Skip to main content

Low nitrogen stress regulates chlorophyll fluorescence in coordination with photosynthesis and Rubisco efficiency of rice

Abstract

Nitrogen (N) is the basis of plant growth and development and, is considered as one of the priming agents to elevate a range of stresses. Plants use solar radiations through photosynthesis, which amasses the assimilatory components of crop yield to meet the global demand for food. Nitrogen is the main regulator in the allocation of photosynthetic apparatus which changes of the photosynthesis (Pn) and quantum yield (Fv/Fm) of the plant. In the present study, dynamics of the photosynthetic establishment, N-dependent relation with chlorophyll fluorescence attributes and Rubisco efficacy was evaluated in low-N tolerant (cv. CR Dhan 311) and low-N sensitive (cv. Rasi) rice cultivars under low-N and optimum-N conditions. There was a decrease in the stored leaf N under low-N condition, resulting in the decreased Pn and Fv/Fm efficiency of the plants through depletion in the activity and content of Rubisco. The Pn and Fv/Fm followed the parallel trend of leaf N content during low-N condition along with depletion of intercellular CO2 concentration and overall conductance under low-N condition. Photosynthetic saturation curve cleared abrupt decrease of effective quantum yield in the low-N sensitive rice cultivar than the low-N tolerant rice. Also, the rapid light curve highlighted the unacclimated regulation of photochemical and non-photochemical quenching in the low-N condition. The low-N sensitive rice cultivar triumphed non-photochemical quenching, whereas the low-N tolerant rice cultivar rose gradually during the light curve. Our study suggested that the quantum yield is the key limitation for photosynthesis in low-N condition. Regulation of Rubisco, photochemical and non-photochemical quenching may help plants to grow under low-N level.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

cv.:

Cultivar

Ci :

Inter-cellular concentration of CO2

ETR:

Electron transfer rate

Fv/Fm :

Maximum photochemical quantum yield

LNC:

Leaf nitrogen content

NPQ:

Non-photochemical fluorescence quenching

PAR:

Photosynthetically active radiation

Pn :

Net photosynthesis

PSC:

Photosynthesis saturation curve

PSII:

Photosystem II

qP:

Photochemical fluorescence quenching

RLC:

Rapid light curve

Rubisco:

Ribulose bisphosphate carboxylase/oxygenase

SP:

Saturation pulse

Y(II):

Effective photochemical quantum yield

References

  1. Baggs E, Rees R, Smith K, Vinten A (2000) Nitrous oxide emission from soils after incorporating crop residues. Soil Use Manag 16:82–87. https://doi.org/10.1111/j.1475-2743.2000.tb00179.x

    Article  Google Scholar 

  2. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998. https://doi.org/10.1104/pp.008250

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Bharti RK, Srivastava S, Thakur IS (2014) Proteomic analysis of carbon concentrating chemolithotrophic bacteria Serratia sp. for sequestration of carbon dioxide. PloS One 9(3):e91300. https://doi.org/10.1371/journal.pone.0091300

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Cao X, Zhu C, Zhong C, Hussain S, Zhu L, Wu L, Jin Q (2018) Mixed-nitrogen nutrition-mediated enhancement of drought tolerance of rice seedlings associated with photosynthesis, hormone balance and carbohydrate partitioning. Plant Growth Regul 84:451–465. https://doi.org/10.1007/s10725-017-0352-6

    Article  CAS  Google Scholar 

  5. Carmo-Silva E, Scales JC, Madgwick PJ, Parry MA (2015) Optimizing Rubisco and its regulation for greater resource use efficiency. Plant Cell Environ 38(9):1817–1832

    Article  CAS  Google Scholar 

  6. Carvalho L, Esquível M, Martins I, Ricardo CP, Amâncio S (2005) Monitoring the stability of Rubisco in micro propagated grapevine (Vitis vinifera L.) by two-dimensional electrophoresis. J Plant Physiol 162:365–374. https://doi.org/10.1016/j.jplph.2004.09.013

    Article  PubMed  CAS  Google Scholar 

  7. Cen H, Weng H, Yao J, He M, Lv J, Hua S, Li H, He Y (2017) Chlorophyll fluorescence imaging uncovers photosynthetic fingerprint of Citrus huanglongbing. Front Plant Sci 8:1509. https://doi.org/10.3389/fpls.2017.01509

    Article  PubMed  PubMed Central  Google Scholar 

  8. Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S (2018) Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiol Plant 164:349–363. https://doi.org/10.1111/ppl.12737

    Article  PubMed  CAS  Google Scholar 

  9. Fan M, Shen J, Yuan L, Jiang R, Chen X, Davies WJ, Zhang F (2011) Improving crop productivity and resource use efficiency to ensure food security and environmental quality in China. J Exp Bot 63:13–24. https://doi.org/10.1093/jxb/err248

    Article  PubMed  CAS  Google Scholar 

  10. Hou W, Yan J, Jákli B, Lu J, Ren T, Cong R, Li X (2018) Synergistic effects of nitrogen and potassium on quantitative limitations to photosynthesis in rice (Oryza sativa L.). J Agric Food Chem 66:5125–5132. https://doi.org/10.1021/acs.jafc.8b01135

    Article  PubMed  CAS  Google Scholar 

  11. Humplík JF, Lazár D, Fürst T, Husičková A, Hýbl M, Spíchal L (2015) Automated integrative high-throughput phenotyping of plant shoots: a case study of the cold-tolerance of pea (Pisum sativum L.). Plant Methods 11:20. https://doi.org/10.1186/s13007-015-0063-9

    Article  PubMed  PubMed Central  Google Scholar 

  12. Jimenez RR, Ladha JK (1993) Automated elemental analysis: a rapid and reliable but expensive measurement of total carbon and nitrogen in plant and soil samples. Commun Soil Sci Plant Anal 24:1897–1924. https://doi.org/10.1080/00103629309368926

    Article  CAS  Google Scholar 

  13. 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 5:9311. https://doi.org/10.1038/srep09311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Juneau P, Green B, Harrison P (2005) Simulation of Pulse-Amplitude-Modulated (PAM) fluorescence: limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica 43:75–83. https://doi.org/10.1007/s11099-005-5083-7

    Article  CAS  Google Scholar 

  15. Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V (2014) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem 81:16–25. https://doi.org/10.1016/j.plaphy.2014.03.029

    Article  PubMed  CAS  Google Scholar 

  16. Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354(6314):857–861. https://doi.org/10.1126/science.aai8878

    Article  PubMed  CAS  Google Scholar 

  17. Kumagai E, Hamaoka N, Araki T, Ueno O (2014) Dorsoventral asymmetry of photosynthesis and photoinhibition in flag leaves of two rice cultivars that differ in nitrogen response and leaf angle. Physiol Plant 151:533–543. https://doi.org/10.1111/ppl.12145

    Article  PubMed  CAS  Google Scholar 

  18. Kursar TA, Alberte RS (1983) Photosynthetic unit organization in a red alga: relationships between light-harvesting pigments and reaction centers. Plant Physiol 72:409–414. https://doi.org/10.1104/pp.72.2.409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Lawlor D, Boyle F, Young A, Keys A, Kendall A (1987) Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves. J Exp Bot 38:393–408. https://doi.org/10.1093/jxb/38.3.393

    Article  Google Scholar 

  20. Li P, Weng J, Zhang Q, Yu L, Yao Q, Chang L, Niu Q (2018) Physiological and biochemical responses of Cucumis melo L. chloroplasts to low-phosphate stress. Front Plant Sci 9:1525. https://doi.org/10.3389/fpls.2018.01525

    Article  PubMed  PubMed Central  Google Scholar 

  21. Liu T, Ren T, White PJ, Cong R, Lu J (2018) Storage nitrogen co-ordinates leaf expansion and photosynthetic capacity in winter oilseed rape. J Exp Bot 69:2995–3007. https://doi.org/10.1093/jxb/ery134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Makino A, Sakuma H, Sudo E, Mae T (2003) Differences between maize and rice in N-use efficiency for photosynthesis and protein allocation. Plant Cell Physiol 44:952–956. https://doi.org/10.1093/pcp/pcg113

    Article  PubMed  CAS  Google Scholar 

  23. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence -a practical guide. J Exp Bot 51:659–668. https://doi.org/10.1093/jexbot/51.345.659

    Article  PubMed  CAS  Google Scholar 

  24. Nunes MA, Ramalho JC, Dias MA (1993) Effect of nitrogen supply on the photosynthetic performance of leaves from coffee plants exposed to bright light. J Exp Bot 44:893–899. https://doi.org/10.1093/jxb/44.5.893

    Article  CAS  Google Scholar 

  25. Pan C, Ahammed GJ, Li X, Shi K (2018) Elevated CO2 improves photosynthesis under high temperature by attenuating the functional limitations to energy fluxes, electron transport and redox homeostasis in tomato leaves. Front Plant Sci 9:1739. https://doi.org/10.3389/fpls.2018.01739

    Article  PubMed  PubMed Central  Google Scholar 

  26. Rascher U, Liebig M, Lüttge U (2000) Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant Cell Environ 23:1397–1405. https://doi.org/10.1046/j.13653040.2000.00650.x

    Article  CAS  Google Scholar 

  27. Sakai H, Hasegawa T, Kobayashi K (2006) Enhancement of rice canopy carbon gain by elevated CO2 is sensitive to growth stage and leaf nitrogen concentration. N Phytol 170:321–332. https://doi.org/10.1111/j.1469-8137.2006.01688.x

    Article  CAS  Google Scholar 

  28. Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Huang Liu Q, Yuan XQ (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652. https://doi.org/10.1038/ng.2958

    Article  PubMed  CAS  Google Scholar 

  29. Terashima I, Evans JR (1988) Effects of light and nitrogen nutrition on the organization of the photosynthetic apparatus in spinach. Plant Cell Physiol 29:143–155. https://doi.org/10.1093/oxfordjournals.pcp.a077461

    Article  CAS  Google Scholar 

  30. Tremblay N, Wang Z, Cerovic ZG (2012) Sensing crop nitrogen status with fluorescence indicators. A review. Agron Sustain Dev 32:451–464. https://doi.org/10.1007/s13593-011-0041-1

    Article  CAS  Google Scholar 

  31. Usuda H (1985) The activation state of ribulose 1, 5-bisphosphate carboxylase in maize leaves in dark and light. Plant Cell Physiol 26:1455–1463. https://doi.org/10.1093/oxfordjournals.pcp.a077047

    Article  CAS  Google Scholar 

  32. Wang X, Kolattukudy PE (1996) Isolation of a protein containing covalently linked large and small subunits of ribulose-1, 5-bisphosphate carboxylase/oxygenase from Botryococcus braunii. Plant Physiol 111(2):441–445. https://doi.org/10.1104/pp.111.2.441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Ware MA, Belgio E, Ruban AV (2014) Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. J Exp Bot 66(5):1259–1270. https://doi.org/10.1093/jxb/eru477

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Xiaochuang C, Chu Z, Lianfeng Z, Junhua Z, Hussain S, Lianghuan W, Qianyu J (2017) Glycine increases cold tolerance in rice via the regulation of N uptake, physiological characteristics, and photosynthesis. Plant Physiol Biochem 112:251–260

    Article  CAS  Google Scholar 

  35. Yang J, Gong W, Shi S, Du L, Sun J, Song S, Chen B, Zhang Z (2016) Analyzing the performance of fluorescence parameters in the monitoring of leaf nitrogen content of paddy rice. Sci Rep 6:28787. https://doi.org/10.1038/srep28787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  36. Yokoya NS, Necchi O, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 19:197–205. https://doi.org/10.1007/s10811-006-9124-9

    Article  CAS  Google Scholar 

  37. Yousuf PY, Abdallah EF, Nauman M, Asif A, Hashem A, Alqarawi AA, Ahmad A (2017) Responsive proteins in wheat cultivars with contrasting nitrogen efficiencies under the combined stress of high temperature and low nitrogen. Genes 8:356. https://doi.org/10.3390/genes8120356

    Article  PubMed Central  CAS  Google Scholar 

  38. Zhao LS, Li K, Wang QM, Song XY, Su HN, Xie BB, Zhang XY, Huang F, Chen XL, Zhou BC (2017) Nitrogen starvation impacts the photosynthetic performance of Porphyridium cruentum as revealed by chlorophyll fluorescence. Sci Rep 7:8542. https://doi.org/10.1038/s41598-017-08428-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Zhong C, Cao X, Bai Z, Zhang J, Zhu L, Huang J, Jin Q (2018) Nitrogen metabolism correlates with the acclimation of photosynthesis to short-term water stress in rice (Oryza sativa L.). Plant Physiol Biochem 125:52–62. https://doi.org/10.1016/j.plaphy.2018.01.024

    Article  PubMed  CAS  Google Scholar 

  40. Zhou X, Sun C, Zhu P, Liu F (2018) Effects of antimony stress on photosynthesis and growth of Acorus calamus. Front Plant Sci 9:579. https://doi.org/10.3389/fpls.2018.00579

    Article  PubMed  PubMed Central  Google Scholar 

  41. Živcak M, Olsovska K, Slamka P, Galambosova J, Rataj V, Shao HB, Kalaji HM, Brestic M (2014) Measurements of chlorophyll fluorescence in different leaf positions may detect nitrogen deficiency in wheat. Zemdirbyste 101:437–444. https://doi.org/10.13080/z-a.2014.101.056

    Article  Google Scholar 

Download references

Funding

This work was supported by research Grants from DBT-NEWS-India-UK (BT/IN/UK-VNC/44/NR/2015-16).

Author information

Affiliations

Authors

Contributions

A. Ahmad conception and design of the study, acquisition of data, analysis, and interpretation of data, drafting the article and final approval of the submitted version. The author takes responsibility for the integrity of the article as a whole. aahmad.bo@amu.ac.in. A.Y. Tantray conception and design of the study, acquisition of data, interpretation of data, drafting the article, final approval. S.S. Bashir conception of the study, acquisition of data, analysis, and interpretation of data, final approval.

Corresponding author

Correspondence to Altaf Ahmad.

Ethics declarations

Conflict of interest

All authors have declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 12 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tantray, A.Y., Bashir, S.S. & Ahmad, A. Low nitrogen stress regulates chlorophyll fluorescence in coordination with photosynthesis and Rubisco efficiency of rice. Physiol Mol Biol Plants 26, 83–94 (2020). https://doi.org/10.1007/s12298-019-00721-0

Download citation

Keywords

  • Net photosynthesis
  • Nitrogen
  • Quantum yield
  • Rapid light curve
  • Rice (Oryza sativa L.)