Abstract
Main conclusion
Early-stage low nitrogen priming promotes root growth and delays leaf senescence through gene expression, enhancing nitrogen absorption and assimilation in wheat seedlings, thereby alleviating growth inhibition under nitrogen deficit stress and supporting normal seedling development.
Abstract
Verifying the strategies to reduce the amount of nitrogen (N) fertilizer while maintaining high crop yields is important for improving crop N use efficiency (NUE) and protecting the environment. To determine whether low N (LN) priming (LNP) can alleviate the impact of N-deficit stress on the growth of wheat seedlings and improve their tolerance to N-deficit stress, we conducted hydroponic experiments using two wheat cultivars, Yangmai 158 (YM158, LN tolerant) and Zaoyangmai (ZYM, LN sensitive) to study the effects of LNP on wheat seedlings under N-deficit stress. N-deficit stress decreased the plant dry weight, leaf area, and leaf N content (LNC), while LNP could significantly reduce this reduction. Distinct sensitivities to N-deficit stress were observed between the wheat cultivars, with ZYM showing an early decrease in leaf N content compared to YM158, which exhibited a late-stage reduction. LNP promoted root growth, expanded N uptake area, and upregulated the expression of TaNRT1.1, TaNRT2.1, and TaNRT2.2 in wheat seedlings, suggesting that LNP can enhance root N uptake capacity to increase N accumulation in plants. In addition, LNP improved the activity of glutamine synthase (GS) to enhance the capacity of N assimilation of plants. The relative expression of TaGS1 in the lower leaves of priming and stress (PS) was lower than that of no priming and stress (NS) after LNP, indicating that the rate of N transfer from the lower leaves to the upper leaves became slower after LNP, which alleviated the senescence of the lower leaves. The relative expression of TaGS2 was significantly increased, which might be related to the enhanced photorespiratory ammonia assimilation capacity after LNP, which reduced the N loss and maintained higher LNC. Therefore, LNP in the early stage can improve the N absorption and assimilation ability and maintain the normal N supply to alleviate the inhibition of N-deficit stress in wheat seedlings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.
Abbreviations
- N:
-
Nitrogen
- GS:
-
Glutamine synthase
- HATS:
-
High-affinity transport system
- LATS:
-
Low-affinity transport system
- LN:
-
Low nitrogen
- LNP:
-
Low nitrogen priming
- LNC:
-
Leaf nitrogen content
- NUE:
-
Nitrogen use efficiency
- NR:
-
Nitrite reductase
- NN:
-
No priming + no stress
- NS:
-
No priming + stress
- PN:
-
Priming + no stress
- PS:
-
Priming + stress
- YM158:
-
Yangmai 158
- ZYM:
-
Zaoyangmai
References
Baki GK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays under salinity. Plant Cell Environ 23(5):515–521. https://doi.org/10.1046/j.1365-3040.2000.00568.x
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analy Biochem 72(1-2):248–254. https://doi.org/10.1006/abio.1976.9999
Fan X, Naz M, Fan X, Xuan W, Miller A, Xu G (2017) Plant nitrate transporters: from gene function to application. J Exp Bot 68(10):2463–2475. https://doi.org/10.1093/jxb/erx011
Fatholahi S, Ehsanzadeh P, Karimmojeni H (2020) Ancient and improved wheats are discrepant in nitrogen uptake, remobilization, and use efficiency yet comparable in nitrogen assimilating enzymes capabilities. Field Crops Res 249(4):107761. https://doi.org/10.1016/j.fcr.2020.107761
Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F, Gojon A (2001) An arabidopsis T-DNA mutant affected in NTR2 genes is impaired in nitrate uptake. FEBS Lett 489(2–3):220–224. https://doi.org/10.1016/S0014-5793(01)02096-8
Gao J, Wang F, Hu H, Jiang S, Abid M, Shao Y, Sun C, Tian Z, Jiang D, Dai T (2018a) Improved leaf nitrogen reutilisation and rubisco activation under short-term nitrogen-deficient conditions promotes photosynthesis in winter wheat (Triticum Aestivum L.) at the seedling stage. Funct Plant Biol 45(8):840. https://doi.org/10.1071/FP17232
Gao J, Wang F, Sun J, Tian Z, Hu H, Jiang S, Luo Q (2018b) Enhanced rubisco activation associated with maintenance of electron transport alleviates inhibition of photosynthesis under low nitrogen conditions in winter wheat seedlings. J Exp Bot 69(22):5477–5488. https://doi.org/10.1093/jxb/ery315
Gao J, Luo Q, Sun C, Hu H, Wang F, Tian Z, Jiang D, Cao W, Dai T (2019) Low nitrogen priming enhances photosynthesis adaptation to water-deficit stress in winter wheat (Triticum Aestivum L.) seedlings. Front Plant Sci 10(6):818. https://doi.org/10.3389/fpls.2019.00818
Guan Y, Liu D, Qiu J, Liu Z, He Y, Fang Z, Huang X, Gong J (2022) The nitrate transporter OsNPF79 mediates nitrate allocation and the divergent nitrate use efficiency between Indica and Japonica rice. Plant Physiol 189(1):215–229. https://doi.org/10.1093/plphys/kiac044
Haling R, Yang Z, Shadwell N, Culvenor R, Stefanski A, Ryan M, Sandral G, Kidd D, Lambers H, Simpson R (2016) Root morphological traits that determine phosphorus-acquisition efficiency and critical external phosphorus requirement in pasture species. Funct Plant Biol 43(9):815–826. https://doi.org/10.1071/FP16037
Hermans C, Hammond J, White P, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11(12):610–617. https://doi.org/10.1016/j.tplants.2006.10.007
Hu M, Zhao X, Liu Q, Hong X, Zhang W, Zhang Y, Sun L, Li H, Tong Y (2018) Transgenic expression of plastidic Glutamine Synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol J 16(11):1858–1867. https://doi.org/10.1111/pbi.12921
Islam S, Zhang J, Zhao Y, She M, Ma W (2021) Genetic regulation of the traits contributing to wheat nitrogen use efficiency. Plant Sci 303(2):110759. https://doi.org/10.1016/j.plantsci.2020.110759
Jia Z, Giehl R, Meyer R, Altmann T, Wiren N (2019) Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen. Nat Commun 10(1):2378. https://doi.org/10.1038/s41467-019-10331-9
Jiang S, Sun J, Tian Z, Hu H, Michel E, Cai J, Jiang D, Cao W, Dai T (2017) Root extension and nitrate transporter up-regulation induced by nitrogen deficiency improves nitrogen status and plant growth at the seedling stage of winter wheat (Triticum Aestivum L.). Environ Exp Bot 141(9):28–40. https://doi.org/10.1016/j.envexpbot.2017.06.006
Ju C, Buresh R, Wang Z, Zhang H, Liu L, Yang J, Zhang J (2015) 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(4):47–55. https://doi.org/10.1016/j.fcr.2015.02.007
Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant Cell Physiol 57(4):707–714. https://doi.org/10.1093/pcp/pcw052
Koyama H, Kamiya M, Sasaki Y, Yamakawa R, Kuniyoshi H (2023) Cloning of glutamine synthetase gene from abdominal muscle of kuruma shrimp Marsupenaeus japonicus and its expression profile. Fish Sci 89:215–222. https://doi.org/10.1007/s12562-022-01658-2
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25(6):115–122. https://doi.org/10.1016/j.pbi.2015.05.010
Lehretz G, Sonnewald S, Lugassi N, Granot D, Sonnewald U (2021) Future proofing potato for drought and heat tolerance by overexpression of hexokinase and SP6A. Front Plant Sci 11(1):614534. https://doi.org/10.3389/fpls.2020.614534
Li K, Zhao Y, Yuan X, Zhao H, Wang Z, Li S, Malhi S (2012) Comparison of factors affecting soil nitrate nitrogen and ammonium nitrogen extraction. Commun Soil Sci Plant Anal 43(3):571–588. https://doi.org/10.1080/00103624.2012.639108
Li D, Tian M, Cai J, Jiang D, Cao W, Dai T (2013) Effects of low nitrogen supply on relationships between photosynthesis and nitrogen status at different leaf position in wheat seedlings. Plant Growth Regul 70(3):257–263. https://doi.org/10.1007/s10725-013-9797-4
Li X, Topbjerg H, Jiang D, Liu F (2015) Drought priming at vegetative stage improves the antioxidant capacity and photosynthesis performance of wheat exposed to a short-term low temperature stress at jointing stage. Plant Soil 393(1–2):307–318. https://doi.org/10.1007/s11104-015-2499-0
Liu X, Hu B, Chu C (2022) Nitrogen assimilation in plants: current status and future prospects. J Genet Genomics 49(5):394–404. https://doi.org/10.1016/j.jgg.2021.12.006
Moison M, Marmagne A, Dinant S, Soulay F, Azzopardi M, Lothier J, Citerne S (2018) Three cytosolic Glutamine Synthetase isoforms localized in different-order veins act together for N remobilization and seed filling in arabidopsis. J Exp Bot 69(18):4379–4393. https://doi.org/10.1093/jxb/ery217
Ru C, Hu X, Chen D, Song T, Wang W, Lu M, Hansen N (2022) Nitrogen modulates the effects of short-term heat, drought and combined stresses after anthesis on photosynthesis, nitrogen metabolism, yield, and water and nitrogen use efficiency of wheat. Water 14(9):1407. https://doi.org/10.3390/w14091407
Rupp L, Molitor M, Lucey J (2018) Effect of processing methods and protein content of the concentrate on the properties of milk protein concentrate with 80% protein. J Dairy Sci 101(9):7702–7713. https://doi.org/10.3168/jds.2018-14383
Sandhu K, Mihalyov P, Lewien M, Pumphrey M, Carter A (2021) Combining genomic and phenomic information for predicting grain protein content and grain yield in spring wheat. Front Plant Sci 12(2):613300. https://doi.org/10.3389/fpls.2021.613300
Santos C, Boiteux L (2013) Breeding biofortified cowpea lines for semi-arid tropical areas by combining higher seed protein and mineral levels. Genet Mol Res 12(4):6782–6789. https://doi.org/10.4238/2013.December.16.4
Setién I, Mendizabal T, Gonzalez A (2013) High irradiance improves ammonium tolerance in wheat plants by increasing N assimilation. J Plant Physiol 170(8):758–771. https://doi.org/10.1016/j.jplph.2012.12.015
Shi Z, Li D, Jing Q, Cai J, Jiang D, Cao W, Dai T (2012) Effects of nitrogen applications on soil nitrogen balance and nitrogen utilization of winter wheat in a rice-wheat rotation. Field Crop Res 127(2):241–247. https://doi.org/10.1016/j.fcr.2011.11.025
Shiratake K, Notaguchi M, Makino H, Sawai Y, Borghi L (2019) Petunia pleiotropic drug resistance is a strigolactone short-distance transporter with long-distance outcomes. Plant Cell Physiol 60(8):1722–1733. https://doi.org/10.1093/pcp/pcz081
Siddiqui M, Pandey K, Bhadhury S, Sadeqi B, Schneider M (2023) Convergently selected NPF2.12 coordinates root growth and nitrogen use efficiency in wheat and barley. New Phytol 238(5):2175–2193. https://doi.org/10.1111/nph.18820
Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate and nitrate deficiency induced root development and auxin transport in rice. J Exp Bot 65(22):6735–6746. https://doi.org/10.1093/jxb/eru029
Tian Z, Li Y, Liang Z, Guo H, Cai J, Jiang D, Cao W, Dai T (2016) Genetic improvement of nitrogen uptake and utilization of winter wheat in the Yangtze River Basin of China. Field Crop Res 196(9):251–260. https://doi.org/10.1016/j.fcr.2016.07.007
Tian Z, Liu X, Gu S, Yu J, Zhang L, Zhang W, Jiang D, Cao W, Dai T (2018) Postponed and reduced basal nitrogen application improves nitrogen use efficiency and plant growth of winter wheat. J Integr Agric 17(12):2648–2661. https://doi.org/10.1016/S2095-3119(18)62086-6
Wang Q, Sun D, Hao W, Li Y, Mei X, Zhang Y (2012) Human activities and nitrogen in waters. Acta Ecol Sin 32(4):174–179. https://doi.org/10.1016/j.chnaes.2012.04.010
Wang H, Yang Z, Yu Y, Chen S, He Z, Wang Y, Jiang L (2017) Drought enhances nitrogen uptake and assimilation in maize roots. Agron J 109(1):39–46. https://doi.org/10.2134/agronj2016.01.0030
Wang Y, Cheng Y, Chen K, Tsay Y (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69(1):85–122. https://doi.org/10.1146/annurev-arplant-042817-040056
Wang J, Song K, Sun L, Qin Q, Sun Y, Pan J, Xue Y (2019) Morphological and transcriptome analysis of wheat seedlings response to low nitrogen stress. Plants 8(4):98. https://doi.org/10.3390/plants8040098
Wang J, Chen Q, Wu W, Chen Y, Zhou Y, Guo G, Chen M (2021) Genome-wide analysis of long non-coding RNAs responsive to multiple nutrient stresses in arabidopsis thaliana. Funct Integr Genomics 21(1):17–30. https://doi.org/10.1007/s10142-020-00758-5
Wang X, Ge J, He M, Li Q, Cai J, Zhou Q, Zhong Y, Wollenweber B, Jiang D (2023) Enhancing crop resilience: Understanding the role of drought priming in wheat stress response. Field Crops Res 302:109083. https://doi.org/10.1016/j.fcr.2023.109083
Zhang H, Jiao B, Dong F, Liang X, Zhou S, Wang H (2022) Genome-wide identification of CCT genes in wheat (Triticum aestivum L.) and their expression analysis during vernalization. PLOS ONE 17(1):e0262147. https://doi.org/10.1371/journal.pone.0262147
Zorzan M, Collazuol D, Ribaudo G, Ongaro A, Scaroni C (2019) Biological effects and potential mechanisms of action of pistacia lentiscus chios mastic extract in Caco-2 cell model. J Funct Foods 54(3):92–97. https://doi.org/10.1016/j.jff.2019.01.0
Acknowledgements
This study was financially supported from the National Natural Science Foundation of China (Grant No. 32272215), the National Key R&D Program of Jiangsu (BE2021361-1), and Collaborative Innovation Center for Modern Crop Production by Province and Ministry (CIC-MCP), Nanjing Agricultural University.
Author information
Authors and Affiliations
Contributions
LG, TD, and ZT conceived and designed the experiments. YL and LG experimented and wrote the manuscript. JH, XL, and DJ revised the manuscript. ZT and TD supervised the project and revised the manuscript. All the authors contributed to the article and approved the submitted version.
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Stefan de Folter.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lu, Y., Gao, L., Hu, J. et al. Low nitrogen priming improves nitrogen uptake and assimilation adaptation to nitrogen deficit stress in wheat seedling. Planta 259, 107 (2024). https://doi.org/10.1007/s00425-024-04385-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04385-3