Photosynthetica 2024, 62(3):252-262 | DOI: 10.32615/ps.2024.028

Physiological response to low-nitrogen stress and comprehensive evaluation in four rice varieties

Y.F. ZHANG, H. CAI, E.T. YOU, X.Q. QIAO, Z.P. GAO, G.X. CHEN
College of Life Sciences, Nanjing Normal University, 210023 Nanjing, China

Rice (Oryza sativa L.) research has rarely focused on the response to low-nitrogen stress in different subtypes previously and lacked a low-nitrogen tolerance evaluation system. Here, we investigated the physiological characteristics under moderate and low-nitrogen stress conditions in two japonica cultivars (NG46 and NG9108) and two indica cultivars (LYP9 and 9311). Using subordinate function analysis and principal component analysis, the low-nitrogen tolerance of four rice varieties was comprehensively evaluated; stomatal conductance, total carotenoid content, and nitrate reductase NR activity were taken as the low-nitrogen tolerance evaluation system. Among the four rice cultivars, NG46 and LYP9 had significant advantages in photosynthetic gas-exchange capacity, optimizing the balance between light-harvesting capacity, the ratio of reaction center inactivation, the magnitude of decrease in heat dissipation, and nitrogen-metabolism enzyme activities. The results investigated the physiological mechanisms of rice adaptation to low-nitrogen stress and offered a reliable method for assessing low-nitrogen tolerance in rice.

Additional key words: low-nitrogen tolerance evaluation; nitrogen metabolism; photosynthesis; rice; subordinate function analysis.

Received: March 11, 2024; Revised: July 2, 2024; Accepted: July 26, 2024; Prepublished online: August 6, 2024; Published: October 14, 2024  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
ZHANG, Y.F., CAI, H., YOU, E.T., QIAO, X.Q., GAO, Z.P., & CHEN, G.X. (2024). Physiological response to low-nitrogen stress and comprehensive evaluation in four rice varieties. Photosynthetica, 62(3), 252-262. doi: 10.32615/ps.2024.028
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileZhang_3104_supplement-Table_1S.xlsx

    File size: 10.79 kB

    Download fileZhang_3104_supplement-Table_2S.xlsx

    File size: 10.75 kB

    References

    1. Akhter M.S., Noreen S., Mahmood S. et al.: Influence of salinity stress on PSII in barley (Hordeum vulgare L.) genotypes, probed by chlorophyll-a fluorescence. - J. King Saud Univ. Sci. 33: 101239, 2021. Go to original source...
    2. Arnon D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
    3. Beckmann J., Lehr F., Finazzi G. et al.: Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. - J. Biotechnol. 142: 70-77, 2009. Go to original source...
    4. Bo W., Fu B., Qin G. et al.: Evaluation of drought resistance in Iris germanica L. based on subordination function and principal component analysis. - Emir. J. Food Agric. 29: 770-778, 2017. Go to original source...
    5. Cao X., Jiang F., Wang X. et al.: Comprehensive evaluation and screening for chilling-tolerance in tomato lines at the seedling stage. - Euphytica 205: 569-584, 2015. Go to original source...
    6. Chen X., Min D., Yasir T.A., Hu Y.-G.: Evaluation of 14 morphological, yield-related and physiological traits as indicators of drought tolerance in Chinese winter bread wheat revealed by analysis of the membership function value of drought tolerance (MFVD). - Field Crop. Res. 137: 195-201, 2012. Go to original source...
    7. Chen Z., Niu J., Guo Z. et al.: Graphene enhances photosynthesis and the antioxidative defense system and alleviates salinity and alkalinity stresses in alfalfa (Medicago sativa L.) by regulating gene expression. - Environ. Sci.-Nano 8: 2731-2748, 2021. Go to original source...
    8. Dahlin A.S., Marstorp H.: Release pattern from green manures can be modified through species composition. - Acta Agr. Scand. B-S. P. 62: 659-665, 2012. Go to original source...
    9. Deng Y., Sun X., Zhang Q. et al.: Comprehensive evaluation and physiological response of quinoa genotypes to low nitrogen. - Agronomy 13: 1597, 2023. Go to original source...
    10. Dong H.Z., Li W.J., Tang W. et al.: Effects of genotypes and plant density on yield, yield components and photosynthesis in Bt transgenic cotton. - J. Agron. Crop Sci. 192: 132-139, 2006. Go to original source...
    11. Farnden K.J.F., Robertson J.G.: Methods for studying enzymes involved in metabolism related to nitrogenase. - In: Bergersen F.J. (ed.): Methods for Evaluating Biological Nitrogen Fixation. Pp. 265-314. Portland Press, Chichester 1980.
    12. Filacek A., Zivcak M., Barboricova M. et al.: Diversity of responses to nitrogen deficiency in distinct wheat genotypes reveals the role of alternative electron flows in photoprotection. - Photosynth. Res. 154: 259-276, 2022. Go to original source...
    13. Fuentes S.I, Allen D.J, Ortiz-Lopez A., Hernández G.: Over-expression of cytosolic glutamine synthetase increases photosynthesis and growth at low nitrogen concentrations. - J. Exp. Bot. 52: 1071-1081, 2001. Go to original source...
    14. Gao D., Ran C., Zhang Y. et al.: Effect of different concentrations of foliar iron fertilizer on chlorophyll fluorescence characteristics of iron-deficient rice seedlings under saline sodic conditions. - Plant Physiol. Biochem. 185: 112-122, 2022. Go to original source...
    15. Gong X.W., Liu C.J., Ferdinand U. et al.: Effect of intercropping on leaf senescence related to physiological metabolism in proso millet (Panicum miliaceum L.). - Photosynthetica 57: 993-1006, 2019. Go to original source...
    16. Haegele J.W., Cook K.A., Nichols D.M., Below F.E.: Changes in nitrogen use traits associated with genetic improvement for grain yield of maize hybrids released in different decades. - Crop Sci. 53: 1256-1268, 2013. Go to original source...
    17. Han M., Okamoto M., Beatty P.H. et al.: The genetics of nitrogen use efficiency in crop plants. - Annu. Rev. Genet. 49: 269-289, 2015. Go to original source...
    18. Hlahla J.M., Mafa M.S., van der Merwe R. et al.: The photosynthetic efficiency and carbohydrates responses of six edamame (Glycine max. L. Merrill) cultivars under drought stress. - Plants-Basel 11: 394, 2022. Go to original source...
    19. Hu B., Wang W., Ou S. et al.: Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. - Nat. Genet. 47: 834-838, 2015. Go to original source...
    20. Jiang D., Lu B., Liu L. et al.: Exogenous melatonin improves the salt tolerance of cotton by removing active oxygen and protecting photosynthetic organs. - BMC Plant Biol. 21: 331, 2021. Go to original source...
    21. Jin H., Li M., Duan S. et al.: Optimization of light-harvesting pigment improves photosynthetic efficiency. - Plant Physiol. 172: 1720-1731, 2016. Go to original source...
    22. Ju C., Buresh R.J., Wang Z. et al.: Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. - Field Crop. Res. 175: 47-55, 2015. Go to original source...
    23. Kalaji H.M., Oukarroum A., Alexandrov V. et al.: Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. - Plant Physiol. Biochem. 81: 16-25, 2014a. Go to original source...
    24. Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. - Photosynth. Res. 122: 121-158, 2014b. Go to original source...
    25. Kishorekumar R., Bulle M., Wany A., Gupta K.J.: An overview of important enzymes involved in nitrogen assimilation of plants. - In: Gupta K.J. (ed.): Nitrogen Metabolism in Plants: Methods and Protocols. Pp. 1-13. Humana, New York 2020. Go to original source...
    26. Kitajima K., Hogan K.P.: Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. - Plant Cell Environ. 26: 857-865, 2003. Go to original source...
    27. Krapp A.: Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. - Curr. Opin. Plant Biol. 25: 115-122, 2015. Go to original source...
    28. Kusano M., Fukushima A., Redestig H., Saito K.: Metabolomic approaches toward understanding nitrogen metabolism in plants. - J. Exp. Bot. 62: 1439-1453, 2011. Go to original source...
    29. Li W., Mo W., Ashraf U. et al.: Evaluation of physiological indices of waterlogging tolerance of different maize varieties in South China. - Appl. Ecol. Env. Res. 16: 2059-2072, 2018. Go to original source...
    30. Li X., Cao K., Wang C. et al.: Variation of photosynthetic tolerance of rice cultivars (Oryza sativa L.) to chilling temperature in the light. - Afr. J. Biotechnol. 9: 1325-1337, 2010. Go to original source...
    31. Liang X.L., Fang S.M., Ji W.B., Zheng D.F.: The positive effects of silicon on rice seedlings under saline-alkali mixed stress. - Commun. Soil Sci. Plant Anal. 46: 2127-2138, 2015. Go to original source...
    32. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
    33. Lin C.C., Kao C.H.: Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl. - Plant Growth Regul. 18: 233-238, 1996. Go to original source...
    34. Liu C., Gong X., Wang H. et al.: Low-nitrogen tolerance comprehensive evaluation and physiological response to nitrogen stress in broomcorn millet (Panicum miliaceum L.) seedling. - Plant Physiol. Biochem. 151: 233-242, 2020. Go to original source...
    35. Luo J., Li H., Liu T. et al.: Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. - J. Exp. Bot. 64: 4207-4224, 2013. Go to original source...
    36. Ma N., Hu C., Wan L. et al.: Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. - Front. Plant Sci. 8: 1671, 2017. Go to original source...
    37. Maeda S., Konishi M., Yanagisawa S., Omata T.: Nitrite transport activity of a novel HPP family protein conserved in cyanobacteria and chloroplasts. - Plant Cell Physiol. 55: 1311-1324, 2014. Go to original source...
    38. Matsubara S., Förster B., Waterman M. et al.: From ecophysiology to phenomics: some implications of photoprotection and shade-sun acclimation in situ for dynamics of thylakoids in vitro. - Philos. T. Roy. Soc. B 367: 3503-3514, 2012. Go to original source...
    39. Miao J., Shi F., Li W. et al.: Comprehensive screening of low nitrogen tolerant maize based on multiple traits at the seedling stage. - PeerJ 10: e14218, 2022. Go to original source...
    40. Pei X., Wang J., Dang J. et al.: [An approach to the screening index for low nitrogen tolerant wheat genotype.] - J. Plant Nutr. Fertil. 13: 93-98, 2007. [In Chinese]
    41. Perrine Z., Negi S., Sayre R.T.: Optimization of photosynthetic light energy utilization by microalgae. - Algal Res. 1: 134-142, 2012. Go to original source...
    42. Plett D., Baumann U., Schreiber A.W. et al.: Maize maintains growth in response to decreased nitrate supply through a highly dynamic and developmental stage-specific transcriptional response. - Plant Biotechnol. J. 14: 342-353, 2016. Go to original source...
    43. Singh J., Thakur J.K.: Photosynthesis and abiotic stress in plants. - In: Vats S. (ed.): Biotic and Abiotic Stress Tolerance in Plants. Pp. 27-46. Springer, Singapore 2018. Go to original source...
    44. Sivakumar J., Prashanth J.E.P., Rajesh N. et al.: Principal component analysis approach for comprehensive screening of salt stress-tolerant tomato germplasm at the seedling stage. - J. Biosci. 45: 141, 2020. Go to original source...
    45. Skopelitis D.S., Paranychianakis N.V., Paschalidis K.A. et al.: Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. - Plant Cell 18: 2767-2781, 2006. Go to original source...
    46. Stitt M., Müller C., Matt P. et al.: Steps towards an integrated view of nitrogen metabolism. - J. Exp. Bot. 53: 959-970, 2002. Go to original source...
    47. Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321-362. Springer, Dordrecht 2004. Go to original source...
    48. 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. Pla. 26: 83-94, 2020. Go to original source...
    49. Tian J., Pang Y., Yuan W. et al.: Growth and nitrogen metabolism in Sophora japonica (L.) as affected by salinity under different nitrogen forms. - Plant Sci. 322: 111347, 2022. Go to original source...
    50. Vialet-Chabrand S., Matthews J.S.A., Simkin A.J. et al.: Importance of fluctuations in light on plant photosynthetic acclimation. - Plant Physiol. 173: 2163-2179, 2017. Go to original source...
    51. Wen B., Li C., Fu X. et al.: Effects of nitrate deficiency on nitrate assimilation and chlorophyll synthesis of detached apple leaves. - Plant Physiol. Biochem. 142: 363-371, 2019. Go to original source...
    52. Weng J., Li P., Rehman A. et al.: Physiological response and evaluation of melon (Cucumis melo L.) germplasm resources under high temperature and humidity stress at seedling stage. - Sci. Hortic.-Amsterdam 288: 110317, 2021. Go to original source...
    53. Xu G., Jiang M., Lu D. et al.: [Optimum combination of irrigation and nitrogen supply form achieving high photosynthetic and nitrogen utilization efficiency.] - J. Plant Nutr. Fertil. 26: 1239-1250, 2020. [In Chinese]
    54. Xuan W., Beeckman T., Xu G.: Plant nitrogen nutrition: sensing and signaling. - Curr. Opin. Plant Biol. 39: 57-65, 2017. Go to original source...
    55. Zhang T.-J., Zheng J., Yu Z.-C. et al.: Variations in photoprotective potential along gradients of leaf development and plant succession in subtropical forests under contrasting irradiances. - Environ. Exp. Bot. 154: 23-32, 2018. Go to original source...
    56. Zheng X., Yu Z., Zhang Y., Shi Y.: Effect of nitrogen rates on wheat photosynthesis, anatomical parameters and photoassimilate partitioning in North China Plain. - Int. J. Plant Prod. 15: 161-172, 2021. Go to original source...
    57. Zou C.L., Huang K.J., Zhai R.N. et al.: [Evaluation of drought resistance of maize during germination stage based on membership function method and principal components analysis.] - Jiangsu Agric. Sci. 50: 7-13, 2022. [In Chinese]

    Return to the content