Nitrogen (N) plays a key role in the plant life cycle. It is the main plant mineral nutrient needed for chlorophyll production and other plant cell components (proteins, nucleic acids, amino acids). Crop yield is affected by plant N status. Thus, the optimization of nitrogen fertilization has become the object of intense research due to its environmental and economic impact. This article focuses on reviewing current methods and techniques used to determine plant N status. Kjeldahl digestion and Dumas combustion have been used as reference methods for N determination in plants, but they are destructive and time consuming. By using spectroradiometers, reflectometers, imagery from satellite sensors and digital cameras, optical properties have been measured to estimate N in plants, such as crop canopy reflectance, leaf transmittance, chlorophyll and polyphenol fluorescence. High correlation has been found between optical parameters and plant N status, and those techniques are not destructive. However, some drawbacks include chlorophyll saturation, atmospheric and soil interference, and the high cost of instruments. Electrical properties of plant tissue have been used to estimate quality in fruits, and water content in plants, as well as nutrient deficiency, which suggests that they have potential for use in plant N determination.
References
[1]
Sinfield, J.V.; Fagerman, D.; Colic, O. Evaluation of sensing technologies for on-the-go detection of macro-nutrients in cultivated soils. Comput. Electron. Agric. 2010, 70, 1–18.
[2]
Hoffland, E.; Dicke, M.; van Tintelen, W.; Dijkman, H.; van Beusichem, M.L. Nitrogen availability and defense of tomato against two-spotted spider mite. J. Chem. Ecol. 2000, 26, 2697–2711.
[3]
Tremblay, N.; Fallon, E.; Ziadi, N. Sensing of crop nitrogen status: Opportunities, tools, limitations, and supporting information requirements. Hort Technol. 2011, 21, 274–281.
[4]
Taiz, L.; Zeiger, E. Plant Physiology, 5th ed. ed.; Sinauer Associates Inc.: Sunderland, MA, USA, 2010; pp. 67–86.
[5]
Vigneau, N.; Ecarnot, M.; Rabatel, G.; Roumet, P. Potential of field hyperspectral imaging as a non destructive method to assess leaf nitrogen content in Wheat. Field Crop. Res. 2011, 122, 25–31.
[6]
Rubio-Covarrubias, O.A.; Brown, P.H.; Weinbaum, S.A.; Johnson, R.S.; Cabrera, R.I. Evaluating foliar nitrogen compounds as indicators of nitrogen status in Prunus persica trees. Sci. Hort. 2009, 120, 27–33.
[7]
Zebarth, B.J.; Drury, C.F.; Tremblay, N.; Cambouris, A.N. Opportunities for improved fertilizer nitrogen management in production of arable crops in eastern Canada: A review. Can. J. Soil Sci. 2009, 89, 113–132.
[8]
Timmer, B.; Olthuis, W.; van den Berg, A. Ammonia sensors and their applications: A review. Sens. Actuators B. 2005, 107, 666–677.
[9]
Parks, S.E.; Irving, D.E.; Milham, P.J. A critical evaluation of on-farm rapid tests for measuring nitrate in leafy vegetables. Sci. Hort. 2012, 134, 1–6.
[10]
Houlès, V.; Guerif, M.; Mary, B. Elaboration of a nitrogen nutrition indicator for winter wheat based on leaf area index and chlorophyll content for making nitrogen recommendations. Eur. J. Agron. 2007, 27, 1–11.
[11]
Demotes-Mainard, S.; Boumaza, R.; Meyer, S.; Cerovic, Z.G. Indicators of nitrogen status for ornamental woody plants based on optical measurements of leaf epidermal polyphenol and chlorophyll contents. Sci. Hort. 2008, 115, 377–385.
[12]
Li, Y.; Chen, D.; Walker, C.N.; Angus, J.F. Estimating the nitrogen status of crops using a digital camera. Field Crop. Res. 2010, 118, 221–227.
[13]
He, J.-X.; Wang, Z.-Y.; Shi, Y.-L.; Qin, Y.; Zhao, D.-J.; Huang, L. A prototype portable system for bioelectrical impedance spectroscopy. Sens. Lett. 2011, 9, 1151–1156.
Greenham, C.G.; Randall, P.J.; Müller, W.J. Studies of phosphorus and potassium deficiencies in Trifolium subterraneum based on electrical measurements. Can. J. Bot. 1982, 60, 634–644.
[16]
Tomkiewicz, D.; Piskier, T. A plant based sensing method for nutrition stress monitoring. Precis. Agric. 2012, 13, 370–383.
[17]
Kjeldahl, J. Neue Methode zur Bestimmung des Stickstoffs in organischen K？rpern. Fresenius J. Anal. Chem. 1883, 22, 366–382.
[18]
Labconco, C. A Guide to Kjeldahl Nitrogen Determination Methods and Apparatus; Labconco Corporation: Houston, TX, USA, 1998.
[19]
Kalra, Y.P. Hand Book of Reference Methods for Plant Analysis; CRC Press: Boca Raton, FL, USA, 1998; pp. 75–92.
[20]
Domini, C.; Vidal, L.; Cravotto, G.; Canals, A. A simultaneous, direct microwave/ultrasound-assisted digestion procedure for the determination of total Kjeldahl nitrogen. Ultrason. Sonochem. 2009, 16, 564–569.
[21]
Sáez-Plaza, P.; Michalowski, T.; Navas, M.J.; Asuero, A.G.; Wybraniec, S. An overview of the Kjeldahl method of nitrogen determination. Part I. Early history, chemistry of the procedure, and titrimetric finish. Crit. Rev. Anal. Chem.. In Revision .
[22]
Michalowski, T.; Asuero, A.G.; Wybraniec, S.A. The titration in the kjeldahl method of nitrogen determination: Base or acid as titrant? J. Chem. Educ. 2013, 90, 191–197.
[23]
Lee, D.; Nguyen, V.; Littlefield, S. Comparison of methods for determination of nitrogen levels in soil, plant and body tissues, and water. Commun. Soil Sci. Plant Anal. 1996, 27, 783–793.
[24]
Amin, M.; Flowers, T.H. Evaluation of Kjeldahl digestion method. J. Res. Science 2004, 15, 159–179.
[25]
Saha, U.K.; Sonon, L.; Kissel, D.E. Comparison of conductimetric and colorimetric methods with distillation-titration method of analyzing ammonium nitrogen in total kjeldahl digests. Commun. Soil Sci. Plant Anal. 2012, 43, 2323–2341.
[26]
Clifton, K.E.; Clifton, L.M. A field method for the determination of total nitrogen in plant tissue. Commun. Soil Sci. Plant Anal. 1991, 22, 851–860.
[27]
Handson, P.D.; Shelley, B.C. A review of plant analysis in Australia. Anim. Prod. Sci. 1993, 33, 1029–1038.
[28]
Pontes, F.V.M.; Carneiro, M.C.; Vaitsman, D.S.; da Rocha, G.P.; da Silva, L.I.D.; Neto, A.A.; Monteiro, M.I.C. A simplified version of the total kjeldahl nitrogen method using an ammonia extraction ultrasound-assisted purge-and-trap system and ion chromatography for analyses of geological samples. Anal. Chim. Acta. 2009, 632, 284–288.
[29]
Dumas, J.B.A. Procedes de l'analyse organic. Ann. Chim. Phys. 1831, 247, 198–213.
[30]
Unkovich, M.; Herridge, D.; Peoples, M.; Cadisch, G.; Boddey, B.; Giller, K.; Alves, B.; Chalk, P. Measuring Plant-associated Nitrogen Fixation in Agricultural Systems; Australian Centre for International Agricultural Research (ACIAR): Canberra, ACT, Australia, 2008; pp. 45–62.
[31]
Watson, M.E.; Galliher, T.L. Comparison of Dumas and Kjeldahl methods with automatic analyzers on agricultural samples under routine rapid analysis conditions. Commun. Soil Sci. Plant Anal. 2001, 32, 2007–2019.
[32]
Goffart, J.P.; Olivier, M.; Frankinet, M. Potato crop nitrogen status assessment to improve N fertilization management and efficiency: Past-present-future. Potato Res. 2008, 51, 355–383.
[33]
Sáez-Plaza, P.; Navas, M.J.; Wybrainiec, S.; Michalowski, T.; Asuero, A.G. An overview of the Kjeldahl method on nitrogen determination. Part II. Sampling preparation, working scale, instrumental finish, and quality control. Crit. Rev. Anal. Chem.. In Revision .
[34]
Perry, E.M.; Davenport, J.R. Spectral and spatial differences in response of vegetation indices to nitrogen treatments on apple. Comput. Electron. Agric. 2007, 59, 56–65.
[35]
Miao, Y.; Mulla, D.J.; Randall, G.W.; Vetsch, J.A.; Vintila, R. Combining chlorophyll meter readings and high spatial resolution remote sensing images for in-season site-specific nitrogen management of corn. Precis. Agric. 2009, 10, 45–62.
[36]
Lin, F.F.; Qiu, L.F.; Deng, J.S.; Shi, Y.Y.; Chen, L.S.; Wang, K. Investigation of SPAD meter-based indices for estimating rice nitrogen status. Comput. Elecron. Agric. 2010, 71, S60–S65.
[37]
Cabangon, R.J.; Castillo, E.G.; Tuong, T.P. Chlorophyll meter-based nitrogen management of rice grown under alternate wetting and drying irrigation. Field Crop. Res. 2011, 121, 136–146.
[38]
Yu, H.; Wu, H.-S.; Wang, Z.-J. Evaluation of SPAD and Dualex for in-season corn nitrogen status estimation. Acta Agron. Sin. 2010, 36, 840–847.
[39]
Solari, F.; Shanahan, J.F.; Ferguson, R.B.; Adamchuk, V.I. An active sensor algorithm for corn nitrogen recommendations based on a chlorophyll meter algorithm. Agron. J. 2010, 102, 1090–1098.
[40]
Yu, W.; Miao, Y.; Feng, G.; Yue, S.; Liu, B. Evaluating Different Methods of Using Chlorophyll Meter for Diagnosing Nitrogen Status of Summer Maize. Proceedings of the 2012 First International Conference on Agro-Geoinformatics (Agro-Geoinformatics), Shangai, China, 2–4 August 2012; pp. 1–4.
[41]
Goffart, J.-P.; Olivier, M.; Frankinet, M. Crop nitrogen status assessment tools in a decision support system for nitrogen fertilization management of potato crops. Hort Technol. 2011, 21, 282–286.
[42]
Zhu, J.; Tremblay, N.; Liang, Y. A corn nitrogen status indicator less affected by soil water content. Agron. J. 2011, 103, 890–898.
Thoren, D.; Schmidhalter, U. Nitrogen status and biomass determination of oilseed rape by laser-induced chlorophyll fluorescence. Eur. J. Agron. 2009, 30, 238–242.
[45]
Tremblay, N.; Wang, Z.; Cerovic, Z.G. Sensing crop nitrogen status with fluorescence indicators. A review. Agronomy Sust. Dev. 2012, 32, 451–464.
[46]
Agati, G.; Foschi, L.; Grossi, N.; Guglielminetti, L.; Cerovic, Z.G.; Volterrani, M. Fluorescence-based versus reflectance proximal sensing of nitrogen content in Paspalum vaginatum and Zoysia matrella turfgrasses. Eur. J. Agron. 2013, 45, 39–51.
[47]
Stroppiana, D.; Boschetti, M.; Brivio, P.A.; Bocchi, S. Plant nitrogen concentration in paddy rice from field canopy hyperspectral radiometry. Field Crop. Res. 2009, 111, 119–129.
[48]
Li, F.; Gnyp, M.L.; Jia, L.; Miao, Y.; Yu, Z.; Koppe, W.; Bareth, G.; Chen, X.; Zhang, F. Estimating N status of winter wheat using a handheld spectrometer in the North China Plain. Field Crop. Res. 2008, 106, 77–85.
[49]
Foster, A.J.; Kakani, V.G.; Ge, J.; Mosali, J. Discrimination of switchgrass cultivars and nitrogen treatments using pigment profiles and hyperspectral leaf reflectance data. Remote Sens. 2012, 4, 2576–2594.
[50]
Rambo, L.; Ma, B.L.; Xiong, Y.; Regis Ferreira da Silvia, P. Leaf and canopy optical characteristics as crop-N-status indicators for field nitrogen management in corn. J. Plant Nutr. Soil Sci. 2010, 173, 434–443.
[51]
Zhu, Y.; Yao, X.; Tian, Y.; Liu, X.; Cao, W. Analysis of common canopy vegetation indices for indicating leaf nitrogen accumulations in wheat and rice. Int. J. Appl. Earth Obs. Geoinf. 2008, 10, 1–10.
[52]
Lee, Y.-J.; Yang, C.-M.; Chang, K.-W.; Shen, Y. A simple spectral index using reflectance of 735 nm to assess nitrogen status of rice canopy. Agron. J. 2008, 100, 205–212.
[53]
Zhou, Q.-F.; Liu, Z.-Y.; Huang, J.-F. Detection of nitrogen-overfertilized rice plants with leaf positional difference in hyperspectral vegetation index. J. Zhejiang Univ. Sci. B 2010, 11, 465–470.
[54]
Tremblay, N.; Wang, Z.; Ma, B.-L.; Belec, C.; Vigneault, P. A comparison of crop data measured by two commercial sensors for variable-rate nitrogen application. Precis. Agric. 2009, 10, 145–161.
[55]
Shaver, T.M.; Khosla, R.; Westfall, D.G. Evaluation of two crop canopy sensors for nitrogen variability determination in irrigated maize. Precis. Agric. 2011, 12, 892–904.
[56]
Wu, J.; Wang, D.; Rosen, C.J.; Bauer, M.E. Comparison of petiole nitrate concentrations, SPAD chlorophyll readings, and QuickBird satellite imagery in detecting nitrogen status of potato canopies. Field Crop. Res. 2007, 101, 96–103.
[57]
Navarro-Cerrillo, R.M.; Trujillo, J.; de la Orden, M.S.; Hernández-Clemente, R. Hyperspectral and multispectral satellite sensors for mapping chlorophyll content in a Mediterranean Pinus sylvestris L. plantation. Int. J. Appl. Earth Obs. Geoinf. 2014, 26, 88–96.
[58]
Sims, N.C.; Culvenor, D.; Newnham, G.; Coops, N.C.; Hopmans, P. Towards the operational use of satellite hyperspectral image data for mapping nutrient status and fertilizer requirements in australian plantation forests. IEEE J. Sel. Top. Appl. Earth Obs. Remote Sens. 2013, 6, 320–328.
[59]
Graeff, S.; Pfenning, J.; Claupein, W.; Liebig, H.-P. Evaluation of image analysis to determine the N-fertilizer demand of broccoli plants (Brassica oleracea convar. botrytis var. italica). Adv. Opt. Technol. 2008, 2008, 1–8.
[60]
Kim, Y.; Reid, J.F.; Zhang, Q. Fuzzy logic control of a multispectral imaging sensor for in-field plant sensing. Comput. Electron. Agric. 2008, 60, 279–288.
[61]
Mercado-Luna, A.; Rico-García, E.; Lara-Herrera, A.; Soto-Zarazúa, G.; Ocampo-Velázquez, R.; Guevara-González, R.; Herrera-Ruiz, G.; Torres-Pacheco, I. Nitrogen determination on tomato (Lycopersicon esculentum Mill.) seedlings by color image analysis (RGB). Afr. J. Biotechnol. 2010, 9, 5326–5332.
[62]
Rodrigo, M.; Ginestar, J.; Boix, M.; Ramos, C. Evaluation of Rapid Methods for Nitrate Plant Sap Analysis of Globe Artichoke Grown in Sand Culture. Proceedings of International Symposium on Soilless Culture and Hydroponics 697, Almeria, Spain; 2004; pp. 393–397.
[63]
Lemaire, G.; Jeuffroy, M.-H.; Gastal, F. Diagnosis tool for plant and crop N status in vegetative stage: Theory and practices for crop N management. Eur. J. Agron. 2008, 28, 614–624.
[64]
Montemurro, F. Are organic N fertilizing strategies able to improve lettuce yield, use of nitrogen and N status? J. Plant Nutr. 2010, 33, 1980–1997.
[65]
Di Gioia, F.; Simonne, E.H.; Gonnella, M.; Santamaria, P.; Gazula, A.; Sheppard, Z. Assessment of ionic interferences to nitrate and potassium analyses with ion-selective electrodes. Commun. Soil Sci. Plant Anal. 2011, 41, 1750–1768.
[66]
Azzarello, E.; Masi, E.; Mancuso, S. Electrochemical Impedance Spectroscopy. In Plant Electrophysiology; Volkov, A.G., Ed.; Springer-Verlag: Heidelberg, Germany, 2012; pp. 205–223.
[67]
Moon, J.R.; Tobkin, S.E.; Roberts, M.D.; Dalbo, V.J.; Kerksick, C.M.; Bemben, M.G.; Cramer, J.T.; Stout, J.R. Total body water estimations in healthy men and women using bioimpedance spectroscopy: A deuterium oxide comparison. Nutr. Metab. 2008, 5, 7.
[68]
Meeuwsen, S.; Horgan, G.W.; Elia, M. The relationship between BMI and percent body fat, measured by bioelectrical impedance, in a large adult sample is curvilinear and influenced by age and sex. Clin. Nutr. 2010, 29, 560–566.
[69]
Cho, S.; Thielecke, H. Electrical characterization of human mesenchymal stem cell growth on microelectrode. Microelectron. Eng. 2008, 85, 1272–1274.
[70]
Wu, L.; Ogawa, Y.; Tagawa, A. Electrical impedance spectroscopy analysis of eggplant pulp and effects of drying and freezing-thawing treatments on its impedance characteristics. J. Food Eng. 2008, 87, 274–280.
