Plant Growth Regulation

, Volume 87, Issue 1, pp 55–67 | Cite as

The root nitrogen uptake response to partial nitrogen stress is related to previous nutritional status

  • Xiaoli Niu
  • Tiantian HuEmail author
  • Fucang Zhang
  • Aiwang Duan
  • Jiyang Zhang
Original paper


We investigated the dynamics and factors influencing the N uptake capacity in two sub-root systems of maize seedlings under partial N stress. Maize seedlings were grown in split-root containers containing nutrient solutions. Two N application conditions prior to partial N stress (full-strength N (4.0 mM): CP; N stress: SP) were considered. Thus, two experiments were conducted: (A) four treatments: CPNc, CPN2, CPN1 and CPN0, in which half of the root system was exposed to 4.0 mM, 2 mM, 1 mM and 0 mM N (CPNc–c, CPN2–2, CPN1–1 and CPN0–0), respectively, and the other half received full-strength N (CPNc–c, CPN2–c, CPN1–c and CPN0–c); (B) four treatments: SPNc, SPN2, SPN1 and SPN0, in which both sub-root systems received 4.0 mM, 2 mM, 1 mM and 0 mM N for 6 days, respectively, after which half of the root system was maintained at original N level (SPNc–c, SPN2–2, SPN1–1 and SPN0–0) and the other half received full-strength N (SPNc–c, SPN2–c, SPN1–c and SPN0–c). At 0.25 days after treatment (DAT), CPN2–c and CPN1–c enhanced N inflow rates (Iroot), whereas CPN0–c decreased it by 27.3% compared with CPNc–c, Iroot in CPN2–c, CPN1–c and CPN0–c was uniformly enhanced at 1 DAT, but were only enhanced in CPN0–c at 5 DAT compared with CPNc–c. In contrast, SPN1–c had a significantly increased Iroot by 10.52% compared with SPNc–c, although other treatments showed a negative effect on Iroot at 0.25 DAT. At 1 and 5 DAT, Iroot in SPN2–c, SPN2–2, SPN1–c, SPN1–1 and SPN0–c were significantly lower than that in SPNc–c. Furthermore, CP significantly enhanced Iroot in non-stressed sub-roots compared with SP. Additionally, CPN2 improved shoot dry mass and N use efficiency even under SPN2. Thus, N uptake capacity in each sub-root zone varied not only depending on the severity and duration of the N stress, but was also related to the N status prior to partial N stress. Moreover, the occurrence and disappearance of the root compensatory effect were delayed with increasing N stress severity. A higher compensatory effect developed following CP, even under CPN0.


Root N inflow rate N use efficiency N stress severity Previous nutritional status Partial root system Maize 



This work was funded by research grants from the National Natural Science Foundation of China (51709263, 51079124), Central Public-interest Scientific Institution Basal Research Fund (Farmland Irrigation Research Institute, CAAS, FIRI2016-01), and Special Fund for Agro-scientific Research in the Public Interest (201503130).

Supplementary material

10725_2018_451_MOESM1_ESM.tif (392 kb)
Supplementary material 1 (TIF 392 KB). Supplementary Fig. S1: Relative root area on that of CPNc-c or SPNc-c under different previous N status. To investigate the effects of N status prior to partial N stress, the relative amounts in all treatments compared with the control were calculated (i.e., CPN2/CPNc, CPN1/CPNc, CPN0/CPNc, SPN2/SPNc, SPN1/SPNc, SPN0/SPNc) for experiment A (CP) and B (SP). Error bars indicate standard deviation of mean (n=3). Using the Tukey HSD test with P<0.05, the letters a, b, c and d indicate significant difference between lines. The symbols represent as in Fig. 2, 3. The statistics for CPN2-c, CPN1-c, CPN0-c, SPN2-c, SPN1-c and SPN0-c are: 0 DAT: a, a, a, b, c, d; 0.25 DAT: a, a, b, b, c, d; 0.5 DAT: a, b, c, d, e, e; 1 DAT: b, a, a, c, d, e; 3 DAT: a, ab, a, b, c, d; 5 DAT: a, b, b, b, c, d; 7 DAT: a, c, c, d, d, e; 9 DAT: a, bc, c, b, d, e, respectively.
10725_2018_451_MOESM2_ESM.tif (2.1 mb)
Supplementary material 2 (TIF 2105 KB). Supplementary Fig. S2: Relative plant N accumulation (A) and N concentration (B) on that of CPNc or SPNc under different previous nutrition status at 0.5 DAT. To investigate the effects of N status prior to partial N stress, the relative amounts in all treatments compared with the control were calculated (i.e., CPN2/CPNc, CPN1/CPNc, CPN0/CPNc, SPN2/SPNc, SPN1/SPNc, SPN0/SPNc) for experiment A (CP) and B (SP). Error bars indicate standard deviation of mean (n=3). Different letters indicate significant difference between different treatments for shoot or all sub-roots (p<0.05).The symbols represent as in Fig. 2, 3.


  1. Abdellaoui A, Talouizte A (2001) Effect of previous nitrogen starvation on NO3 and NH4 + uptake and assimilation associated with the endogenous soluble carbohydrate utilization in Moroccan wheat seedlings. J Plant Nutr 24:1995–2007CrossRefGoogle Scholar
  2. Anandacoomaraswamy A, De Costa W, Tennakoon P, Van der Werf A (2002) The physiological basis of increased biomass partitioning to roots upon nitrogen deprivation in young clonal tea (Camellia sinensis (L.) O. Kuntz). Plant Soil 238:1–9CrossRefGoogle Scholar
  3. Balazadeh S, Schildhauer J, Araujo WL, Munne-Bosch S, Fernie AR, Proost S, Humbeck K, Mueller-Roeber B (2014) Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J Exp Bot 65:3975–3992CrossRefGoogle Scholar
  4. Bliss KM (2001) Impact of nutrient heterogeneity on plant response and competition in coastal plain species. PhD thesis, Virginia Tech, Blacksburg, VAGoogle Scholar
  5. Bremner JM, Mulvaney CS (1982) Nitrogen—total. In: Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy, Madison, pp 595–624Google Scholar
  6. Cai J, Jiang D, Liu F, Dai T, Cao W (2011) Effects of split nitrogen fertilization on post-anthesis photoassimilates, nitrogen use efficiency and grain yield in malting barley. Acta Agriculturae Scandinavica Sect B-Soil Plant Sci 61:410–420CrossRefGoogle Scholar
  7. De La Rocha CL, Terbrüggen A, Hohn S, Völker C (2010) Response to and recovery from nitrogen and silicon starvation in Thalassiosira weissilogii: growth rates, nutrient uptake and C, Si and N content per cell. Mar Ecol Prog Ser 412:57–68CrossRefGoogle Scholar
  8. Ding L, Li Y, Gao L, Lu Z, Wang M, Ling N, Shen Q, Guo S (2018) Aquaporin expression and water transport pathways inside leaves are affected by nitrogen supply through transpiration in rice plants. Int J Mol Sci 19:256CrossRefGoogle Scholar
  9. Fernandes AM, Soratto RP, Gonsales JR (2014) Root morphology and phosphorus uptake by potato cultivars grown under deficient and sufficient phosphorus supply. Sci Hortic 180:190–198CrossRefGoogle Scholar
  10. Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68CrossRefGoogle Scholar
  11. Fort F, Cruz P, Catrice O, Delbrut A, Luzarreta M, Stroia C, Jouany C (2015) Root functional trait syndromes and plasticity drive the ability of grassland Fabaceae to tolerate water and phosphorus shortage. Environ Exp Bot 110:62–72CrossRefGoogle Scholar
  12. Galinha C, Bilsborough G, Tsiantis M (2009) Hormonal input in plant meristems: a balancing act. Semin Cell Dev Biol 20:1149–1156CrossRefGoogle Scholar
  13. Gao K, Chen F, Yuan L, Zhang F, Mi G (2014) A comprehensive analysis of root morphological changes and nitrogen allocation in maize in response to low nitrogen stress. Plant Cell Environ 38(4):740–750Google Scholar
  14. Garnett T, Conn V, Plett D, Conn S, Zanghellini J, Mackenzie N, Enju A, Francis K, Holtham L, Roessner U, Boughton B, Bacic A, Shirley N, Rafalski A, Dhugga K, Tester M, Kaiser BN (2013) The response of the maize nitrate transport system to nitrogen demand and supply across the lifecycle. New Phytol 198:82–94CrossRefGoogle Scholar
  15. Hauck R, Bremner J (1976) Use of tracers for soil and fertilizer nitrogen research. Adv Agron 28:219–266CrossRefGoogle Scholar
  16. Henke M, Sarlikioti V, Kurth W, Buck-Sorlin GH, Pages L (2014) Exploring root developmental plasticity to nitrogen with a three-dimensional architectural model. Plant Soil 385:49–62CrossRefGoogle Scholar
  17. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24CrossRefGoogle Scholar
  18. Horwath WR (2014) Isotope methods to study the soil N cycleGoogle Scholar
  19. Hou X, Tigabu M, Zhang Y, Ma X, Cai L, Wu P, Liu A, Wang C, Qiu H (2017) Root plasticity, whole plant biomass, and nutrient accumulation of Neyraudia reynaudiana in response to heterogeneous phosphorus supply. J Soils Sedim 17:172–180CrossRefGoogle Scholar
  20. Hu TT, Kang SZ, Zhang FC, Zhang JH (2006) Alternate application of osmotic and nitrogen stresses to partial root system: effects on root growth and nitrogen use efficiency. J Plant Nutr 29:2079–2092CrossRefGoogle Scholar
  21. Hu TT, Kang SZ, Li FS, Zhang JH (2009) Effects of partial root-zone irrigation on the nitrogen absorption and utilization of maize. Agric Water Manag 96:208–214CrossRefGoogle Scholar
  22. Ishikawa-Sakurai J, Hayashi H, Murai-Hatano M (2014) Nitrogen availability affects hydraulic conductivity of rice roots, possibly through changes in aquaporin gene expression. Plant Soil 289–300Google Scholar
  23. Ivans CY, Leffler AJ, Spaulding U, Stark JM, Ryel RJ, Caldwell MM (2003) Root responses and nitrogen acquisition by Artemisia tridentata and Agropyron desertorum following small summer rainfall events. Oecologia 134(3):317–324CrossRefGoogle Scholar
  24. Jackson RB, Caldwell MM (1991) Kinetic responses of Pseudoroegneria roots to localized soil enrichment. Plant Soil 138(2):231–238CrossRefGoogle Scholar
  25. Jing J, Zhang F, Rengel Z, Shen J (2012) Localized fertilization with P plus N elicits an ammonium-dependent enhancement of maize root growth and nutrient uptake. Field Crops Res 133:176–185CrossRefGoogle Scholar
  26. Kembel SW, Kroon HD, Cahill JF, Mommer L (2008) Improving the scale and precision of hypotheses to explain root foraging ability. Ann Bot 101(9):1295–1301CrossRefGoogle Scholar
  27. Kraiser T, Gras DE, Gutierrez AG, Gonzalez B, Gutierrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466CrossRefGoogle Scholar
  28. Lee BR, Jin YL, Park SH, Zaman R, Zhang Q, Avice JC, Ourry A, Kim TH (2015) Genotypic variation in N uptake and assimilation estimated by 15N tracing in water deficit-stressed Brassica napus. Environ Exp Bot 109:73–79CrossRefGoogle Scholar
  29. 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):776–784Google Scholar
  30. Li H, Ma Q, Li H, Zhang F, Rengel Z, Shen J (2014) Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits. Plant Soil 376:151–163CrossRefGoogle Scholar
  31. Lomas MW, Glibert PM (2000) Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J Phycol 36:903–913CrossRefGoogle Scholar
  32. Lyu Y, Tang H, Li H, Zhang F, Rengel Z, Whalley WR, Shen J (2016) Major crop species show differential balance between root morphological and physiological responses to variable phosphorus supply. Front Plant Sci 7:1939CrossRefGoogle Scholar
  33. Martinez V, Del Amor FM, Marcelis LFM (2005) Growth and physiological response of tomato plants to different periods of nitrogen starvation and recovery. J Hortic Sci Biotechnol 80:147–153CrossRefGoogle Scholar
  34. Matimati I, Verboom GA, Cramer MD (2014) Nitrogen regulation of transpiration controls mass-flow acquisition of nutrients. J Exp Bot 65:159–168CrossRefGoogle Scholar
  35. Mi G, Chen F, Wu Q, Lai N, Yuan L, Zhang F (2010) Ideotype root architecture for efficient nitrogen acquisition by maize in intensive cropping systems. Sci China-Life Sci 53:1369–1373CrossRefGoogle Scholar
  36. Miller A, Cramer M (2005) Root nitrogen acquisition and assimilation. In: Root physiology: from gene to function. Springer, New York, pp. 1–36Google Scholar
  37. 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
  38. Moreira X, Zas R, Sampedro L (2012) Genetic variation and phenotypic plasticity of nutrient re-allocation and increased fine root production as putative tolerance mechanisms inducible by methyl jasmonate in pine trees. J Ecol 100:810–820CrossRefGoogle Scholar
  39. Mou P, Jones R, Tan Z, Bao Z, Chen H (2013) Morphological and physiological plasticity of plant roots when nutrients are both spatially and temporally heterogeneous. Plant Soil 364:373–384CrossRefGoogle Scholar
  40. Nishikawa T, Tarutani K, Yamamoto T (2010) Nitrate and phosphate uptake kinetics of the harmful diatom Coscinodiscus wailesii, a causative organism in the bleaching of aquacultured Porphyra thalli. Harmful Algae 9:563–567CrossRefGoogle Scholar
  41. Niu X, Hu T, Zhang F, Feng P (2016) Severity and duration of osmotic stress on partial root system: effects on root hydraulic conductance and root growth. Plant Growth Regul 79:177–186CrossRefGoogle Scholar
  42. Niwa K, Harada K (2013) Physiological responses to nitrogen deficiency and resupply in different blade portions of Pyropia yezoensis f. narawaensis (Bangiales, Rhodophyta). J Exp Mar Biol Ecol 439:113–118CrossRefGoogle Scholar
  43. Rashid SZ, Kyo M (2010) Ectopic expression of ARR1∆DDK in tobacco: alteration of cell fate in root tip region and shoot organogenesis in cultured segments. Plant Biotechnol Rep 4:53–59CrossRefGoogle Scholar
  44. Richard-Molard C, Krapp A, Brun F, Ney B, Daniel-Vedele F, Chaillou S (2008) Plant response to nitrate starvation is determined by N storage capacity matched by nitrate uptake capacity in two Arabidopsis genotypes. J Exp Bot 59:779–791CrossRefGoogle Scholar
  45. Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11:440–448CrossRefGoogle Scholar
  46. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53:971–977CrossRefGoogle Scholar
  47. Tamaki V, Mercier H (2007) Cytokinins and auxin communicate nitrogen availability as long-distance signal molecules in pineapple (Ananas comosus). J Plant Physiol 164:1543–1547CrossRefGoogle Scholar
  48. Tantanasarit C, Englande AJ, Babel S (2013) Nitrogen, phosphorus and silicon uptake kinetics by marine diatom Chaetoceros calcitrans under high nutrient concentrations. J Exp Mar Biol Ecol 446:67–75CrossRefGoogle Scholar
  49. Van Vuuren M, Robinson D, Griffiths B (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
  50. Wang Q, Cheng Y (2004) Response of fine roots to soil nutrient spatial heterogeneity. Chin J Appl Ecol 15(6):1063–1068Google Scholar
  51. Wang L, Mou PP, Jones RH (2006) Nutrient foraging via physiological and morphological plasticity in three plant species. Can J For Res 36:164–173CrossRefGoogle Scholar
  52. Wang XL, Wang JJ, Sun RH, Hou XG, Zhao W, Shi J, Zhang YF, Qi L, Li XL, Dong PH, Zhang LX, Xu GW, Gan HB (2016) Correlation of the corn compensatory growth mechanism after post-drought rewatering with cytokinin induced by root nitrate absorption. Agric Water Manag 166:77–85CrossRefGoogle Scholar
  53. Wijesinghe DK, John EA, Beurskens S, Hutchings MJ (2001) Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. J Ecol 89(6):972–983CrossRefGoogle Scholar
  54. Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. In: Merchant SS annual review of plant biology, vol 63, pp. 153–182Google Scholar
  55. Xu H, Liu C, Lu R, Guo G, Chen Z, He T, Gao R, Li Y, Huang J (2016) The difference in responses to nitrogen deprivation and re-supply at seedling stage between two barley genotypes differing nitrogen use efficiency. Plant Growth Regul 79:119–126CrossRefGoogle Scholar
  56. Yandell BS (1997) Practical data analysis for designed experiments. Chapman &Hall, LondonCrossRefGoogle Scholar
  57. Yano K, Kume T (2005) Root morphological plasticity for heterogeneous phosphorus supply in Zea mays L. Plant Prod Sci 8(4):427–432CrossRefGoogle Scholar
  58. Yu P, White P, Hochholdinger F, Li C (2014) Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240:667–678CrossRefGoogle Scholar
  59. Yu P, Hochholdinger F, Li C (2015) Root-type-specific plasticity in response to localized high nitrate supply in maize (Zea mays). Ann Bot 116:751–762CrossRefGoogle Scholar
  60. Zhang S, Shan L (2001) Research progress on water uptake in plant roots. Chin J Appl Environ Biol 7:396–402Google Scholar
  61. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58:2329–2338CrossRefGoogle Scholar
  62. Zhang L, Zhao H, Yan W, Tan G, Bian S (2015) Effects of water and nitrogen stress on maize yield and nitrogen intake transport. J Maize Sci 23:117–123Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Xiaoli Niu
    • 1
    • 2
    • 3
  • Tiantian Hu
    • 2
    Email author
  • Fucang Zhang
    • 2
  • Aiwang Duan
    • 1
  • Jiyang Zhang
    • 1
  1. 1.Key Laboratory for Crop Water Requirement and its Regulation, Ministry of Agriculture, Farmland Irrigation Research InstituteChinese Academy of Agricultural SciencesXinxiangChina
  2. 2.College of Water Resources and Architectural EngineeringNorthwest A&F UniversityYanglingChina
  3. 3.College of Agricultural Equipment EngineeringHenan University of Science and TechnologyLuoyangChina

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