The effects of nitrogen form on root morphological and physiological adaptations of maize, white lupin and faba bean under phosphorus deficiency

AoB PLANTS

Volumn 8, Issue , 2016, Pages

  Liu, Haitao ^a   Tang, Caixian ^b   Li, Chunjian ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

Low P availability; Organic acids; Rhizosphere; Root exudation; Root morphology; Species variation

Indexed keywords

EID: 85010670147     PISSN: None     EISSN: 20412851     Source Type: Journal    
DOI: 10.1093/aobpla/plw058     Document Type: Article

References (71)

1. Anghinoni I, Barber S. 1980. Phosphorus influx and growth characteristics of corn roots as influenced by phosphorus supply. Agronomy Journal 72:685-688.
2. Balemi T, Negisho K. 2012. Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. Journal of Soil Science and Plant Nutrition 12:547-562.
3. Barber SA. 1995. Soil nutrient bioavailability: a mechanistic approach. New York: John Wiley.
4. Bhadoria PS, Steingrobe B, Claassen N, Liebersbach H. 2002. Phosphorus efficiency of wheat and sugar beet seedlings grown in soils with mainly calcium, or iron and aluminium phosphate. Plant and Soil 246:41-52.
5. Brewster J, Tinker P. 1972. Nutrient flow rates into roots. Soils and Fertilizers 35:355-359.
6. Calderón-Vázquez C, Sawers RJ, Herrera-Estrella L. 2011. Phosphate deprivation in maize: genetics and genomics. Plant Physiology 156:1067-1077.
7. Claassen N, Jungk A. 1984. Bedeutung der Kaliumaufnahmerate, Wurzelwachstum und Wurzelhaare fü r das Kaliumaneignungsvermögen verschiedener Pflanzenarten. Zeitschrift Fuer Pflanzenernährung Und Bodenkungde 147:276-289.
8. Clark RB. 1982. Nutrient solution growth of sorghum and corn in mineral nutrition studies. Journal of Plant Nutrition 5:1039-1057.
9. Corrales I, Amenós M, Poschenrieder C, Barceló J. 2007. Phosphorus efficiency and root exudates in two contrasting tropical maize varieties. Journal of Plant Nutrition 30:887-900.
10. Deng Y, Chen K, Teng W, Zhan A, Tong Y, Feng G, Cui Z, Zhang F, Chen X. 2014. Is the inherent potential of maize roots efficient for soil phosphorus acquisition? PloS One 9:e90287.
11. Dinkelaker B, Römheld V, Marschner H. 1989. Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell and Environment 12:285-292.
12. Fernández MC, Belinque H, Boem FHG, Rubio G. 2009. Compared phosphorus efficiency in soybean, sunflower and maize. Journal of Plant Nutrition 32:2027-2043.
13. Fernández MC, Rubio G. 2015. Root morphological traits related to phosphorus-uptake efficiency of soybean, sunflower, and maize. Journal of Plant Nutrition and Soil Science 178:807-815.
14. Föhse D, Claassen N, Jungk A. 1988. Phosphorus efficiency of plants: I. External and internal P requirement and P uptake efficiency of different plant species. Plant and Soil 110:101-109.
15. Gahoonia TS, Nielsen NE. 1992. The effects of root-induced pH changes on the depletion of inorganic and organic phosphorus in the rhizosphere. Plant and Soil 143:185-191.
16. Gardner W, Barber D, Parbery D. 1983. The acquisition of phosphorus by Lupinus albus L. Plant and Soil 70:107-124.
17. Gardner W, Parbery D, Barber D. 1982. The acquisition of phosphorus by Lupinus albus L. Plant and Soil 68:19-32.
18. Gaume A, Mächler F, De León 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 and Soil 228:253-264.
19. George T, Gregory P, Robinson J, Buresh R. 2002. Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant and Soil 246:65-73.
20. Gerke J, Römer W, Jungk A. 1994. The excretion of citric and malic acid by proteoid roots of Lupinus albus L.; effects on soil solution concentrations of phosphate, iron, and aluminum in the proteoid rhizosphere in samples of an oxisol and a luvisol. Zeitschrift Für Pflanzenernährung Und Bodenkunde 157:289-294.
21. Hinsinger P. 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237:25-41.
22. Hinsinger P, Plassard C, Tang C, Jaillard B. 2003. Origins of rootmediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant and Soil 248:43-59.
23. Jaillard B, Plassard C, Hinsinger P. 2003. Measurements of Hp fluxes and concentrations in the rhizosphere. In: Rengel Z, eds. Handbook of soil acidity. New York: Dekker, 231-266.
24. Jakobsen I, Abbott L, Robson A. 1992. External hyphae of vesiculararbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytologist 120:371-380.
25. Krey T, Vassilev N, Baum C, Eichler-Löbermann B. 2013. Effects of long-term phosphorus application and plant-growth promoting rhizobacteria on maize phosphorus nutrition under field conditions. European Journal of Soil Biology 55:124-130.
26. Kummerová M. 1986. Localization of acid phosphatase activity in maize root under phosphorus deficiency. Biologia Plantarum 28: 270-274.
27. Lambers H, Clode PL, Hawkins HJ, Laliberte E, Oliveira RS, Reddell P, Shane MW, Stitt M, Weston P. 2015. Metabolic adaptations of the non-mycotrophic proteaceae to soils with low phosphorus. Annual Plant Reviews, Phosphorus Metabolism in Plants 48:289.
28. Lambers H, Finnegan PM, Laliberte E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ. 2011. Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiology 156:1058-1066.
29. Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrientacquisition strategies change with soil age. Trends in Ecology and Evolution 23:95-103.
30. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ. 2006. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98:693-713.
31. Li H, Shen J, Zhang F, Clairotte M, Drevon J, Le Cadre E, Hinsinger P. 2008. Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant and Soil 312:139-150.
32. Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS. 2007. Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of the National Academy of Sciences 104:11192-11196.
33. Li SM, Li L, Zhang FS, Tang C. 2004. Acid phosphatase role in chickpea/ maize intercropping. Annals of Botany 94:297-303.
34. Li Z, Xu C, Li K, Yan S, Qu X, Zhang J. 2012. Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biology 12:89.
35. 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 Science 167: 217-223.
36. Lynch JP, Ho MD. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269:45-56.
37. Lynch JP. 2007. Turner review no. 14. Roots of the second green revolution. Australian Journal of Botany 55:493-512.
38. Marschner H, Römheld V. 1983. In vivo measurement of rootinduced pH changes at the soil-root interface: effect of plant species and nitrogen source. Zeitschrift Fü r Pflanzenphysiologie 111:241-251.
39. Marschner P. 2012. Mineral nutrition of higher plants, 3rd edn. London: Academic Press.
40. McLachlan K. 1980. Acid phosphatase activity of intact roots and phosphorus nutrition in plants. 2. Variations among wheat roots. Crop and Pasture Science 31:441-448.
41. Mengel K, Kosegarten H, Kirkby EA, Appel T. 2001. Principles of plant nutrition. New York: Springer Science and Business Media.
42. Miller MH. 1974. Effects of nitrogen on phosphorus absorption by plants. In: Carson E, eds. The plant root and its environment. Charlottesville: University Press of Virginia, 643-668.
43. Mollier A, Pellerin S. 1999. Maize root system growth and development as influenced by phosphorus deficiency. Journal of Experimental Botany 50:487-497.
44. Neumann G, Martinoia E. 2002. Cluster roots-an underground adaptation for survival in extreme environments. Trends in Plant Science 7:162-167.
45. Neumann G, Massonneau A, Martinoia E, Römheld V. 1999. Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373-382.
46. Neumann G, Römheld V. 1999. Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant and Soil 211: 121-130.
47. Niu J, Chen F, Mi G, Li C, Zhang F. 2007. Transpiration, and nitrogen uptake and flow in two maize (Zea mays L.) inbred lines as affected by nitrogen supply. Annals of Botany 99:153-160.
48. Nuruzzaman M, Lambers H, Bolland MD, Veneklaas EJ. 2005a. Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant and Soil 271:175-187.
49. Nuruzzaman M, Lambers H, Bolland MD, Veneklaas EJ. 2005b. Phosphorus uptake by grain legumes and subsequently grown wheat at different levels of residual phosphorus fertiliser. Crop and Pasture Science 56:1041-1047.
50. Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KH, Bolland MD, Denton MD, Lambers H. 2010. Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant and Soil 331:241-255.
51. Paponov IA, Engels C. 2003. Effect of nitrogen supply on leaf traits related to photosynthesis during grain filling in two maize genotypes with different N efficiency. Journal of Plant Nutrition and Soil Science 166:756-763.
52. Plénet D, Mollier A, Pellerin S. 2000. Growth analysis of maize field crops under phosphorus deficiency. II. Radiation-use efficiency, biomass accumulation and yield components. Plant and Soil 224:259-272.
53. Raghothama K. 1999. Phosphate acquisition. Annual Review of Plant Biology 50:665-693.
54. Richardson AE, Hocking PJ, Simpson RJ, George TS. 2009. Plant mechanisms to optimise access to soil phosphorus. Crop and Pasture Science 60:124-143.
55. Schachtman DP, Reid RJ, Ayling SM. 1998. Phosphorus uptake by plants: from soil to cell. Plant Physiology 116:447-453.
56. Shen J. 1998. Separation and determination of low-molecularweight organic acids and Phenolic acids in root exudates. PhD Thesis, China Agricultural University, China.
57. Shen J, Tang C, Rengel Z, Zhang F. 2004. Root-induced acidification and excess cation uptake by N2-fixing Lupinus albus grown in phosphorus-deficient soil. Plant and Soil 260:69-77.
58. Soon Y, Kalra Y. 1995. Short communication: a comparison of plant tissue digestion methods for nitrogen and phosphorus analyses. Canadian Journal of Soil Science 75:243-245.
59. Sun J, Dai S, Wang R, Chen S, Li N, Zhou X, Lu C, Shen X, Zheng X, Hu Z, Zhang Z, Song J, Xu Y. 2009. Calcium mediates root Kp/Nap homeostasis in poplar species differing in salt tolerance. Tree Physiology 29:1175-1186.
60. Tang C, Barton L, McLay C. 1997. A comparison of proton excretion of twelve pasture legumes grown in nutrient solution. Animal Production Science 37:563-570.
61. Tang C, Conyers MK, Nuruzzaman M, Poile G, Li Liu D. 2011. Biological amelioration of subsoil acidity through managing nitrate uptake by wheat crops. Plant and Soil 338:383-397.
62. Tang C, Han XZ, Qiao YF, Zheng SJ. 2009. Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environmental and Experimental Botany 67:228-234.
63. Tang C, Rengel Z. 2003. Role of plant cation/anion uptake ratio in soil acidification. In: Rengel Z, eds. Handbook of soil acidity. New York: Dekker, 57-81.
64. Vlek P, Lüttger A, Manske G. 1996. The potential contribution of arbuscular mycorrhiza to the development of nutrient and water efficient wheat. In: Tanner DG, Payne TS, Abdalla OS, eds. The ninth regional wheat workshop for eastern, central and Southern Africa. Addis Ababa, Ethiopia: CIMMYT, 28-46.
65. Wang Z, Shen J, Zhang F. 2006. Cluster-root formation, carboxylate exudation and proton release of Lupinus pilosus Murr. as affected by medium pH and P deficiency. Plant and Soil 287: 247-256.
66. White PJ, Veneklaas EJ. 2012. Nature and nurture: the importance of seed phosphorus content. Plant and Soil 357:1-8.
67. Xu Y, Sun T, Yin LP. 2006. Application of non-invasive microsensing system to simultaneously measure both Hp and O2 fluxes around the pollen tube. Journal of Integrative Plant Biology 48: 823-831.
68. Yan H, Li K, Ding H, Liao C, Li X, Yuan L, Li C. 2011. Root morphological and proteomic responses to growth restriction in maize plants supplied with sufficient N. Journal of Plant Physiology 168:1067-1075.
69. Yu P, Li X, Yuan L, Li C. 2013. A novelmorphological response ofmaize (Zea mays) adult roots to heterogeneous nitrate supply revealed by a split-root experiment. Physiologia Plantarum150:133-144.
70. Zhang Y, Yu P, Peng Y, Li X, Chen F, Li C. 2012. Fine root patterning and balanced inorganic phosphorus distribution in the soil indicate distinctive adaptation of maize plants to phosphorus deficiency. Pedosphere 22:870-877.
71. Zhu J, Kaeppler SM, Lynch JP. 2005. Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant and Soil 270:299-310.