Dynamics of localised nitrogen supply and relevance for root growth of Vicia faba (‘Fuego’) and Hordeum vulgare (‘Marthe’) in soil

Forde, B. & Lorenzo, H. The nutritional control of root development. Plant Soil 232, 51–68. https://doi.org/10.1023/A:1010329902165 (2001).

CAS  Article  Google Scholar 

Hodge, A. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol. 162, 9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x (2004).

Article  Google Scholar 

Robinson, D. Tansley review no 73. The responses of plants to non-uniform supplies of nutrients. New Phytol. 127, 635–674 (1994).

CAS  Article  Google Scholar 

Yu, P., White, P. J., Hochholdinger, F. & Li, C. Phenotypic plasticity of the maize root system in response to heterogeneous nitrogen availability. Planta 240, 667–678. https://doi.org/10.1007/s00425-014-2150-y (2014).

CAS  Article  PubMed  Google Scholar 

Osmont, K. S., Sibout, R. & Hardtke, C. S. Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58, 93–113. https://doi.org/10.1146/annurev.arplant.58.032806.104006 (2007).

CAS  Article  PubMed  Google Scholar 

Ahmed, S. et al. Imaging the interaction of roots and phosphate fertiliser granules using 4D X-ray tomography. Plant Soil 401, 125–134. https://doi.org/10.1007/s11104-015-2425-5 (2016).

CAS  Article  Google Scholar 

Drew, M. & Saker, L. 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 a localized supply of phosphate. J. Exp. Bot. 29, 435–451 (1978).

CAS  Article  Google Scholar 

Flavel, R. J., Guppy, C. N., Tighe, M. K., Watt, M. & Young, I. M. Quantifying the response of wheat (Triticum aestivum L.) root system architecture to phosphorus in an Oxisol. Plant Soil 385, 303–310. https://doi.org/10.1007/s11104-014-2191-9 (2014).

CAS  Article  Google Scholar 

Nacry, P., Bouguyon, E. & Gojon, A. Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370, 1–29. https://doi.org/10.1007/s11104-013-1645-9 (2013).

CAS  Article  Google Scholar 

Bloom, A. J., Frensch, J. & Taylor, A. R. Influence of inorganic nitrogen and pH on the elongation of maize seminal roots. Ann. Bot. 97, 867–873. https://doi.org/10.1093/aob/mcj605 (2006).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Bloom, A. J., Jackson, L. E. & Smart, D. R. Root-growth as a function of ammonium and nitrate in the root zone. Plant Cell Environ. 16, 199–206. https://doi.org/10.1111/j.1365-3040.1993.tb00861.x (1993).

CAS  Article  Google Scholar 

Caba, J. M., Centeno, M. L., Fernandez, B., Gresshoff, P. M. & Ligero, F. Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta 211, 98–104. https://doi.org/10.1007/s004250000265 (2000).

CAS  Article  PubMed  Google Scholar 

Gerendás, J. & Sattelmacher, B. Influence of nitrogen form and concentration on growth and ionic balance of tomato (Lycopersicon esculentum) and potato (Solanum tuberosum). In Plant nutrition—physiology and applications (ed. van Beusichem, M. L.) 33–37 (Springer, Berlin, 1990).

Google Scholar 

Granato, T. C. & Raper, C. D. Jr. Proliferation of maize (Zea mays L.) roots in response to localized supply of nitrate. J. Exp. Bot. 40, 263–275. https://doi.org/10.1093/jxb/40.2.263 (1989).

CAS  Article  PubMed  Google Scholar 

Maizlish, N., Fritton, D. & Kendall, W. Root morphology and early development of maize at varying levels of nitrogen 1. Agron. J. 72, 25–31 (1980).

CAS  Article  Google Scholar 

Ogawa, S., Valencia, M. O., Ishitani, M. & Selvaraj, M. G. Root system architecture variation in response to different NH₄⁺ concentrations and its association with nitrogen-deficient tolerance traits in rice. Acta Physiol. Plant. 36, 2361–2372. https://doi.org/10.1007/s11738-014-1609-6 (2014).

CAS  Article  Google Scholar 

Sattelmacher, B. & Thoms, K. Root growth and 14C-translocation into the roots of maize (Zea mays L.) as influenced by local nitrate supply. J. Plant Nutr. Soil Sci. 152, 7–10 (1989).

CAS  Google Scholar 

Schortemeyer, M., Feil, B. & Stamp, P. Root morphology and nitrogen uptake of maize simultaneously supplied with ammonium and nitrate in a split-root system. Ann. Bot. 72, 107–115. https://doi.org/10.1006/anbo.1993.1087 (1993).

CAS  Article  Google Scholar 

Thoms, K. & Sattelmacher, B. Influence of nitrate placement on morphology and physiology of maize (Zea mays) root systems. In Plant nutrition—physiology and applications (ed van Beusichem, M. L.) 29–32 (Springer, Berlin, 1990).

Google Scholar 

Tian, Q., Chen, F., Liu, J., Zhang, F. & Mi, G. Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J. Plant Physiol. 165, 942–951. https://doi.org/10.1016/j.jplph.2007.02.011 (2008).

CAS  Article  PubMed  Google Scholar 

Gruber, B. D., Giehl, R. F., Friedel, S. & von Wiren, N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163, 161–179. https://doi.org/10.1104/pp.113.218453 (2013).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Lima, J. E., Kojima, S., Takahashi, H. & von Wiren, N. Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22, 3621–3633. https://doi.org/10.1105/tpc.110.076216 (2010).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Remans, T. et al. The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl. Acad. Sci. U. S. A. 103, 19206–19211. https://doi.org/10.1073/pnas.0605275103 (2006).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Zhang, H. & Forde, B. G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409. https://doi.org/10.1126/science.279.5349.407 (1998).

ADS  CAS  Article  PubMed  Google Scholar 

Zhang, H., Jennings, A., Barlow, P. W. & Forde, B. G. Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. U.S.A. 96, 6529–6534. https://doi.org/10.1073/pnas.96.11.6529 (1999).

ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

Drew, M. Comparison of the effects of a localised supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol. 75, 479–490 (1975).

CAS  Article  Google Scholar 

Drew, M. & Saker, L. Nutrient Supply and the Growth of the Seminal Root System in Barley II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J. Exp. Bot. 26, 79–90 (1975).

CAS  Article  Google Scholar 

Drew, M., Saker, L. & Ashley, T. 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, 1189–1202 (1973).

CAS  Article  Google Scholar 

Beeckman, F., Motte, H. & Beeckman, T. Nitrification in agricultural soils: impact, actors and mitigation. Curr. Opin. Biotechnol. 50, 166–173. https://doi.org/10.1016/j.copbio.2018.01.014 (2018).

CAS  Article  PubMed  Google Scholar 

Heil, J., Vereecken, H. & Bruggemann, N. A review of chemical reactions of nitrification intermediates and their role in nitrogen cycling and nitrogen trace gas formation in soil. Eur. J. Soil Sci. 67, 23–39. https://doi.org/10.1111/ejss.12306 (2016).

CAS  Article  Google Scholar 

Blume, H.-P. et al. Scheffer/Schachtschabel Soil Science (Springer, Berlin, 2015).

Google Scholar 

Nieder, R., Benbi, D. K. & Scherer, H. W. Fixation and defixation of ammonium in soils: a review. Biol. Fertil. Soils 47, 1–14. https://doi.org/10.1007/s00374-010-0506-4 (2011).

CAS  Article  Google Scholar 

Nommik, H. & Vahtras, K. Retention and fixation of ammonium and ammonia in soils. In Nitrogen in Agricultural Soils 22, (ed. Stevenson, F. J.) 123–171 (Wiley, Madison, Wisconsin, USA, 1982).

Google Scholar 

Morris, E. C. et al. Shaping 3D root system architecture. Curr. Biol. 27, R919–R930. https://doi.org/10.1016/j.cub.2017.06.043 (2017).

CAS  Article  PubMed  Google Scholar 

Anghinoni, I. & Barber, S. A. Corn root-growth and nitrogen uptake as affected by ammonium placement. Agron. J. 80, 799–802. https://doi.org/10.2134/agronj1988.00021962008000050021x (1988).

Article  Google Scholar 

Anghinoni, I., Magalhaes, J. R. & Barber, S. A. Enzyme-activity, nitrogen uptake and corn growth as affected by ammonium concentration in soil solution. J. Plant Nutr. 11, 131–144. https://doi.org/10.1080/01904168809363791 (1988).

CAS  Article  Google Scholar 

Pan, W. L., Madsen, I. J., Bolton, R. P., Graves, L. & Sistrunk, T. Ammonia/ammonium toxicity root symptoms induced by inorganic and organic fertilizers and placement. Agron. J. 108, 2485–2492. https://doi.org/10.2134/agronj2016.02.0122 (2016).

CAS  Article  Google Scholar 

Xu, L. et al. Nitrogen transformation and plant growth in response to different urea-application methods and the addition of DMPP. J. Plant Nutr. Soil Sci. 177, 271–277. https://doi.org/10.1002/jpln.201100390 (2014).

CAS  Article  Google Scholar 

Zhang, J. C. & Barber, S. A. Corn root distribution between ammonium fertilized and unfertilized soil. Commun. Soil Sci. Plant Anal. 24, 411–419. https://doi.org/10.1080/00103629309368811 (1993).

Article  Google Scholar 

Maestre, F. T. & Reynolds, J. F. Small-scale spatial heterogeneity in the vertical distribution of soil nutrients has limited effects on the growth and development of Prosopis glandulosa seedlings. Plant Ecol. 183, 65–75. https://doi.org/10.1007/s11258-005-9007-1 (2006).

Article  Google Scholar 

Rabbi, S. M., Guppy, C., Flavel, R., Tighe, M. & Young, I. Root plasticity not evident in N-enriched soil volumes for wheat (Triticum aestivum L.) and Barley (Hordeum vulgare L.) varieties. Commun. Soil Sci. Plant Anal. 48, 2002–2012 (2017).

CAS  Article  Google Scholar 

Van Vuuren, M., Robinson, D. & Griffiths, B. Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant Soil 178, 185–192 (1996).

Article  Google Scholar 

Hodge, A., Robinson, D., Griffiths, B. S. & Fitter, A. H. Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ. 22, 811–820. https://doi.org/10.1046/j.1365-3040.1999.00454.x (1999).

Article  Google Scholar 

Hodge, A., Stewart, J., Robinson, D., Griffiths, B. S. & Fitter, A. H. Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. New Phytol. 139, 479–494. https://doi.org/10.1046/j.1469-8137.1998.00216.x (1998).

Article  Google Scholar 

Hodge, A., Stewart, J., Robinson, D., Griffiths, B. S. & Fitter, A. H. Plant, soil fauna and microbial responses to N-rich organic patches of contrasting temporal availability. Soil Biol. Biochem. 31, 1517–1530. https://doi.org/10.1016/S0038-0717(99)00070-X (1999).

CAS  Article  Google Scholar 

Li, H. B. et al. Root morphological responses to localized nutrient supply differ among crop species with contrasting root traits. Plant Soil 376, 151–163. https://doi.org/10.1007/s11104-013-1965-9 (2014).

CAS  Article  Google Scholar 

Abalos, D., Sanz-Cobena, A., Misselbrook, T. & Vallejo, A. Effectiveness of urease inhibition on the abatement of ammonia, nitrous oxide and nitric oxide emissions in a non-irrigated Mediterranean barley field. Chemosphere 89, 310–318. https://doi.org/10.1016/j.chemosphere.2012.04.043 (2012).

ADS  CAS  Article  PubMed  Google Scholar 

Slangen, J. H. G. & Kerkhoff, P. Nitrification inhibitors in agriculture and horticulture—a literature-review. Fertil. Res. 5, 1–76. https://doi.org/10.1007/Bf01049492 (1984).

CAS  Article  Google Scholar 

Zaman, M., Zaman, S., Nguyen, M. L., Smith, T. J. & Nawaz, S. The effect of urease and nitrification inhibitors on ammonia and nitrous oxide emissions from simulated urine patches in pastoral system: a two-year study. Sci. Tot. Environ. 465, 97–106. https://doi.org/10.1016/j.scitotenv.2013.01.014 (2013).

CAS  Article  Google Scholar 

Metzner, R. et al. Direct comparison of MRI and X-ray CT technologies for 3D imaging of root systems in soil: potential and challenges for root trait quantification. Plant Methods 11, 17. https://doi.org/10.1186/s13007-015-0060-z (2015).

Article  PubMed  PubMed Central  Google Scholar 

Beuters, P., Scherer, H. W., Spott, O. & Vetterlein, D. Impact of potassium on plant uptake of non-exchangeable NH₄⁺-N. Plant Soil 387, 37–47. https://doi.org/10.1007/s11104-014-2275-6 (2014).

CAS  Article  Google Scholar 

Vetterlein, D., Kuhn, T., Kaiser, K. & Jahn, R. Illite transformation and potassium release upon changes in composition of the rhizophere soil solution. Plant Soil 371, 267–279. https://doi.org/10.1007/s11104-013-1680-6 (2013).

CAS  Article  Google Scholar 

VDLUFA, M. Band 1. Die Untersuchung von Böden (VDLUFA-Verlag, Darmstad, 1991) ((in German)).

Google Scholar 

Koebernick, N. et al. In situ visualization and quantification of three-dimensional root system architecture and growth using X-ray computed tomography. Vadose Zone J. https://doi.org/10.2136/vzj2014.03.0024 (2014).

Article  Google Scholar 

Blaser, S. R. G. A., Schlüter, S. & Vetterlein, D. How much is too much?-Influence of X-ray dose on root growth of faba bean (Vicia faba) and barley (Hordeum vulgare). PLoS ONE 13, e0193669. https://doi.org/10.1371/journal.pone.0193669 (2018).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Schlüter, S., Blaser, S. R. G. A., Weber, M., Schmidt, V. & Vetterlein, D. Quantification of root growth patterns from the soil perspective via root distance models. Front. Plant Sci. 9, 1084. https://doi.org/10.3389/fpls.2018.01084 (2018).

Article  PubMed  PubMed Central  Google Scholar 

Flavel, R. J. et al. Non-destructive quantification of cereal roots in soil using high-resolution X-ray tomography. J. Exp. Bot. 63, 2503–2511. https://doi.org/10.1093/jxb/err421 (2012).

CAS  Article  PubMed  Google Scholar 

Doube, M. et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone 47, 1076–1079. https://doi.org/10.1016/j.bone.2010.08.023 (2010).

Article  PubMed  PubMed Central  Google Scholar 

Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682. https://doi.org/10.1038/nmeth.2019 (2012).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Kirschke, T., Spott, O. & Vetterlein, D. Impact of urease and nitrification inhibitor on NH₄⁺ and NO₃⁻ dynamic in soil after urea spring application under field conditions evaluated by soil extraction and soil solution sampling. J. Plant Nutr. Soil Sci. 182, 441–450. https://doi.org/10.1002/jpln.201800513 (2019).

CAS  Article  Google Scholar 

61Bergmann, W. Farbatlas Ernährungsstörungen bei Kulturpflanzen: visuelle und analytische Diagnose. (1986).

Bennett, W. F., Pesek, J. & Hanway, J. J. Effect of nitrate and ammonium on growth of corn in nutrient solution sand culture. Agron. J. 56, 342–345 (1964).

CAS  Article  Google Scholar 

Magalhaes, J. R. & Wilcox, G. E. Tomato growth and nutrient-uptake patterns as influenced by nitrogen form and light-intensity. J. Plant Nutr. 6, 941–956. https://doi.org/10.1080/01904168309363157 (1983).

CAS  Article  Google Scholar 

Ganmore-Neumann, R. & Kafkafi, U. root temperature and percentage NO₃⁻/NH₄⁺ effect on tomato plant development I. Morphology and growth 1. Agron. J. 72, 758–761 (1980).

CAS  Article  Google Scholar 

Einsmann, J. C., Jones, R. H., Pu, M. & Mitchell, R. J. Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J. Ecol. 87, 609–619. https://doi.org/10.1046/j.1365-2745.1999.00376.x (1999).

Article  Google Scholar 

Gao, W., Blaser, S. R. G. A., Schluter, S., Shen, J. B. & Vetterlein, D. Effect of localised phosphorus application on root growth and soil nutrient dynamics in situ—comparison of maize (Zea mays) and faba bean (Vicia faba) at the seedling stage. Plant Soil 441, 469–483. https://doi.org/10.1007/s11104-019-04138-2 (2019).

CAS  Article  Google Scholar 

Britto, D. T. & Kronzucker, H. J. NH₄⁺ toxicity in higher plants: a critical review. J. Plant Physiol. 159, 567–584. https://doi.org/10.1078/0176-1617-0774 (2002).

CAS  Article  Google Scholar 

Adjel, F., Bouzerzour, H. & Benmahammed, A. Salt stress effects on seed germination and seedling growth of barley (Hordeum vulgare L.) Genotypes. J. Agric. Sustain. 3, 223–237 (2013).

Google Scholar 

Ahmed, A. K., Tawfik, K. & Abd El-Gawad, Z. Tolerance of seven faba bean varieties to drought and salt stresses. Res. J. Agric. Biol. Sci. 4, 175–186 (2008).

Google Scholar 

Link, W. et al. Genotypic variation for drought tolerance in Vicia faba. Plant Breed. 118, 477–483. https://doi.org/10.1046/j.1439-0523.1999.00412.x (1999).

Article  Google Scholar 

Varshney, R. K. et al. Genome wide association analyses for drought tolerance related traits in barley (Hordeum vulgare L.). Field Crops Res. 126, 171–180. https://doi.org/10.1016/j.fcr.2011.10.008 (2012).

Article  Google Scholar 

Wilcox, G. E., Magalhaes, J. R. & Silva, F. L. I. M. Ammonium and nitrate concentrations as factors in tomato growth and nutrient-uptake. J. Plant Nutr. 8, 989–998. https://doi.org/10.1080/01904168509363401 (1985).

Article  Google Scholar 

Elamin, O. M. & Wilcox, G. E. Nitrogen form ratio influence on muskmelon growth, composition, and manganese toxicity. J. Am. Soc. Hortic. Sci. 111, 320–322 (1986).

Google Scholar 

Handa, S., Warren, H. L., Huber, D. M. & Tsai, C. Y. Nitrogen nutrition and seedling development of normal and opaque-2 maize genotypes. Can. J. Plant Sci. 64, 885–894. https://doi.org/10.4141/cjps84-121 (1984).

CAS  Article  Google Scholar