-1128-4
44. Willett, W. C., and Buzzard, M. (1998). "Nature of variation in diet, " in Nutritional Epidemiology, 2nd Edn, ed. W. C. Willett (New York: Oxford University Press), 33-49.
45. Ye, H., Zhang, X.-Q., Broughton, S., Westcott, S., Wu, D., Lance, R., et al. (2011). A nonsense mutation in a putative sulphate transporter gene results in low phytic acid barley. Funct. Integr. Genomics 11, 103-110. doi: 10.1007/s10142-011-0209-4
46. Zhu, Y.-G., and Smith, S. E. (2001). Seed phosphorus (P) content affects growth, and P uptake of wheat plants and their association with arbuscular mycorrhizal (AM) fungi. Plant Soil 231, 105-112. doi: 10.1023/A:1010320903592