Maize Under Phosphate Limitation

  • Carlos Calderón-Vázquez
  • Fulgencio Alatorre-Cobos
  • June Simpson-Williamson
  • Luis Herrera-Estrella


Phosphorus is one of the least available macronutrient for plants in soils, and is therefore considered to be a major constraint for plant growth and crop productivity. As a consequence, plants evolved a number a biochemical and developmental adaptations to combat this deficiency. In maize, such adaptations are based on a wide spectrum of mechanisms needed to increase the P uptake, assimilation and use efficiency. These mechanisms frequently act in parallel with a morphological plasticity in root architecture. Such adaptive strategies have been reported in several phosphate efficient genotypes, identified and selected from the large natural and man-made diversity found within the maize species. Advances in research have now begun to identify at the molecular level the adaptations evolved by maize to cope with Pi limitation. In this chapter we summarize the current research on the development of tolerant genotypes and the physiological, biochemical and molecular adaptations associated with low phosphate availability. Such knowledge will allows us to identify putative targets for breeding and opens the possibility to improve nutrient acquisition and productivity in maize and other cereals.


Quantitative Trait Locus Arbuscular Mycorrhizal Lateral Root Root Hair Seminal Root 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Akiyama, K., Matsuzaki, K., Hayashi, H. (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827.PubMedGoogle Scholar
  2. Alves, V., Parentoni, S., Vasconcellos, C., Bahia Filho, A., Pitta, G., Schaffert, R. (2001) Mechanisms of phosphorus efficiency in maize. In W Horst, ed, Plant Nutrition- Food Security and Sustainability of Agro-Ecosystems. Kluwer Academic Publishers, The Netherlands, pp 566–567.Google Scholar
  3. Andersson, M.X., Stridh, M.H., Larsson, K.E., Liljenberg, C., Sandelius, A.S. (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galac-tolipid digalactosyldiacylglycerol. FEBS Lett 537: 128–132.PubMedGoogle Scholar
  4. Anghinoni, I., Barber, S.A. (1980) Phosphorus influx and growth characteristics of corn roots as influenced by phosphorus supply. Agron J 172: 655–668.Google Scholar
  5. Baldwin, J.C., Karthikeyan, A.S., Raghothama, K.G. (2001) LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125: 728–737.PubMedGoogle Scholar
  6. Baligar, V., Pitta, G., Gama, E., Schaffert, R., Bahia Filho, A.d.C., Clark, R. (1997) Soil acidity effects on nutrient use efficiency in exotic maize genotypes. Plant Soil 192: 9–13.Google Scholar
  7. Bari, R., Datt Pant, B., Stitt, M., Scheible, W.R. (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141: 988–99.PubMedGoogle Scholar
  8. Bariola, P.A., Howard, C.J., Taylor, C.B., Verburg, M.T., Jaglan, V.D., Green, P.J. (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6: 673–685.PubMedGoogle Scholar
  9. Barry, D., Miller, M. (1989) Phosphorus nutritional requirement of maize seedlings for maximum yield. Agron J 81: 95–99.Google Scholar
  10. Bates, D., Lynch, J. (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low P availability. Plant Cell Environ 19: 529–538.Google Scholar
  11. Bates, T.R., Lynch, J.P. (2000a) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87: 964–970.Google Scholar
  12. Bates, T.R., Lynch, J.P. (2000b) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot 87: 958–963.Google Scholar
  13. Bhadoria, P., El Dessougi, H., Liebersbach, H., Claassen, N. (2004) Phosphorus uptake kinetics, size of root system and growth of maize and groundnut in solution culture. Plant Soil 262: 327–336.Google Scholar
  14. Bonser, A.M., Lynch, J., Snapp, S. (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132: 281–288.PubMedGoogle Scholar
  15. Bressan, W., Vasconcellos, C.A. (2002) Alteracoes morfológicas no sistema radicular do milho induzidas por fungos micorrízicos e fósforo. Pesq Agropec Brasil 37: 509–517.Google Scholar
  16. Bucher, M. (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173: 11–26.PubMedGoogle Scholar
  17. Cakmak, I. (2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247: 3–24.Google Scholar
  18. Chen, Z., Nimmo, G., Jenkins, G., Nimmo, H. (2007) BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J. 405(Pt 1): 191–198.PubMedGoogle Scholar
  19. Chiou, T.J., Liu, H., Harrison, M.J. (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J 25: 281–293.PubMedGoogle Scholar
  20. Corrales, I., Amenos, M., Poschenrieder, C., Barcelo, J. (2007) Phosphorus efficiency and root exudates in two contrasting tropical maize varieties. J Plant Nutr 30: 887–900.Google Scholar
  21. Da Silva, Á.E., Gabelman, W.H. (1992) Screening maize inbred lines for tolerance to low-P stress condition. Plant Soil 146: 181–187.Google Scholar
  22. Daram, P., Brunner, S., Persson, B.L., Amrhein, N., Bucher, M. (1998) Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206: 225–233.PubMedGoogle Scholar
  23. del Pozo, J.C., Allona, I., Rubio, V., Leyva, A., de la Pena, A., Aragoncillo, C., Paz-Ares, J. (1999) A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J 1 9: 579–589.PubMedGoogle Scholar
  24. Devaiah, B.N., Karthikeyan, A., Raghothama, K.G. (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143: 1789–801.Google Scholar
  25. Devaiah, B.N., Nagarajan, V.K., Raghothama, K.G. (2007b) Phosphate Homeostasis and Root Development in Arabidopsis Is Synchronized by the Zinc Finger Transcription Factor ZAT6. Plant Physiol 145: 147–159.Google Scholar
  26. Dietz, K.-J., Harris, G.C. (1997) Photosynthesis under nutrient deficiency. In M Pessarakli, ed, Handbook of Photosynthesis. Marcel Dekker, Inc., New York, USA, pp 951–975.Google Scholar
  27. Dooner, H.K., Robbins, T.P. and Jorgensen, R.A. (1991) Genetic and developmental control of anthocyanin biosynthesis. Annu Rev Genet 25: 173–199.PubMedGoogle Scholar
  28. Dowswell, C.R., Paliwal, R., Cantrell, R.P. (1996) Maize in the third world. Westview Press, Oxford, Great Britain.Google Scholar
  29. Duff, S.M., Moorhead, G.B., Lefebvre, D.D., Plaxton, W.C. (1989) Phosphate starvation inducible ‘Bypasses’ of adenylate and phosphate dependent glycolytic enzymes in brassica nigra suspension cells. Plant Physiol 90: 1275–1278.PubMedGoogle Scholar
  30. Duff, S.M.G., Sarath, G., Plaxton, W.C. (1994) The role of acid phosphatase in plant phosphorus metabolism. Physiol Plant 90: 791–800.Google Scholar
  31. Eckardt, N. (2005) Insights into pant cellular mechanisms: of phosphate transporters and arbuscular mycorrhizal infection. Plant Cell 17: 3213–3216.Google Scholar
  32. Englestad, P., Hellums, D.T. (1992) Water solubility of phosphate fertilizers: agronomic aspects–a literature review. In International Fertilizer Development Center (IFDC), Muscle Shoals, Alabama, USA.Google Scholar
  33. Essigmann, B., Guler, S., Narang, R.A., Linke, D., Benning, C. (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 1950–1955.PubMedGoogle Scholar
  34. Ezawa, T., Hayatsu, M., Saito, M. (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Mol Plant-Microbe Interact 18: 1046–1053.PubMedGoogle Scholar
  35. Fairhurst, T., Lefroy, R., Mutert, E. and Batjes, N. H. (1999). The important, distribution and causes of phosphorus deficiency as a constraint to crop production in the tropics. Agroforestry Forum 9 (4): 2–8.Google Scholar
  36. Fan, M., Zhu, J., Richards, C., Brown, K.M., Lynch, J.P. (2003) Physiological roles for aeren-chyma in phosphorus-stressed roots. Funct Plant Biol 30: 493–506.Google Scholar
  37. Fan, M., Bai, R., Zhao, X., Zhang, J. (2007) Aerenchyma formed under phosphorus deficiency contributes to the reduced root hydraulic conductivity in maize roots. J Integr Plant Biol 4 9: 598–604.Google Scholar
  38. FAO (1992) Maize in Human Nutrition. Food and Agriculture Organization of the United Nations (FAO), Rome, Italy.Google Scholar
  39. FAO (2007) Agro-MAPS: Global Spatial Database of Agricultural Land-use Statistics www.fao. org/landandwater/agll/agromaps/interactive/page.jspx.
  40. Fernández, S.M., Ramírez, R. (2000) Efecto de la fuente de fósforo sobre la morfología radical y la acumulación del elemento en siete líneas de maíz. Bioagro 12: 41–46.Google Scholar
  41. Fixen, P. (2002) Soil test levels in North America. Better Crops 86: 12–15.Google Scholar
  42. Fixen, P. (2003) Dinámica del fósforo en el suelo y en el suelo en relación al manejo de los ferti-lizantes fosfatados. In International Plant Nutrition Institute,
  43. Gaume, A., Mächler, F., De Leon, C., Narro, L., Frossard, E. (2001) Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228: 253–264.Google Scholar
  44. Gavito, M.E., Varela, L. (1995) Response of “criollo” maize to single and mixed species inocula of arbuscular mycorrhizal fungi. Plant Soil 176: 101–105.Google Scholar
  45. Gavito, M.E., Miller, M.H. (1998) Early phosphorus nutrition, mycorrhizae evelopment, dry matter partitioning and yield of maize. Plant Soil 199: 177–186.Google Scholar
  46. Glassop, D., Smith, S.E., Smith, F.W. (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222: 688–698.PubMedGoogle Scholar
  47. Granato, T., Raper, C. (1989) Proliferation of maize ( Zea mays L.) roots in response to localized supply of nitrate. J Exp Bot 40: 263–275.PubMedGoogle Scholar
  48. Grant, C., Bittman, S., Montrea, M., Plenchette, C., Morel, C. (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85: 3–14.Google Scholar
  49. Hajabbasi, M., Schumacher, T. (1994) Phosphorus effects on root growth and development in two maize genotypes. Plant Soil 158: 39–46.Google Scholar
  50. Halsted, M., Lynch, J. (1996) Phosphorus responses of C3 and C4 species. J Exp Bot 47: 497–505.Google Scholar
  51. Hammond, J.P., Broadley, M.R., White, P.J. (2004) Genetic responses to phosphorus deficiency. Ann Bot (Lond) 94: 323–332.Google Scholar
  52. Hardtke, C.S. (2006) Root development–branching into novel spheres. Curr Opin Plant Biol 9:66–71.PubMedGoogle Scholar
  53. Hernandez, G., Ramirez, M., Valdes-Lopez, O., Tesfaye, M., Graham, M.A., Czechowski, T., Schlereth, A., Wandrey, M., Erban, A., Cheung, F., Wu, H.C., Lara, M., Town, C.D., Kopka, J., Udvardi, M.K., Vance, C.P. (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144: 752–767.PubMedGoogle Scholar
  54. Herrera-Estrella, L. (1999) Transgenic plants for tropical regions: some considerations about their development and their transfer to the small farmer. Proc Natl Acad Sci USA 96: 5978 – 5981.PubMedGoogle Scholar
  55. Hinsinger, P. (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237: 173–195.Google Scholar
  56. Hochholdinger, F., Woll, K., Sauer, M., Dembinsky, D. (2004) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann Bot (Lond) 93: 359–368.Google Scholar
  57. Hodge, A. (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162: 9–24.Google Scholar
  58. Horst, W.J. (2000) Fitting maize into sustainable cropping systems on acid soils of the tropics. International Atomic Energy Agency-TECDOC-1159, ISSN 1011-4289, 47–59.Google Scholar
  59. Howeler, R., Sieverding, E., Saif, S. (1987) Practical aspects of mycorrhizal technology in some tropical crops and pastures. Plant Soil 100: 249–283.Google Scholar
  60. Huber, S., Edwards, G. (1975) Inhibition of phosphoenolpyruvate carboxylase from C4 plants by malate and aspartate. Can J Bot 53: 1925–1933.Google Scholar
  61. Iqbal, R.M., Iqbal Chauhan, H.Q. (2003) Relationship between different growth and yield parameters in maize under varying levels of phosphorus. J Biol Sci 3: 921–925.Google Scholar
  62. Jacob, J., Lawlor, D. (1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. J Exp Bot 42: 1003–1011.Google Scholar
  63. Jacob, J., Lawlor, D. (1993) In vivo photosynthetic electron transport does not limit photosyn-thetic capacity in phosphate-deficient sunflower and maize leaves. Plant Cell Environ 16: 785–795.Google Scholar
  64. Jungk, A., Asher, C., Edwards, D., Meyer, D. (1990) Influence of phosphate status on phosphate uptake kinetics of maize (Zea mays) and soybean (Glycine max). Plant Soil 124: 175–182.Google Scholar
  65. Kaeppler, S.M., Parke, J.L., Mueller, S.M., Senior, L., Stuber, C., Tracy, W.F. (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci 40: 358–364.Google Scholar
  66. Kothari, S., Marschner, H., Römheld, V. (1990) Direct and indirect effects of VA mycorrhizal fungi and rhizosphere microorganisms on acquisition of mineral nutrients by maize (Zea mays L.) in a calcareous soil. New Phytol 116: 637–645.Google Scholar
  67. Lafitte, H. (2001) Estreses abióticos que afectan al maíz. In RL Paliwal, G Granados H R Lafitte, AD Violic, JP Marathee, eds, El maíz en los trópicos. CIMMYT, Rome, Italy, pp. 95–106.Google Scholar
  68. Leakey, A.D., Uribelarrea, M., Ainsworth, E.A., Naidu, S.L., Rogers, A., Ort, D.R., Long, S.P. (2006) Photosynthesis, productivity, and yield of maize are not affected by open-air elevation of CO2 concentration in the absence of drought. Plant Physiol 140: 779–790.PubMedGoogle Scholar
  69. Li, D., Zhu, H., Liu, K., Liu, X., Leggewie, G., Udvardi, M., Wang, D. (2002) Purple acid phos-phatases of Arabidopsis thaliana. J Biol Chem 277: 27772–27781.PubMedGoogle Scholar
  70. Li, K., Xu, Z., Zhang, K., Yang, A., Zhang, J. (2006) Efficient production and characterization for maize inbred lines with low-phosphorus tolerance. Plant Sci 172: 255–264.Google Scholar
  71. Li, K., Xu, C., Zhang, K., Yang, A., Zhang, J. (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize ( Zea mays L.) plants. Proteomics 7: 1501–1512.PubMedGoogle Scholar
  72. Lim, J., Jung, J.W., Lim, C.E., Lee, M.H., Kim, B.J., Kim, M., Bruce, W.B., Benfey, P.N. (2005) Conservation and diversification of SCARECROW in maize. Plant Mol Biol 59: 619–30.PubMedGoogle Scholar
  73. Liu, C., Muchhal, U.S., Raghothama, K.G. (1997) Differential expression of TPSI1, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33: 867–874.PubMedGoogle Scholar
  74. Liu, C., Muchhal, U.S., Mukatira, U.T., Kononowicz, A.K., Raghothama, K.G. (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116: 91–99.PubMedGoogle Scholar
  75. Liu, Y., Mi, G., Chen, F., Zhang, J., Zhang, F. (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci 167: 217–223.Google Scholar
  76. Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, L., Nieto-Jacobo, M.F., Simpson, J., Herrera-Estrella, L. (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129: 244–256.PubMedGoogle Scholar
  77. Lynch, J. (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13.PubMedGoogle Scholar
  78. Lynch, J.P. (1998) The role of nutrient efficient crops in modern agriculture. J Crop Prod 1: 241–264.Google Scholar
  79. Lynch, J.P., Brown, K.M. (2001) Topsoil Foraging: an architectural adaptation to low phosphorus availability. Plant Soil 237: 225–237.Google Scholar
  80. Lynch, J.P., Ho, M.D. (2005) Rhizoeconomics: carbon costs of phosphorus acquisition. Plant Soil 269: 45–56.Google Scholar
  81. Ma, Z., Bielenberg, D., Brown, K., Lynch, J. (2001a) Regulation of root hair density by P availability in Arabidopsis thaliana. Plant Cell Environ 24: 459–467.Google Scholar
  82. Ma, Z., Walk, T., Marcus, A., Lynch, J. (2001b) Morphological synergism in root hair length, density, initiation and geometry for P acquisition in Arabidopsis thaliana: a modeling approach. Plant Soil 236: 221–235.Google Scholar
  83. Ma, Z., Baskin, T., Brown, K., Lynch, J.P. (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol. 131: 1381–1390.PubMedGoogle Scholar
  84. Marschner, H. (1995) Mineral Nutrition in Plants, 2nd Ed. Academic Press, San Diego, CA.Google Scholar
  85. McCully, M., Canny, M. (1988) Pathways and processes of water and nutrient movement in roots. Plant Soil 111: 159–170.Google Scholar
  86. Ming, Z., Wen, J., Ishill, R., Li, C. (2006) Genotypic differences in photosynthesis and dynamic characteristics of NPQ in maize. Asian J Plant Sci 5: 709–712.Google Scholar
  87. Misson, J., Raghothama, K.G., Jain, A., Jouhet, J., Block, M.A., Bligny, R., Ortet, P., Creff, A., Somerville, S., Rolland, N., Doumas, P., Nacry, P., Herrerra-Estrella, L., Nussaume, L., Thibaud, M.C. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102: 11934–11939.PubMedGoogle Scholar
  88. Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A.S., Raghothama, K.G., Baek, D., Koo, Y.D., Jin, J.B., Bressan, R.A., Yun, D.J., Hasegawa, P.M. (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102; 7760–5.PubMedGoogle Scholar
  89. Mollier, A., Pellerin, S. (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50: 487–497.Google Scholar
  90. Morcuende, R., Bari, R., Gibon, Y., Zheng, W., Pant, B.D., Blasing, O., Usadel, B., Czechowski, T., Udvardi, M.K., Stitt, M., Scheible, W.R. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30: 85–112.PubMedGoogle Scholar
  91. Morris, M.L., Lopez-Pereira, M.A. (1999) Impacts of maize breeding research in Latin America, 1966–1997. International Maize and Wheat Improvement Center, Mexico City (Mexico). Economics Program Report. Mexico City (Mexico). ISBN: 970-648-034-X.Google Scholar
  92. Nagy, R., Vasconcelos, M.J., Zhao, S., McElver, J., Bruce, W., Amrhein, N., Raghothama, K.G., Bucher, M. (2006) Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.). Plant Biol (Stuttg) 8: 186–197.Google Scholar
  93. Nakajima, K., Benfey, P.N. (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14 Suppl, S265–76.Google Scholar
  94. Nandi, S., Pant, R., Nissen, P. (1987) Multiphasic uptake of phosphate by corn roots. Plant Cell Environ 10: 463–474.Google Scholar
  95. Natr, L. (1992) Mineral nutrients-a ubiquitous stress factor for photosynthesis. Photosynthetica 27: 271–294.Google Scholar
  96. Neumann, G., Römheld, V. (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211: 121–130.Google Scholar
  97. Nielsen, N.E., Barber, S.A. (1978) Differences among genotypes of corn in the kinetics of P uptake. Agron J 70: 695–698.Google Scholar
  98. Nielsen, T., Krapp, A., Roper-Schwarz, U., Stitt, M. (1998) The sugar mediated regulation encoding the small subunit of Rubisco and the regulatory subunit of ADP glucosa pyrophosphory-lase is modified by phosphate and nitrogen. Plant, Cell Environ 21: 443–454.Google Scholar
  99. Paszkowski, U., Boller, T. (2002) The growth defect of lrt1, a maize mutant lacking lateral roots, can be complemented by symbiotic fungi or high phosphate nutrition. Planta 214: 584–590.PubMedGoogle Scholar
  100. Pellerin, S., Mollier, A., Plenet, D. (2000) Phosphorus Deficiency affects the rate of emergence and number of maize adventitious nodal roots. Agron J 92: 690–697.Google Scholar
  101. Pieters, A.J., Paul, M.J., Lawlor, D.W. (2001) Low sink demand limits photosynthesis under Pi deficiency. J Exp Bot 52: 1083–1091.PubMedGoogle Scholar
  102. Pingali, P.L., Pandey, S. (2001) Part 1: Meeting world maize needs: technological opportunities and priorities for the public sector. In PL Pingali, ed, CIMMYT 1999–2000 World Maize Facts and Trends. Meeting World Maize Needs: Technological Opportunities and Priorities for the Public Sector. CIMMYT, Mexico, D. F., pp 1–24.Google Scholar
  103. Plénet, D., Etchebest, S., Mollier, A., Pellerin, S. (2000a) Growth analysis of maize field crops under phosphorus deficiency. I. Leaf Growth. Plant Soil 223: 117–130.Google Scholar
  104. Plénet, D., Mollier, A., Pellerin, S. (2000b) Growth analysis of maize field crops under phosphorus deficiency. II. Radiation-use efficiency, biomass accumulation and yield components. Plant Soil 224: 259–272.Google Scholar
  105. Poirier, Y. and Bucher, M. (2002) Phosphate transport and homeostasis in Arabidopsis. In C Somerville, E Meyerowitz, eds., The Arabidopsis Book. Vo l 2007. American Society of Plant Biologists, Rockville MD, pp. DOI: 10.1199/tab.0024,
  106. Raghothama, K.G. (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665–693.PubMedGoogle Scholar
  107. Raghothama, K.G., Karthikeyan, A.S. (2005) Phosphate acquisition. Plant Soil 274: 37–49.Google Scholar
  108. Ramírez, R. (2006) Eficiencia del uso del fósforo de la roca fosfórica por cultivares de maíz. Interciencia 31: 45–49.Google Scholar
  109. Rao, I., Friesen, D., Osaki, M. (1995) Plant adaptation to phosphorus-limited tropical soils. In M Pessarakli, ed, Handbook of Plant and Crop Physiology. Marcel Dekker, Inc., New York, USA, pp 61–95.Google Scholar
  110. Rao, I.M., Arulanantham, A.R., Norman, T. (1989) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. Plant Physiol 90: 820–826.PubMedGoogle Scholar
  111. Reiter, R., Coors, J., Sussman, M., Gabelman, W. (1991) Genetic analysis of tolerance to low-phosphorus stress in maize using restriction fragment length polymorphisms. Theor Appl Genet 82: 561–568.Google Scholar
  112. Reymond, M., Svistoonoff, S., Loudet, O., Nussame, L., Desnos, T. (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29: 115–125(111).PubMedGoogle Scholar
  113. Robinson, D. (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127: 635–674.Google Scholar
  114. Rubio, V., Linhares, F., Solano, R., Martin, A.C., Iglesias, J., Leyva, A., Paz-Ares, J. (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Dev 15: 2122–33.Google Scholar
  115. Sachay, J., Wallace, R., Johns, M. (1991) Phosphate stress response in hydroponically grown maize. Plant Soil 132: 85–90.Google Scholar
  116. Sanchez-Calderon, L., Lopez-Bucio, J., Chacon-Lopez, A., Cruz-Ramirez, A., Nieto-Jacobo, F., Dubrovsky, J.G., Herrera-Estrella, L. (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174–184.PubMedGoogle Scholar
  117. Schaffert, R., Alves, V., Parentoni, S., Raghothama, K. (2000) Genetic control of phosphorus uptake and utilization efficiency in maize and sorghum under marginal soil conditions. In JM Ribaut, D Poland, eds, Molecular Approaches for the Genetic Improvement of Cereals for Stable Production in Water-Limited Environments. A Strategic Planning Workshop, 21–25 Jun 1999. CIMMYT, El Batan, Texcoco, Mexico, pp 79–85.Google Scholar
  118. Shenoy, V., Kalagudi, G. (2005) Enhancing plant phosphorus use efficiency for sustainable cropping. Biotechnol Adv 23: 501–513.PubMedGoogle Scholar
  119. Sierra, J., Noël, C., Dufour, L., Ozier-Lafontaine, H., Welcker, C., Desfontaines, L. (2003) Mineral nutrition and growth of tropical maize as affected by soil acidity. Plant Soil 252: 215–226.Google Scholar
  120. Stryker, R., Gilliam, J., Jackson, W. (1974) Non uniform phosphorus distribution in the root zone of corn: growth and phosphorus uptake. Soil Sci Soc Am Proc 38: 334–340.Google Scholar
  121. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., Nussaume, L., Desnos, T. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39: 792–796.PubMedGoogle Scholar
  122. Theodorou, M.E., Plaxton, W.C. (1993) Metabolic Adaptations of Plant Respiration to Nutritional Phosphate Deprivation. Plant Physiol 101: 339–344.PubMedGoogle Scholar
  123. Torres de Toledo Machado, C., Cangiani Furlani, A.M. (2004) Kinetics of phosphorus uptake and root morphology of local and improved varieties of maize. Sci Agric (Piracicaba, Braz.) 61: 69–76.Google Scholar
  124. Tu, S., Cananaugh, J., Boswell, R. (1990) Phosphate uptake by excised maize root tips studied by in vivo 31P nuclear magnetic resonance spectroscopy. Plant Physiol 93: 778–784.PubMedGoogle Scholar
  125. Uhde-Stone, C., Zinn, K.E., Ramirez-Yanez, M., Li, A., Vance, C.P., Allan, D.L. (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131: 1064–1079.PubMedGoogle Scholar
  126. Usuda, H., Shimogawara, K. (1991) Phosphate deficiency in maize. I. Leaf phosphate status, growth, photosynthesis and carbon partitioning. Plant Cell Physiol 32: 497–504.Google Scholar
  127. Vance, C.P., Uhde-Stone, C., Allan, D.L. (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157: 423–447.Google Scholar
  128. Varney, G., Canny, M. (1993) Rates of water uptake into the mature roots system of maize plants. New Phytol 123: 775–786.Google Scholar
  129. Vieten, A., Sauer, M., Brewer, P.B., Friml, J. (2007) Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci 12: 160–8.PubMedGoogle Scholar
  130. von Uexküll, H.R., Mutert, E. (1995) Global extent, development and economic impact of acid soils. Plant Soil 171: 1–15.Google Scholar
  131. Wang, X., Canny, M., McCully, M. (1991) The water status of the roots of soil-grown maize in relation to the maturity of their xylem. Physiol Plant 82: 157–162.Google Scholar
  132. Wang, X., McCully, M., Canny, M. (1994) The branch roots of Zea. IV. The maturation and openness of xylem conduits in first-order branches of soil-grown roots. New Phytol 126: 21–29.Google Scholar
  133. Wasaki, J., Yonetani, R., Shinano, T., Kai, M., Osaki, M. (2003) Expression of the OsPI1 gene, cloned from rice roots using cDNA microarray, rapidly responds to phosphorus status. New Phytol 158: 239–248.Google Scholar
  134. Wasaki, J., Shinano, T., Onishi, K., Yonetani, R., Yazaki, J., Fujii, F., Shimbo, K., Ishikawa, M., Shimatani, Z., Nagata, Y., Hashimoto, A., Ohta, T., Sato, Y., Miyamoto, C., Honda, S., Kojima, K., Sasaki, T., Kishimoto, N., Kikuchi, S., Osaki, M. (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57: 2049–2059.PubMedGoogle Scholar
  135. Weisbach, C., Tiessen, H., Jimenez-Osornio, J.J. (2002) Soil fertility during shifting cultivation in the tropical Karst soils of Yucatan. Agronomie 22: 253–263.Google Scholar
  136. Wen, T., Schnable, P. (1994) Analysis of mutant of three genes that influence root hair development in Zea mays (Graminae) suggest that root hairs are dispensable. Am J Bot 81: 833–842.Google Scholar
  137. Williamson, L.C., Ribrioux, S.P., Fitter, A.H., Leyser, H.M. (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875–882.PubMedGoogle Scholar
  138. Wright, D.P., Scholes, J.D., Read, D.J., Rolfe, S.A. (2005) European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection. New Phytol 167: 881–896.PubMedGoogle Scholar
  139. Wu, P., Ma, L., Hou, X., Wang, M., Wu, Y., Liu, F., Deng, X. (2003) Phosphate starvation triggers distinct alterations of genome expression in arabidopsis roots and leaves. Plant Physiol 132: 1260–1271.PubMedGoogle Scholar
  140. Xie, Q., Frugis, G., Colgan, D., Chua, N.H. (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Dev 14: 3024–36.Google Scholar
  141. Xie, Q., Guo, H.S., Dallman, G., Fang, S., Weissman, A.M., Chua, N.H. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419: 167–170.PubMedGoogle Scholar
  142. Yi, K., Wu, Z., Zhou, J., Du, L., Guo, L., Wu, Y., Wu, P. (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138: 2087–96.PubMedGoogle Scholar
  143. Zhu, J., Lynch, J.P. (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct Plant Biol 31: 949–958.Google Scholar
  144. Zhu, J., Kaeppler, S., Lynch, J. (2005a) Topsoil foraging and phosphorus acquisition efficiency in maize ( Zea mays). Funct Plant Biol 32: 749–762.Google Scholar
  145. Zhu, J., Kaeppler, S.M., Lynch, J.P. (2005b) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270: 299–310.Google Scholar
  146. Zhu, J., Kaeppler, S.M., Lynch, J.P. (2005c) Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor Appl Genet 111: 688–695.Google Scholar
  147. Zhu, J., Mickelson, S., Kaeppler, S., Lynch, J. (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theor Appl Genet 113: 1–10.PubMedGoogle Scholar

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© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  • Carlos Calderón-Vázquez
  • Fulgencio Alatorre-Cobos
  • June Simpson-Williamson
  • Luis Herrera-Estrella

There are no affiliations available

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