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Plant and Soil

, Volume 443, Issue 1–2, pp 185–198 | Cite as

Nitrogen-utilization efficiency during early deficiency after a luxury consumption is improved by sustaining nitrate reductase activity and photosynthesis in cotton plants

  • Eliezer A. Guilherme
  • Cristiano S. Nascimento
  • Ana K. M. Lobo
  • Fabricio E. L. CarvalhoEmail author
  • Joaquim A. G. SilveiraEmail author
Regular Article
  • 195 Downloads

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.

Keywords

Gossypium hirsutum Nitrate assimilation NUE N-nutrition Reserve remobilization 

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

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

11104_2019_4214_MOESM1_ESM.pdf (362 kb)
ESM 1 (PDF 361 kb)

References

  1. Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant kjeldahl digests. Commun Soil Sci Plant Anal 20:961–969Google Scholar
  2. Busch FA, Sage RF, Farquhar GD (2018) Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plant 4:46–54Google Scholar
  3. 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 19:17810–17828PubMedPubMedCentralGoogle Scholar
  4. 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 6:71–80Google Scholar
  5. 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 26:1525–1530Google Scholar
  6. 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 169:41–49PubMedGoogle Scholar
  7. 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 86:995–1005Google Scholar
  8. 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 147:1437–1449PubMedPubMedCentralGoogle Scholar
  9. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356Google Scholar
  10. Felker P (1977) Microdetermination of nitrogen in seed protein extracts with the salicylate-dichloroisocyanurate color reaction. Anal Chem 49:1080–1080Google Scholar
  11. 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 31:602–621PubMedGoogle Scholar
  12. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883PubMedPubMedCentralGoogle Scholar
  13. 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 159:66–74Google Scholar
  14. Hageman RH, Hucklesby DP (1971) Nitrate reduction from higher plants. Methods Enzymol 23:491–503Google Scholar
  15. 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 97:451–457PubMedGoogle Scholar
  16. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–32Google Scholar
  17. Hsieh P, Kan C, Wu H, Yang H, Hsieh M (2018) Early molecular events associated with nitrogen deficiency in rice seedling roots. Sci Rep 8:1–23Google Scholar
  18. 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 157:97–104Google Scholar
  19. Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105:3–7PubMedPubMedCentralGoogle Scholar
  20. 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 5:1–9Google Scholar
  21. Kamada T, Kawai S (1989) An algorithm for drawing general undirected graphs. Inf Process Lett 31:7–15Google Scholar
  22. Kant S (2018) Understanding nitrate uptake , signaling and remobilisation for improving plant nitrogen use efficiency. Semin Cell Dev Biol 74:89–96PubMedGoogle Scholar
  23. Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 57:707–714PubMedPubMedCentralGoogle Scholar
  24. 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 1:27–35Google Scholar
  25. Klughammer C, Schreiber U (2008b) Saturation pulse method for assessment of energy conversion in PSI. PAM Application Notes 1:11–14Google Scholar
  26. 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 199:49–56Google Scholar
  27. Makino A, Sato T, Nakano H, Mae T (1997) Leaf photosynthesis, plant growth and nitrogen allocation in rice under different irradiances. Planta 203:390–398Google Scholar
  28. 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 105:1141–1157PubMedPubMedCentralGoogle Scholar
  29. Mei H-S, Thimann KV (1984) The relation between nitrogen deficiency and leaf senescence. Physiol Plant 62:157–161Google Scholar
  30. 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 49:1895–1908Google Scholar
  31. 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 171:1362–1371PubMedGoogle Scholar
  32. 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 975:384–396Google Scholar
  33. Read JJ, Reddy KR, Jenkins JN (2006) Yield and fiber quality of upland cotton as influenced by nitrogen and potassium nutrition. Eur J Agron 24:282–290Google Scholar
  34. 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 66:164–170PubMedPubMedCentralGoogle Scholar
  35. 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 84:796–802PubMedPubMedCentralGoogle Scholar
  36. Shaner DL, Boyer JS (1976) Nitrate reductase activity in maize ( Zea mays L .) leaves. Plant Physiol 58:499–504PubMedPubMedCentralGoogle Scholar
  37. 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):115–123PubMedGoogle Scholar
  38. 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 6:15–26Google Scholar
  39. Staswick PE (1994) Storage proteins of vegetative plant tissues. Annu Rev Plant Physiol Plant Mol Biol 45:303–322Google Scholar
  40. 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 6:1–10Google Scholar
  41. Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53PubMedGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. van Handel E (1968) Direct microdetermination of sucrose. Anal Biochem 22:280–283PubMedGoogle Scholar
  44. 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 260:119–128PubMedGoogle Scholar
  45. 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 176:1215–1232PubMedGoogle Scholar
  46. Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122PubMedGoogle Scholar
  47. 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 52:57–64Google Scholar
  48. Yemm EW, Cocking EC, Ricketts RE (1955) The determination of amino-acids with ninhydrin. Analyst 80:209–214Google Scholar
  49. 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 7:1–11Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratory of Plant Metabolism, Department of Biochemistry and Molecular BiologyFederal University of CearáFortalezaBrazil

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