Abstract
Aims
Understanding mechanisms underlying N use efficiency (NUE) after luxury consumption and nitrate deprivation is crucial to crop productivity. The aim was to elucidate the importance of photosynthesis, assimilatory nitrate reduction and N-reserve remobilization to NUE in cotton.
Methods
Plants were exposed to three conditions in nutrient solution: (a) previous exposure to high nitrate supply (10 mM) for long-term (8 days); (b) nitrate deprivation (NO3− withdrawal) for 8 days followed by (c) an early N-deficiency for 4 days.
Results
Plants supplied with nitrate excess were able to display increment in shoot NUE related to dry matter gain, whereas photosynthetic N use efficiency did not change, evidencing that excess N per se was not able to improve CO2 assimilation. Nitrate reductase (NR) activity was crucial to remobilize stored nitrate through deprivation phase and free amino acids, total proteins, and chlorophylls were also essential to N-remobilization. High NUE was important to kept high root growth rates throughout deprivation and early deficiency phases. Despite the great decrease in chlorophyll content, PSII and PSI activities were kept stable until the onset of early N-deficiency, when cotton plants displayed high shoot NUE.
Conclusions
These responses are closely associated with high NR activity and sustaining of photosynthesis, which contribute to N-homeostasis in different nutritional regimes.
Similar content being viewed by others
Abbreviations
- Y(NA):
-
Acceptor side limitation of PSI
- Chl:
-
Chlorophyll
- Y(ND):
-
Donor side limitation of PSI
- Y(II):
-
Effective quantum yield of PSII
- AA:
-
Free amino acids
- Fm:
-
Maximum fluorescence in the dark
- Fv/Fm:
-
Maximum potential quantum yield of PSII
- Fo:
-
Minimum fluorescence in the dark
- NUE:
-
N use efficiency
- PN :
-
Net CO2 assimilation
- NR:
-
Nitrate reductase
- Y(I):
-
Effective quantum yield of PSI
- qP:
-
Photochemical quenching coefficient
- PNUE:
-
Photosynthetic activity per N unity in leaves
- PPFD:
-
Photosynthetic photon flux density
- TSS:
-
Total soluble sugars
References
Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant kjeldahl digests. Commun Soil Sci Plant Anal 20:961–969
Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plant 4:46–54
Carpenter KL, Keidel TS, Pihl MC, Hughes NM (2014) Support for a photoprotective function of winter leaf reddening in nitrogen-deficient individuals of Lonicera japonica. Molecules 19:17810–17828
Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80
Cousins AB, Bloom AJ (2003) Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photo-assimilation in maize (Zea mays L.). Plant Cell Environ 26:1525–1530
da Rocha IMA, Vitorello VA, Silva JS, Ferreira-Silva SL, Viégas RA, Silva EN, Silveira JAG (2012) Exogenous ornithine is an effective precursor and the δ-ornithine amino transferase pathway contributes to proline accumulation under high N recycling in salt-stressed cashew leaves. J Plant Physiol 169:41–49
Devienne-Barret F, Justes E, Machet JM, Mary B (2000) Integrated control of nitrate uptake by crop growth rate and soil nitrate availability under field conditions. Ann Bot 86:995–1005
Diaz C, Lemaitre T, Christ A, Azzopardi M, Kato Y, Sato F, Morot-Gaudry J-F, Le Dily F, Masclaux-Daubresse C (2008) Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under low nitrogen nutrition. Plant Physiol 147:1437–1449
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Felker P (1977) Microdetermination of nitrogen in seed protein extracts with the salicylate-dichloroisocyanurate color reaction. Anal Chem 49:1080–1080
Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621
Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883
Guilherme EA, Carvalho FEL, Daloso DM, Silveira JAG (2019) Increase in assimilatory nitrate reduction and photorespiration enhances CO2 assimilation under high light-induced photoinhibition in cotton. Env Exp Bot 159:66–74
Hageman RH, Hucklesby DP (1971) Nitrate reduction from higher plants. Methods Enzymol 23:491–503
Hikosaka K, Terashima I, Katoh S (1994) Effects of leaf age, nitrogen nutrition and photon flux density on the distribution of nitrogen among leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Oecologia 97:451–457
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–32
Hsieh P, Kan C, Wu H, Yang H, Hsieh M (2018) Early molecular events associated with nitrogen deficiency in rice seedling roots. Sci Rep 8:1–23
Huang W, Yang YJ, Hu H, Zhang SB (2016) Response of the water-water cycle to the change in photorespiration in tobacco. J Photochem Photobiol Sci B - Biol 157:97–104
Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105:3–7
Jin X, Yang G, Tan C, Zhao C (2015) Effects of nitrogen stress on the photosynthetic CO2 assimilation, chlorophyll fluorescence, and sugar-nitrogen ratio in corn. Sci Rep 5:1–9
Kamada T, Kawai S (1989) An algorithm for drawing general undirected graphs. Inf Process Lett 31:7–15
Kant S (2018) Understanding nitrate uptake , signaling and remobilisation for improving plant nitrogen use efficiency. Semin Cell Dev Biol 74:89–96
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 57:707–714
Klughammer C, Schreiber U (2008a) Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Application Notes 1:27–35
Klughammer C, Schreiber U (2008b) Saturation pulse method for assessment of energy conversion in PSI. PAM Application Notes 1:11–14
Li Y, Ren B, Gao L, Ding L, Jiang D, Xu X, Shen Q, Guo S (2013) Less chlorophyll does not necessarily restrain light capture ability and photosynthesis in a chlorophyll-deficient rice mutant. J Agron Crop Sci 199:49–56
Makino A, Sato T, Nakano H, Mae T (1997) Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta 203:390–398
Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157
Mei H-S, Thimann KV (1984) The relation between nitrogen deficiency and leaf senescence. Physiol Plant 62:157–161
Noctor G, Foyer CH (1998) A re-evaluation of the ATP:NADPH budget during C photosynthesis : a contribution from nitrate assimilation and its associated respiratory activity? J Exp Bot 49:1895–1908
Ponte LFA, Silva ALC, Carvalho FEL, Maia JM, Voigt EL, Silveira JAG (2014) Salt-induced delay in cotyledonary globulin mobilization is abolished by induction of proteases and leaf growth sink strength at late seedling establishment in cashew. J Plant Physiol 171:1362–1371
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultameous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta - Gen Subj 975:384–396
Read JJ, Reddy KR, Jenkins JN (2006) Yield and fiber quality of upland cotton as influenced by nitrogen and potassium nutrition. Eur J Agron 24:282–290
Reed AJ, Below FE, Hageman RH (1980) Grain protein accumulation and the relationship between leaf nitrate reductase and protease activities during grain development in maize (Zea mays L.): I. variation between genotypes. Plant Physiol 66:164–170
Seemann JR, Sharkey TD, Wang J, Osmond CB (1987) Environmental effects on photosynthesis , nitrogen-use efficiency , and metabolite pools in leaves of sun and shade plants. Plant Physiol 84:796–802
Shaner DL, Boyer JS (1976) Nitrate reductase activity in maize ( Zea mays L .) leaves. Plant Physiol 58:499–504
Silveira JAG, de Almeida Viégas R, da Rocha IMA, de Oliveira Monteiro Moreira AC, de Azevedo Moreira R, Oliveira JTA (2003) Proline accumulation and glutamine synthetase activity are increased by salt-induced proteolysis in cashew leaves. J Plant Physiol 160(2):115–123
Souza GM, Ribeiro RV, Prado CHBA, Damineli DSC, Sato AM, Oliveira MS (2009) Using network connectance and autonomy analyses to uncover patterns of photosynthetic responses in tropical woody species. Ecol Com 6:15–26
Staswick PE (1994) Storage proteins of vegetative plant tissues. Annu Rev Plant Physiol Plant Mol Biol 45:303–322
Sun J, Ye M, Peng S, Li Y (2016) Nitrogen can improve the rapid response of photosynthesis to changing irradiance in rice (Oryza sativa L.) plants. Sci Rep 6:1–10
Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53
Tornkvist A, Liu C, Moschou P (2019) Proteolysis and nitrogen: emerging insights. J Exp Bot 70:2009–2019. https://doi.org/10.1093/jxb/erz024
van Handel E (1968) Direct microdetermination of sucrose. Anal Biochem 22:280–283
Vicente R, Pérez P, Martínez-Carrasco R, Morcuende R (2017) Improved responses to elevated CO2 in durum wheat at a low nitrate supply associated with the upregulation of photosynthetic genes and the activation of nitrate assimilation. Plant Sci 260:119–128
Walker BJ, Drewry DT, Slattery RA, Van Loocke A, Cho YB, Ort DR (2018) Chlorophyll can be reduced in crop canopies with little penalty to photosynthesis. Plant Physiol 176:1215–1232
Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122
Yamane Y, Kashino Y, Koike H, Satoh K (1997) Increases in the fluorescence F(o) level and reversible inhibition of photosystem II reaction center by high-temperature treatments in higher plants. Photosynth Res 52:57–64
Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–214
Zhao LS, Li K, Wang QM, Song XY, Su HN, Xie BB, Zhang XY, Huang F, Chen XL, Zhou BC, Zhang YZ (2017) Nitrogen starvation impacts the photosynthetic performance of porphyridium cruentum as revealed by chlorophyll a fluorescence. Sci Rep 7:1–11
Acknowledgements
The authors are grateful to Coordination for the Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES), National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq), INCT Plant Stress Biotech (Conselho de Desenvolvimento Científico e Tecnológico) Proc. 465480/2014-4 and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) for funding. FELC is supported by FUNCAP/CAPES (Bolsista CAPES/BRASIL – Proc. 88887.162856/2018-00). AKML is supported by CNPq (Proc. 154471/2018-6).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Responsible Editor: Philip John White.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 361 kb)
Rights and permissions
About this article
Cite this article
Guilherme, E.A., Nascimento, C.S., Lobo, A.K.M. et al. Nitrogen-utilization efficiency during early deficiency after a luxury consumption is improved by sustaining nitrate reductase activity and photosynthesis in cotton plants. Plant Soil 443, 185–198 (2019). https://doi.org/10.1007/s11104-019-04214-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04214-7