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Preferential mineral N form uptake by sugarcane genotypes contrasting in nitrogen use efficiency

Published online by Cambridge University Press:  17 August 2022

Oriel Tiago Kölln*
Affiliation:
State University of Northern Paraná – UENP, Campus Luiz Meneghel, Roadway BR 369, km 54, 86660-000, Bandeirantes, PR, Brazil
Beatriz Nastaro Boschiero
Affiliation:
Laboratory of Stable Isotopes, Center for Nuclear Energy in Agriculture, Av. Centenário, 303, 13416-000, Piracicaba, SP, Brazil
Henrique Coutinho Junqueira Franco
Affiliation:
University of Sao Paulo, Luiz de Queiroz College of Agriculture, Av Padua Dias, 11. Piracicaba, SP, Brazil.
Marina Camara Martins Soldi
Affiliation:
Botanic Department, University of Sao Paulo, Biosciences Institute, Rua do Matão 277, São Paulo, SP, Brazil
Guilherme Martinelli Sanches
Affiliation:
University of Sao Paulo, Luiz de Queiroz College of Agriculture, Av Padua Dias, 11. Piracicaba, SP, Brazil.
Sergio Gustavo de Quassi Castro
Affiliation:
AgroQuatro-S Experimentation and Applied Agronomic Consultancy, Avenida 6, n. 883, Orlândia, SP, Brazil
Paulo Cesar Ocheuze Trivelin
Affiliation:
Laboratory of Stable Isotopes, Center for Nuclear Energy in Agriculture, Av. Centenário, 303, 13416-000, Piracicaba, SP, Brazil
*
*Corresponding author. Email: oriel.kolln@uenp.edu.br

Summary

Ammonium has been reported as a ‘preferred’ nitrogen (N) source for sugarcane (Saccharum spp.), which can improve N use efficiency (NUE) in this crop. We aimed to evaluate the preferential uptake of ammonium and nitrate in sugarcane genotypes contrasting with NUE under controlled conditions. Four sugarcane genotypes previously selected by another experiment (ER: efficient and responsive; ENR: efficient and nonresponsive; IR: inefficient and responsive; INR: inefficient and nonresponsive) were grown in a growth chamber and fertilized with two 15N-labeled forms [(NH4)2SO4 (15N-NH4+) or KNO3 (15N-NO3)]; soil was used as substrate. Plants were evaluated at three time points: 0, 24, and 72 h after 15N-fertilization. For the efficient genotypes (ER and ENR), the soil NH4+ levels were about 20% lower than those found for the inefficient genotypes (IR and INR) indicating greater N extraction by the plant. Nitrogen derived from fertilizer (NDFF) and 15N recovery from fertilizer (15N RFF) in roots were influenced by the genotypes, in which responsive genotypes (ER and IR) presented a mean value 40% higher than the genotype INR, showing that greater absorption is more related to response than efficiency. Three days after N application, NDFF and 15N RFF from 15N-NH4+ were greater than 15N-NO3 in 40% and 65% for the roots and aerial part, respectively. The results of this study confirmed that sugarcane presents preferential uptake of NH4+ N form 3 days after fertilization. The use of nitrification inhibitors can be considered for providing a longer NH4+ residence time in the soil, also contributing to augmenting the NUE in sugarcane.

Type
Research Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Armas, R., Valadier, M.H., Champigny, M.L. and Lamaze, T. (1992). Influence of ammonium and nitrate on the growth and photosynthesis of sugarcane. Journal Plant Physiology 140, 531535. https://doi.org/10.1016/S0176-1617(11)80783-2 CrossRefGoogle Scholar
Associação Nacional para difusão de Adubos (ANDA) [National Association for the Diffusion of Fertilizers (ANDA)] (2019). Anuário estatístico setor de fertilizantes (Statistical yearbook of the fertilizer sector). São Paulo: Associação Nacional Para difusão de adubos. ISSN 0103-4790.Google Scholar
Barrie, A. and Prosser, S.J. (1996). Automated analysis of light–element stable isotopes by isotope ratio mass spectrometry. In Boutton, T.W. and Yamasaki, S. (eds.), Mass Spectrometry of Soils. New York: Marcel Dekker, pp. 146.Google Scholar
Barth, G., Otto, R., Almeida, R.F., Cardoso, E.J.B.N., Cantarella, H. and Vitti, G.C. (2020). Conversion of ammonium to nitrate and abundance of ammonium-oxidizing microorganism in Tropical soils with nitrification inhibitor. Scientia Agricola 77, 14. https://doi.org/10.1590/1678-992x-2018-0370 CrossRefGoogle Scholar
Boschiero, B.N., Mariano, E. and Trivelin, P.C.O. (2018). “Preferential” ammonium uptake by sugarcane does not increase the 15N recovery of fertilizer sources. Plant Soil 429, 253269. https://doi.org/10.1007/s11104-018-3672-z CrossRefGoogle Scholar
Boudsocq, S., Niboyet, A., Lata, J.C., Raynaud, X., Loeuille, N., Mathieu, J., Blouin, M., Abbadie, L. and Barot, S. (2012). Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? The American Naturalist 180, 6069. doi: 10.1086/665997 CrossRefGoogle ScholarPubMed
Bown, H.E., Watt, M.S., Clinton, P.W. and Mason, E.G. (2010). Influence of ammonium and nitrate supply on growth, dry matter partitioning, N uptake and photosynthetic capacity of (i) Pinus radiata (/i) seedlings. Trees – Structure and Function 24, 10971107. https://doi.org/10.1007/s00468-010-0482-1 CrossRefGoogle Scholar
Britto, D.T. and Kronzucker, H.J. (2005). Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant, Cell and Environment 28, 13961409. https://doi.org/10.1111/j.1365-3040.2005.01372.x CrossRefGoogle Scholar
Britto, D.T. and Kronzucker, H.J. (2013). Ecological significance and complexity of N–source preference in plants. Annals of Botany 112, 957963. doi: 10.1093/aob/mct157 CrossRefGoogle ScholarPubMed
Cantarella, H. (2007). Nitrogênio. In Novais, R.F., Alvarez, V.H.V., Barros, N.F., Fontes, R.L.F., Cantarutti, R.B and Neves, J.C.L. (eds), Fertilidade Do Solo. Viçosa: Sociedade Brasileira de Ciência do Solo, pp. 375470.Google Scholar
Crawford, D.M. and Chalk, P.M. (1993). Sources of N uptake by wheat ((i)Triticum aestivum (/i) L.) and N transformations in soil treated with a nitrification inhibitor (nitrapyrin). Plant Soil 149, 5972. https://doi.org/10.1007/BF00010763 CrossRefGoogle Scholar
Cuadros-Inostroza, Á., Caldana, C., Redestig, H., Kusano, M., Lisec, J., Peña-Cortés, H., Willmitzer, L. and Hannah, M.A. (2009). TargetSearch – a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics 10, 428. https://doi.org/10.1186/1471-2105-10-428 CrossRefGoogle ScholarPubMed
De Bona, F.D., Fedoseyenko, D., von Wirén, N. and Monteiro, F.A. (2011). Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form. Environmental Experimental Botany 74, 237244. https://doi.org/10.1016/j.envexpbot.2011.06.005 CrossRefGoogle Scholar
Fageria, N.K. and Baligar, V.C. (2005). Enhancing nitrogen use efficiency in crop plants. Advances in Agronomy 88, 97185. https://doi.org/10.1016/S0065-2113(05)88004-6 CrossRefGoogle Scholar
Fageria, N.K., Moreira, A., Moraes, L.C., Hale, A.L. and Viator, R.P. (2013). Sugarcane and energycane, Biofuel crops: Production, Physiology and Genetics. Wallingford: CABI.Google Scholar
Franco, H.C.J., Otto, R., Faroni, C.E., Vitti, A.C., Almeida de Oliveira, E.C. and Trivelin, P.C.O. (2011). Nitrogen in sugarcane derived from fertilizer under Brazilian field conditions. Field Crop Research 121, 2941. https://doi.org/10.1016/j.fcr.2010.11.011 CrossRefGoogle Scholar
Gerloff, G. (1976). Plant efficiencies in the use of nitrogen, phosphorus and potassium. In Wright, M.J. (ed), Plant Adaptation to Mineral Stress in Problem Soils. Ithaca: Cornell University Agricultural Experimental Station, pp. 161173.Google Scholar
Giavalisco, P., Li, Y., Matthes, A., Eckhardt, A., Hubberten, H.M., Hesse, H., Segu, S., Hummel, J., Khl, K. and Willmitzer, L. (2011). Elemental formula annotation of polar and lipophilic metabolites using 13C, 15N and 34S isotope labelling, in combination with high-resolution mass spectrometry. Plant Journal 68, 364376. doi: 10.1111/j.1365-313X.2011.04682.x CrossRefGoogle Scholar
Giné, M.F., Zagatto, E.A.G. and Reis, B.F. (1980). Simulataneous determination of nitrate and nitrite by flow injection analysis. Analytica Chimica Acta 114, 191197. https://doi.org/10.1016/S0003-2670(01)84290-2 CrossRefGoogle Scholar
Gupta, N., Gupta, A.K., Gaur, V.S. and Kumar, A. (2012). Relationship of nitrogen use efficiency with the activities of enzymes involved in nitrogen uptake and assimilation of finger millet genotypes Grown under different nitrogen inputs. Scientific World Journal 2012, 110. https://doi.org/10.1100/2012/625731 Google ScholarPubMed
Hajari, E., Snyman, S.J. and Watt, M.P. (2014). Inorganic nitrogen uptake kinetics of sugarcane (Saccharum spp.) varieties under in vitro conditions with varying N supply. Plant Cell Tissue Organ Culture 117, 361371. https://doi.org/10.1007/s11240-014-0445-0 CrossRefGoogle Scholar
Hajari, E., Snyman, S.J. and Watt, M.P. (2015). Nitrogen use efficiency of sugarcane (Saccharum spp.) varieties under in vitro conditions with varied N supply. Plant Cell, Tissue Organ Culture 122, 2129. https://doi.org/10.1007/s11240-015-0746-y CrossRefGoogle Scholar
Helali, S.M., Nebli, H., Kaddour, R., Mahmoudi, H., Lachaâl, M. and Ouerghi, Z. (2010). Influence of nitrate–ammonium ratio on growth and nutrition of Arabidopsis thaliana . Plant Soil 336, 6574. https://doi.org/10.1007/s11104-010-0445-8 CrossRefGoogle Scholar
Huege, J., Krall, L., Steinhauser, M.C., Giavalisco, P., Rippka, R., Marsac, N.T. and Steinhauser, D. (2011). Sample amount alternatives for data adjustment in comparative cyanobacterial metabolomics. Analytical and Bioanalytical Chemistry 399, 35033517. doi: 10.1007/s00216-011-4678-z CrossRefGoogle ScholarPubMed
International Fertilizer Industry Association – IFA (2017). Assessment of fertilizer use by crop at the global level [WWW Document]. Available at http://www.fertilizer.org (accessed 10 November 2021).Google Scholar
Koch, H., Galushko, A., Albertsen, M., Schintlmeister, A., Gruber-Dorninger, C., Lücker, S., Pelletier, E., Paslier, L.D., Spieck, E., Nielsen, P.H., Wagner, M. and Daims, H. (2014). Microbial metabolism: growth of nitrite- oxidizing bacteria by aerobic hydrogen oxidation. Science 345, 10521054. doi: 10.1126/science.1256985 CrossRefGoogle ScholarPubMed
Kölln, O.T. (2016). Eficiência de uso de nitrogênio pela cana–de–açúcar: diferenças genotípicas, preferência por amônio e emissão de N 2 O . PhD thesis, Center for Nuclear Energy in Agriculture. University of São Paulo, Brazil.Google Scholar
Lea, P.J., Blackwell, R.D., Chen, F.L. and Hecht, U. (1990). Enzymes of ammonia assimilation. In Lea, P.J. (ed), Methods in Plant Biochemistry: Volume 3 – Enzymes of Primary Metabolism. London: Academic Press, pp. 257276.CrossRefGoogle Scholar
Lin, C.H., Lerch, R.N., Garrett, H.E., Jordan, D. and George, M.F. (2007). Ability of forage grasses Exposed to atrazine and isoxaflutole to reduce nutrient levels in soils and shallow groundwater. Communication Soil Science and Plant Analyses 38, 11191136. https://doi.org/10.1080/00103620701327976 CrossRefGoogle Scholar
Loqué, D., Yuan, L., Kojima, S., Gojon, A., Wirth, J., Gazzarrini, S., Ishiyama, K., Takahashi, H. and von Wirén, N. (2006). Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant Journal 48, 522534.CrossRefGoogle ScholarPubMed
Mariano, E., Leite, J.M., Megda, M.X., Torres-Dorante, L. and Trivelin, P.C.O. (2015). Influence of nitrogen form supply on soil mineral nitrogen dynamics, nitrogen uptake, and productivity of sugarcane. Agronomy Journal 107, 641650. https://doi.org/10.2134/agronj14.0422 CrossRefGoogle Scholar
Masclaux-Daubresse, C., Daniel-Vedele, F., Dechorgnat, J., Chardon, F., Gaufichon, L. and Suzuki, A. (2010). Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105, 11411157. doi: 10.1093/aob/mcq028 CrossRefGoogle ScholarPubMed
Moll, R.H., Kamprath, E.J. and Jackson, W.A. (1982). Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agronomy Journal 74, 562564. https://doi.org/10.2134/agronj1982.00021962007400030037x CrossRefGoogle Scholar
Näsholm, T., Kielland, K. and Ganeteg, U. (2009). Uptake of organic nitrogen by plants. New Phytology 182, 3148. https://doi.org/10.1111/j.1469-8137.2008.02751.x CrossRefGoogle ScholarPubMed
Nelson, D.W. and Sommers, L.E. (1996). Total carbon, organic carbon and organic matter. In Sparks, D. L. (ed), Methods of Soil Analysis: Chemical Methods. Madison: ASA and SSSA, pp. 9611010.Google Scholar
O’Neal, D. and Joy, K.W. (1973). Glutamine synthetase of pea leaves. I. Purification, stabilization, and pH optima. Archives of Biochemistry and Biophysics 159, 113122. https://doi.org/10.1016/0003-9861(73)90435-9 CrossRefGoogle Scholar
Otto, R., Castro, S.A.Q., Mariano, E., Castro, S.G.Q., Franco, H.C.J. and Trivelin, P.C.O. (2016). Nitrogen use efficiency for sugarcane-biofuel production: what is next? Bioenergy Research 9, 12721289. https://doi.org/10.1007/s12155-016-9763-x CrossRefGoogle Scholar
Ranjith, S. and Meinzer, F.C. (1997). Physiological correlates of variation in nitrogen-use efficiency in two contrasting sugarcane cultivars. Crop Science 37, 818. https://doi.org/10.2135/cropsci1997.0011183X003700030021x CrossRefGoogle Scholar
Reis, B.F., Vieira, J.A., Krug, F.J. and Giné, M.F. (1997). Development of a flow injection system with two analytical paths for ammonium determination in soil extracts by conductometry. Journal of Brazilian Chemistry Society 8, 523528. https://doi.org/10.1590/S0103-50531997000500015.CrossRefGoogle Scholar
Robinson, N., Brackin, R., Vinall, K., Soper, F., Holst, J., Gamage, H., Paungfoo–Lonhienne, C., Rennenberg, H., Lakshmanan, P. and Schmidt, S. (2011). Nitrate paradigm does not hold up for sugarcane. PLoS One 6, 19 (e19045). https://doi.org/10.1371/journal.pone.0019045 CrossRefGoogle Scholar
Robinson, N., Fletcher, A., Whan, A., Critchley, C., von Wirén, N., Lakshmanan, P. and Schmidt, S. (2007). Sugarcane genotypes differ in internal nitrogen use efficiency. Functional Plant Biology 34, 11221129. https://doi.org/10.1071/FP07183 CrossRefGoogle Scholar
Robinson, N., Vogt, J., Lakshmanan, P. and Schmidt, S. (2013). Nitrogen physiology of sugarcane. In Moore, P.H. and Botha, F.C. (eds), Sugarcane: Physiology, Biochemistry, and Functional Biology. Chichester, UK: John Wiley & Sons Ltd, pp. 169195.CrossRefGoogle Scholar
Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L. and Fernie, A.R. (2001). Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13, 1129. https://doi.org/10.1105/tpc.13.1.11 CrossRefGoogle ScholarPubMed
Salsac, L., Chaillou, S., Morot–Gaudry, J., Lesaint, C. and Jolivet, E. (1987). Nitrate and ammonium nutrition in plants. Plant Physiology Biochemistry 25, 805812.Google Scholar
Schumann, A.W., Meyer, J.H. and Nair, S. (1998). Evidence for different nitrogen use efficiencies. Proceedings of the South African Sugar Technologists Association 72, 7780.Google Scholar
Sehtiya, H.L. and Goyal, S.S. (2000). Comparative uptake of nitrate by intact seedlings of C3 (barley) and C4 (corn) plants: effect of light and exogenously supplied sucrose. Plant Soil 3, 185186. https://doi.org/10.1023/A:1026503700825 CrossRefGoogle Scholar
Serezino, L.H.D. (2015). Caracterização fisiológica e transcricional dos processos de aquisição e remobilização de nitrato em cana-de-açúcar ((i)Saccharum (/i) spp.) [Physiological and transcriptional characterization of nitrate acquisition and remobilization processes in sugarcane ((i)Saccharum (/i) spp.)]. University of São Paulo, Center for Nuclear Energy in Agriculture.Google Scholar
Sheng-Xiu, L., Zhao-Hui, W. and Stewart, B.A. (2013). Responses of crop plants to ammonium and nitrate N. Advances in Agronomy 118, 205397. https://doi.org/10.1016/B978-0-12-405942-9.00005-0 Google Scholar
Shoemaker, H.E., McLean, E.O. and Pratt, P.F. (1961). Buffer methods for determining lime requirement of soils with appreciable amounts of extractable aluminum. Soil Science Society American Journal 25, 274277. https://doi.org/10.2136/sssaj1961.03615995002500040014x CrossRefGoogle Scholar
Siddiqi, M.Y. and Glass, A.D.M. (1981). Utilization index: a modified approach to the estimation and comparison of nutrient utilization efficiency in plants. Journal of Plant Nutrition 4, 289302. https://doi.org/10.1080/01904168109362919 CrossRefGoogle Scholar
Soil Survey Staff (2014). Keys to Soil Taxonomy. Soil Conservation Service.Google Scholar
Trivelin, P.C.O., Lara Cabezas, W.A.R., Victoria, R.L. and Reichardt, K. (1994). Evaluation of a 15N plot design for estimating plant recovery of fertilizer nitrogen applied to sugar cane. Scientia Agricola 51, 226234. https://doi.org/10.1590/S0103-90161994000200005 CrossRefGoogle Scholar
van Raij, B., Andrade, J.C., Cantarella, H. and Quaggio, J.A. (2001). Análise química para avaliação da fertilidade de solos tropicais (Chemical analysis to evaluate the fertility of tropical soils). Campinas: Instituto Agronômico.Google Scholar
Vieira-Megda, M.X., Mariano, E., Leite, J.M., Franco, H.C.J., Vitti, A.C., Megda, M.M., Khan, S.A., Mulvaney, R.L. and Trivelin, P.C.O. (2015). Contribution of fertilizer nitrogen to the total nitrogen extracted by sugarcane under Brazilian field conditions. Nutrient Cycling Agroecosystems 101, 241257. https://doi.org/10.1007/s10705-015-9676-7 CrossRefGoogle Scholar
Weckwerth, W., Loureiro, M.E., Wenzel, K. and Fiehn, O. (2004). Differential metabolic networks unravel the effects of silent plant phenotypes. Proceedings of the National Academy of Sciences 101, 78097814. https://doi.org/10.1073/pnas.0303415101 CrossRefGoogle ScholarPubMed
Whan, A., Robinson, N., Lakshmanan, P., Schmidt, S. and Aitken, K. (2010). A quantitative genetics approach to nitrogen use efficiency in sugarcane. Functional Plant Biology 37, 448. https://doi.org/10.1071/FP09260 CrossRefGoogle Scholar
Willianms, L.E. and Miller, A.J. (2001). Transporters responsible for the uptake and partitioning of nitrogeneous solutes. Annual Review Plant Physiology Plant Molecular Biology 52, 659688. doi: 10.1146/annurev.arplant.52.1.659 CrossRefGoogle Scholar
Wray, J.L. and Fido, R.J. (1990). Nitrate reductase and nitrite reductase. In Dey, P.M. and Harborne, J.B. (eds), Methods in Plant Biochemistry. London: Academic Press, pp. 241256.Google Scholar
Yang, M., Fang, Y., Sun, D. and Shi, Y. (2016). Efficiency of two nitrification inhibitors (dicyandiamide and 3, 4-dimethypyrazole phosphate) on soil nitrogen transformations and plant productivity: a meta-analysis. Scientific Report 110. https://doi.org/10.1038/srep22075 Google ScholarPubMed