Plant and Soil

, Volume 376, Issue 1–2, pp 151–163 | Cite as

Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits

  • Hongbo Li
  • Qinghua Ma
  • Haigang Li
  • Fusuo Zhang
  • Zed Rengel
  • Jianbo ShenEmail author
Regular Article


Background and aims

Roots have morphological plasticity to adapt to heterogeneous nutrient distribution in soil, but little is known about crop differences in root plasticity. The objective of this study was to evaluate root morphological strategies of four crop species in response to soil zones enriched with different nutrients.


Four crop species that are common in intercropping systems [maize (Zea mays L.), wheat (Triticum aestivum L.), faba bean (Vicia faba L.), and chickpea (Cicer arietinum L.)] and have contrasting root morphological traits were grown for 45 days under uniform or localized nitrogen and phosphorus supply.


For each species tested, the nutrient supply patterns had no effect on shoot biomass and specific root length. However, localized supply of ammonium plus phosphorus induced maize and wheat root proliferation in the nutrient-rich zone. Localized supply of ammonium alone suppressed the whole root growth of chickpea and maize, whereas localized phosphorus plus ammonium reversed (maize and chickpea ) the negative effect of ammonium. The localized root proliferation of chickpea in a nutrient-rich zone did not increase the whole root length and root surface area. Faba bean had no significant response to localized nutrient supply.


The root morphological plasticity is influenced by nutrient-specific and species-specific responses, with the greater plasticity in graminaceous (eg. maize) than leguminous species (eg. faba bean and chickpea).


Crop species Nutrient patches Nutrient-specific responses Root/shoot partitioning Root morphological plasticity 



This study was supported by the National Natural Science Foundation of China (NSFC) (Nos. 31330070, 30925024 and 31210103906), the Innovative Group Grant of the NSFC (No. 31121062), and the Program of Introducing International Advanced Agricultural Science and Technology of the Ministry of Agriculture of China (948 Program) (No. 2011-G18).


  1. Banik P, Midya A, Sarkar BK, Ghose SS (2006) Wheat and chickpea intercropping systems in an additive series experiment: Advantages and weed smothering. Eur J Agron 24:325–332CrossRefGoogle Scholar
  2. Ding X, Fu L, Liu C, Chen F, Hoffland E, Shen J, Zhang F, Feng G (2011) Positive feedback between acidification and organic phosphate mineralization in the rhizosphere of maize (Zea mays L.). Plant Soil 349(1–2):13–24CrossRefGoogle Scholar
  3. Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490CrossRefGoogle Scholar
  4. Drew MC, Saker LR (1978) Nutrient supply and the growth of the seminal root system in barley. III. Compensatory increases in growth of lateral roots and in rates of phosphate uptake in response to localized supply of phosphate. J Exp Bot 29:435–451CrossRefGoogle Scholar
  5. Drew MC, Saker LR, Ashley TW (1973) Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. J Exp Bot 24:1189–1202CrossRefGoogle Scholar
  6. Duncan WG, Ohlrogge AJ (1958) Principles of nutrient uptake from fertilizer bands II. Root development in the band. Agron J 50:605–608CrossRefGoogle Scholar
  7. Duncan WG, Ohlrogge AJ (1959) Principles of nutrient uptake from fertilizer bands: III. Band volume, concentration, and nutrient composition. Agron J 51:103–108CrossRefGoogle Scholar
  8. Eissenstat DM, Caldwell MM (1988) Seasonal timing of root growth in favorable microsites. Ecol 69:870–873CrossRefGoogle Scholar
  9. Fan MX, Mackenzie AE (1995) The toxicity of banded urea to corn growth and yield as influenced by triple superphosphate. Can J Soil Sci 75:117–122CrossRefGoogle Scholar
  10. Fan FL, Zhang FS, Song YN, Sun JH, Bao XG, Guo TW, Li L (2006) Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283:275–286CrossRefGoogle Scholar
  11. Farley RA, Fitter AH (1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J Ecol 87:688–696CrossRefGoogle Scholar
  12. Fitter AH (1994) Architecture and biomass allocation as components of the plastic response of root systems to soil heterogeneity. In: Hutchings MJ, John EA, Stewart AJA (eds) Exploitation of environmental heterogeneity by plants. Academic, San Diego, pp 305–322CrossRefGoogle Scholar
  13. Fransen B, de Kroon H (2001) Long-term disadvantages of selective root placement: Root proliferation and shoot biomass of two perennial grass species in a 2-year experiment. J Ecol 89:711–722CrossRefGoogle Scholar
  14. Fransen B, Blijjenberg J, de Kroon H (1999) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant Soil 211(2):179–189CrossRefGoogle Scholar
  15. Gerendás J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B (1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. J Plant Nutr Soil Sci 160(2):239–251Google Scholar
  16. Granato TC, Raper CD Jr (1989) Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. J Exp Bot 40:263–275PubMedCrossRefGoogle Scholar
  17. Gross KL, Pregitizer KS, Burton AJ (1995) Spatial variation in nitrogen availability in three successional plant communities. J Ecol 83:357–367CrossRefGoogle Scholar
  18. Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding K, Vitousek P, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010PubMedCrossRefGoogle Scholar
  19. He Y, Liao H, Yan X (2003) Localised supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248:247–256CrossRefGoogle Scholar
  20. He WM, Shen Y, Cornelissen JHC (2012) Soil nutrient patchiness and plant genotypes interact on the production potential and decomposition of root and shoot litter: evidence from short-term laboratory experiments with Triticum aestivum. Plant Soil 353:145–154CrossRefGoogle Scholar
  21. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24CrossRefGoogle Scholar
  22. Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57(2):401–411PubMedCrossRefGoogle Scholar
  23. Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640PubMedCrossRefGoogle Scholar
  24. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol 139:479–494CrossRefGoogle Scholar
  25. Hodge A, Robinson D, Griffiths BS, Fitter AH (1999) Why plants bother: Root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820CrossRefGoogle Scholar
  26. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Spatial and physical heterogeneity of N supply from soil does not influence N capture by two grass species. Funct Ecol 14:645–653CrossRefGoogle Scholar
  27. Hutchings MJ, de Kroon H (1994) Foraging in plants: The role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238CrossRefGoogle Scholar
  28. Hutchings MJ, John EA (2004) The effects of environmental heterogeneity on root growth and root/shoot partitioning. Ann Bot 94:1–8PubMedCrossRefGoogle Scholar
  29. Jackson RB, Caldwell MM (1993) Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–692CrossRefGoogle Scholar
  30. Jing J, Rui Y, Zhang F, Rengel Z, Shen J (2010) Localized application of phosphorus and ammonium improves growth of maize seedlings by stimulating root proliferation and rhizosphere acidification. Field Crop Res 119:335–364CrossRefGoogle Scholar
  31. Johnson HA, Biondini ME (2001) Root morphological plasticity and nitrogen uptake of 59 plant species from the Great Plains grasslands, U.S.A. Basic Appl Ecol 2:127–14CrossRefGoogle Scholar
  32. Johnson CM, Ulrich A (1959) Analytical methods for use in plant analysis. University of California, Agricultural Experiment Station, BerkeleyGoogle Scholar
  33. Li L, Yang SC, Li XL, Zhang FS, Christie P (1999) Interspecific complementary and competitive interactions between intercropped maize and faba bean. Plant Soil 212:105–114CrossRefGoogle Scholar
  34. Li L, Zhang FS, Li XL, Christie P, Sun JH, Yang SC, Tang CX (2003a) Interspecific facilitation of nutrient uptake by intercropped maize and faba bean. Nutr Cycl Agroecosyst 65:61–71CrossRefGoogle Scholar
  35. Li L, Tang C, Rengel Z, Zhang FS (2003b) Chickpea facilitates phosphorous uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248:297–303CrossRefGoogle Scholar
  36. Li SM, Li L, Zhang FS, Tang C (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot (Lond) 94:297–303CrossRefGoogle Scholar
  37. Li L, Sun J, Zhang FS, Guo T, Bao X, Smith FA, Smith SE (2006) Root distribution and interactions between intercropped species. Oecologia 147(2):280–290PubMedCrossRefGoogle Scholar
  38. 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. Proc Natl Acad Sci 104:11192–11196PubMedCrossRefGoogle Scholar
  39. Li HB, Zhang FS, Shen JB (2012) Contribution of root proliferation in nutrient-rich soil patches to nutrient uptake and growth of maize. Pedosphere 22(6):776–784CrossRefGoogle Scholar
  40. Miller MH, Ohlrogge AJ (1958) Principles of nutrient uptake from fertilizer bands. I. Effect of placement of nitrogen fertilizer on the uptake of band-placed phosphorus at different soil phosphorus levels. Agron J 58:95–97CrossRefGoogle Scholar
  41. Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H (2012) Interactive effects of nutrient heterogeneity and competition: Implications for root foraging theory? Funct Ecol 26:66–73CrossRefGoogle Scholar
  42. Moody PW, Aitken RL, Yo SA, Edwards DG, Bell LC (1995) Effect of banded fertilizers on soil solution composition and short-term root growth I. Ammonium sulphate, ammonium nitrate, potassium nitrate and calcium nitrate. Aust J Soil Res 33:673–687CrossRefGoogle Scholar
  43. Officer SJ, Dunbabin VM, Armstrong RD, Norton RM, Kearney GA (2009) Wheat roots proliferate in response to nitrogen and phosphorus fertilisers in Sodosol and Vertosol soils of south-eastern Australia. Aust J Soil Res 47:91–102CrossRefGoogle Scholar
  44. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127:635–674CrossRefGoogle Scholar
  45. Robinson D, Van Vuuren MMI (1998) Responses of wild plants to nutrient patches in relation to growth rate and life-form. In: Lambers H, Poorter H, Van Vuuren MMI (eds) Inherent variation in plant growth. Physiological mechanisms and ecological consequences. Backhuys Publishers, Leiden, pp 237–257Google Scholar
  46. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: From soil to cell. Plant Physiol 116:447–453PubMedCentralPubMedCrossRefGoogle Scholar
  47. Shen J, Mao D (2011) Research methodology of plant nutrition. China Agricultural University Press, BeijingGoogle Scholar
  48. Shen JB, Yuan LX, Zhang JL, Li HG, Bai ZH, Chen XP, Zhang WF, Zhang FS (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005PubMedCentralPubMedCrossRefGoogle Scholar
  49. Shen JB, Li CJ, Mi GH, Li L, Yuan LX, Jiang RF, Zhang FS (2013) Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J Exp Bot 64(5):1181–1192PubMedCrossRefGoogle Scholar
  50. Shu L, Shen J, Rengel Z, Tang C, Zhang F (2005) Growth medium and phosphorus supply affect cluster root formation and citrate exudation by Lupinus albus grown in a sand/solution split-root system. Plant Soil 276:85–94CrossRefGoogle Scholar
  51. Shu L, Shen J, Rengel Z, Tang C, Zhang F (2007a) Cluster root formation by Lupinus albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 30:271–288CrossRefGoogle Scholar
  52. Shu L, Shen J, Rengel Z, Tang C, Zhang F, Cawthray GR (2007b) Formation of cluster roots and citrate exudation by Lupinus albus in response to localized application of different phosphorus sources. Plant Sci 172:1017–1024CrossRefGoogle Scholar
  53. Sun H, Zhang F, Li L, Tang C (2002) The morphological changes of wheat genotypes as affected by the levels of localised phosphate supply. Plant Soil 245:233–238CrossRefGoogle Scholar
  54. Valizadeh GR, Rengel Z, Rate AW (2002) Role of phosphorus fertilizer banding and the ratio of nitrate ammonium on the uptake of phosphorus and wheat growth: A glasshouse study. Aust J Exp Agric 42:1095–1102CrossRefGoogle Scholar
  55. Valladares F, Sanchez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  56. van Vuuren MMI, Robinson D, Griffiths BS (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178:185–192CrossRefGoogle Scholar
  57. Vance CP, Uhde-stone C, Allan DL (2003) Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource. New Phytol 57:423–427CrossRefGoogle Scholar
  58. Watt M, Evans JR (2003) Phosphorus acquisition from soil by white lupin (Lupinus albus L.) and soybean (Glycine max L.), species with contrasting root development. Plant Soil 248:271–283CrossRefGoogle Scholar
  59. Weligama C, Tang C, Sale PWG, Conyers MK, Liu DL (2008) Localised nitrate and phosphate application enhances root proliferation by wheat and maximises rhizosphere alkalisation in acid subsoil. Plant Soil 312:101–115CrossRefGoogle Scholar
  60. Zhang FS, Li L (2003) Using competitive and facilitative interactions in intercropping systems enhances crop productivity and nutrient-use efficiency. Plant Soil 248:305–312CrossRefGoogle Scholar
  61. Zhang FS, Shen JB, Zhang JL, Zuo YM, Li L, Chen XP (2010) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: Implications for China. Adv Agron 107:1–32CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Hongbo Li
    • 1
  • Qinghua Ma
    • 1
  • Haigang Li
    • 1
  • Fusuo Zhang
    • 1
  • Zed Rengel
    • 2
  • Jianbo Shen
    • 1
    Email author
  1. 1.Centre for Resources, Environmental and Food Security, Department of Plant Nutrition, Key Laboratory of Plant-Soil Interactions, Ministry of EducationChina Agricultural UniversityBeijingPeople’s Republic of China
  2. 2.Soil Science & Plant Nutrition, School of Earth and Environment, The UWA Institute of AgricultureThe University of Western AustraliaCrawleyAustralia

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