Abstract
Main conclusion
The genetic diversity in tetraploid wheat provides a genetic pool for improving wheat productivity and environmental resilience. The tetraploid wheat had strong N uptake, translocation, and assimilation capacity under N deficit stress, thus alleviating growth inhibition and plant N loss to maintain healthy development and adapt to environments with low N inputs.
Abstract
Tetraploid wheat with a rich genetic variability provides an indispensable genetic pool for improving wheat yield. Mining the physiological mechanisms of tetraploid wheat in response to nitrogen (N) deficit stress is important for low-N-tolerant wheat breeding. In this study, we selected emmer wheat (Kronos, tetraploid), Yangmai 25 (YM25, hexaploid), and Chinese spring (CS, hexaploid) as materials. We investigated the differences in the response of root morphology, leaf and root N accumulation, N uptake, translocation, and assimilation-related enzymes and gene expression in wheat seedlings of different ploidy under N deficit stress through hydroponic experiments. The tetraploid wheat (Kronos) had stronger adaptability to N deficit stress than the hexaploid wheats (YM25, CS). Kronos had better root growth under low N stress, expanding the N uptake area and enhancing N uptake to maintain higher NO3− and soluble protein contents. Kronos exhibited high TaNRT1.1, TaNRT2.1, and TaNRT2.2 expression in roots, which promoted NO3− uptake, and high TaNRT1.5 and TaNRT1.8 expression in roots and leaves enhanced NO3− translocation to the aboveground. NR and GS activity in roots and leaves of Kronos was higher by increasing the expression of TANIA2, TAGS1, and TAGS2, which enhanced the reduction and assimilation of NO3− as well as the re-assimilation of photorespiratory-released NH4+. Overall, Kronos had strong N uptake, translocation, and assimilation capacity under N deficit stress, alleviating growth inhibition and plant N loss and thus maintaining a healthy development. This study reveals the physiological mechanisms of tetraploid wheat that improve nitrogen uptake and assimilation adaptation under low N stress, which will provide indispensable germplasm resources for elite low-N-tolerant wheat improvement and breeding.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be made available on request.
Abbreviations
- CS:
-
Wheat cv Chinese spring
- DAT:
-
Days after treatment
- GS:
-
Glutamine synthetase
- LN:
-
Low nitrogen
- NR:
-
Nitrate reductase
- NRT:
-
Nitrate transporter
- NUE:
-
N use efficiency
- YM25:
-
Wheat cv Yangmai 25
References
Abdehpour Z, Ehsanzadeh P (2019) Concurrence of ionic homeostasis alteration and dry mass sustainment in emmer wheats exposed to saline water: implications for tackling irrigation water salinity. Plant Soil 440:427–441. https://doi.org/10.1007/s11104-019-04090-1
Ahmad I, Batyrbek M, Ikram K, Ahmad S, Kamran M, Khan RS, Hou FJ, Han QF (2023) Nitrogen management improves lodging resistance and production in maize (Zea mays L.) at a high plant density. J Integr Agric 22(2):417–433. https://doi.org/10.1016/j.jia.2022.08.074
Alt DS, Doyle JW, Malladi A (2017) Nitrogen-source preference in blueberry (Vaccinium sp.): enhanced shoot nitrogen assimilation in response to direct supply of nitrate. J Plant Physiol 216:79–87. https://doi.org/10.1016/j.jplph.2017.05.014
Ayadi M, Brini F, Masmoudi K (2019) Overexpression of a wheat aquaporin gene, TdPIP2;1, enhances salt and drought tolerance in transgenic durum wheat cv. Maali. Int J Mol 20(10):2389. https://doi.org/10.3390/ijms20102389
Baki GAE, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM (2000) Nitrate reductase in Zea mays L. under salinity. Plant Cell Environ 23(5):515–521. https://doi.org/10.1046/j.1365-3040.2000.00568.x
Balotf S, Kavoosi G, Kholdebarin B (2016) Nitrate reductase, nitrite reductase, glutamine synthetase, and glutamate synthase expression and activity in response to different nitrogen sources in nitrogen-starved wheat seedlings. Biotechnol Appl Biochem 63(2):220–229. https://doi.org/10.1002/bab.1362
Bernard SM, Møller ALB, Dionisio G, Kichey T, Jahn TP, Dubois F, Baudo M, Lopes MS, Tercé-Laforgue T, Foyer CH, Parry MAJ, Forde BG, Araus JL, Hirel B, Schjoerring KJ, Habash DZ (2008) Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol Biol 67:89–105. https://doi.org/10.1007/s11103-008-9303-y
Bouchet AS, Laperche A, Bissuel-Belaygue C, Snowdon R, Nesi N, Stahl A (2016) Nitrogen use efficiency in rapeseed. A review. Agron Sustain Dev 36:1–20. https://doi.org/10.1007/s13593-016-0371-0
Chen CZ, Lv XF, Li JY, Yi HY, Gong JM (2012) Arabidopsis NRT1.5 is another essential component in the regulation of nitrate reallocation and stress tolerance. Plant Physiol 159(4):1582–1590. https://doi.org/10.1104/pp.112.199257
Curci PL, Aiese Cigliano R, Zuluaga DL, Janni M, Sanseverino W, Sonnante G (2017) Transcriptomic response of durum wheat to nitrogen starvation. Sci Rep 7(1):1176. https://doi.org/10.1038/s41598-017-01377-0
De Pessemier J, Moturu TR, Nacry P, Ebert R, De Gernier H, Tillard P, Swarup K, Wells D, Haseloff J, Murray S, Bennett M, Inzé D, Vincent C, Hermans C (2022) Root system size and root hair length are key phenes for nitrate acquisition and biomass production across natural variation in Arabidopsis. J Exp Bot 73(11):3569–3583. https://doi.org/10.1093/jxb/erac118
Dechorgnat J, Francis KL, Dhugga KS, Rafalski JA, Tyerman SD, Kaiser BN (2019) Tissue and nitrogen-linked expression profiles of ammonium and nitrate transporters in maize. BMC Plant Biol 19:1–13. https://doi.org/10.1186/s12870-019-1768-0
Fan X, Naz M, Fan X, Xuan W, Miller AJ, 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 Crop Res 249:107761. https://doi.org/10.1016/j.fcr.2020.107761
Feng H, Fan X, Miller AJ, Xu G (2020) Plant nitrogen uptake and assimilation: regulation of cellular pH homeostasis. J Exp Bot 71(15):4380–4392. https://doi.org/10.1093/jxb/eraa150
Feuillet C, Langridge P, Waugh R (2008) Cereal breeding takes a walk on the wild side. Trends Genet 24(1):24–32. https://doi.org/10.1016/j.tig.2007.11.001
Gao J, Wang F, Hu H, Jiang S, Muhammad A, Shao Y, Sun C, Tian Z, Jiang D, Dai T (2018) 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):840–853. https://doi.org/10.1071/fp17232
Gao J, Luo Q, Sun C, Hu H, Wang F, Tian Z, Jiang D, Cao W, Dai T (2019a) Low nitrogen priming enhances photosynthesis adaptation to water-deficit stress in winter wheat (Triticum aestivum L.) seedlings. Front Plant Sci 10:818. https://doi.org/10.3389/fpls.2019.00818
Gao Y, Bang TC, Schjoerring JK (2019b) Cisgenic overexpression of cytosolic glutamine synthetase improves nitrogen utilization efficiency in barley and prevents grain protein decline under elevated CO2. Plant Biotechnol J 17(7):1209–1221. https://doi.org/10.1111/pbi.13046
Gao S, Wang S, Hu Y, Chen S, Guo J, Shi L (2022) Comparative differences in photosynthetic characteristics, ion balance, and nitrogen metabolism between young and old wild soybean leaves under nitrogen deficiency. Plant Stress 4:100064. https://doi.org/10.1186/s12870-019-2005-6
Goncharov NP (2011) Genus Triticum L. taxonomy: the present and the future. Plant Syst Evol 295:1–11. https://doi.org/10.1007/s00606-011-0480-9
Guan Y, Liu DF, Qiu J, Liu ZJ, He YN, Fang ZJ, Huang XH, Gong JM (2022) The nitrate transporter OsNPF7.9 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
Hawkesford MJ, Griffiths S (2019) Exploiting genetic variation in nitrogen use efficiency for cereal crop improvement. Curr Opin Plant Biol 49:35–42. https://doi.org/10.1016/j.pbi.2019.05.003
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 303:110759. https://doi.org/10.1016/j.plantsci.2020.110759
Jedelská T, Luhová L, Petřivalský M (2021) Nitric oxide signalling in plant interactions with pathogenic fungi and oomycetes. J Exp Bot 72(3):848–863. https://doi.org/10.1093/jxb/eraa596
Jia Z, Giehl RF, Meyer RC, Altmann T, Von Wirén 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 EJ, Gao 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 141:28–40. https://doi.org/10.1016/j.envexpbot.2017.06.006
Kant S (2018) Understanding nitrate uptake, signaling and remobilisation for improving plant nitrogen use efficiency. Semin Cell Dev Biol 74:89–96. https://doi.org/10.1016/j.semcdb.2017.08.034
Kocheva K, Kartseva T, Nenova V, Georgiev G, Brestič M, Misheva S (2020) Nitrogen assimilation and photosynthetic capacity of wheat genotypes under optimal and deficient nitrogen supply. Physiol Mol Biol Plants 26:2139–2149. https://doi.org/10.1007/s12298-020-00901-3
Kumar A, Jayaswal PK, Mahato AK, Arya A, Mandal PK, Singh NK, Sinha SK (2023) Growth stage and nitrate limiting response of NRT2 and NAR2 gene families of bread wheat, and complementation and retrieval of nitrate uptake of atnrt2.1 mutant by a wheat NRT2 gene. Environ Exp Bot 207:105205. https://doi.org/10.1016/j.envexpbot.2022.105205
Langridge P, Paltridge N, Fincher G (2006) Functional genomics of abiotic stress tolerance in cereals. Brief Funct Genom 4(4):343–354. https://doi.org/10.1093/bfgp/eli005
Li KY, Zhao YY, Yuan XL, Zhao HB, Wang ZH, Li SX, Malhi SS (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 70:257–263. https://doi.org/10.1007/s10725-013-9797-4
Li K, Zhang S, Tang S, Zhang J, Dong H, Yang S, Qu H, Xuan W, Gu M, Xu G (2022a) The rice transcription factor Nhd1 regulates root growth and nitrogen uptake by activating nitrogen transporters. Plant Physiol 189(3):1608–1624. https://doi.org/10.1093/plphys/kiac178
Li M, Wang T, Zhang H, Liu S, Li W, Abou Elwafa SF, Tian H (2022b) Tanrt2.1-6b is a dual-affinity nitrate transporter contributing to nitrogen uptake in bread wheat under both nitrogen deficiency and sufficiency. Crop J 10(4):993–1005. https://doi.org/10.1016/j.cj.2021.11.012
Liu Y, Li M, Xu J, Liu X, Wang S, Shi L (2019) Physiological and metabolomics analyses of young and old leaves from wild and cultivated soybean seedlings under low-nitrogen conditions. BMC Plant Biol 19:389. https://doi.org/10.1186/s12870-019-2005-6
Liu X, Hu B, Chu C (2022) Nitrogen assimilation in plants: current status and future prospects. J Genet Genom 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, Morin H, Legay N, Chardon F, Avice J, Reisdorf-Cren M, Masclaux-Daubresse C (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
Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass AD (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol 140(3):1036–1046. https://doi.org/10.1104/pp.105.074385
Ostmeyer TJ, Bahuguna RN, Kirkham MB, Bean S, Jagadish SV (2022) Enhancing sorghum yield through efficient use of nitrogen—challenges and opportunities. Front Plant Sci 13:845443. https://doi.org/10.3389/fpls.2022.845443
Peng WT, Qi WL, Nie MM, Xiao YB, Liao H, Chen ZC (2020) Magnesium supports nitrogen uptake through regulating NRT2.1/2.2 in soybean. Plant Soil 457:97–111. https://doi.org/10.1007/s11104-019-04157-z
Plett DC, Holtham LR, Okamoto M, Garnett TP (2018) Nitrate uptake and its regulation in relation to improving nitrogen use efficiency in cereals. Semin Cell Dev Biol 74:97–104. https://doi.org/10.1016/j.semcdb.2017.08.027
Ren K, Xu M, Li R, Zheng L, Wang H, Liu S, Zhang W, Duan Y, Lu C (2023) Achieving high yield and nitrogen agronomic efficiency by coupling wheat varieties with soil fertility. Sci Total Environ 881:163531. https://doi.org/10.1016/j.scitotenv.2023.163531
Reynolds M, Dreccer F, Trethowan R (2007) Drought-adaptive traits derived from wheat wild relatives and landraces. J Exp Bot 58(2):177–186. https://doi.org/10.1093/jxb/erl250
Rupp LS, Molitor MS, Lucey JA (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
Santos CAF, Boiteux LS (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, Fuertes-Mendizabal T, González A, Aparicio-Tejo PM, González-Murua C, González-Moro MB, Estavillo JM (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
Shiratake K, Notaguchi M, Makino H, Sawai Y, Borghi L (2019) Petunia PLEIOTROPIC DRUG RESISTANCE 1 is a strigolactone short-distance transporter with long-distance outcomes. Plant Cell Physiol 60(8):1722–1733. https://doi.org/10.1093/pcp/pcz081
Sun J, Zheng N (2015) Molecular mechanism underlying the plant NRT1.1 dual-affinity nitrate transporter. Front Physiol 6:386. https://doi.org/10.3389/fphys.2015.00386
Sun Y, Zhang S, Chen W (2020) Root traits of dryland winter wheat (Triticum aestivum L.) from the 1940s to the 2010s in Shaanxi Province, China. Sci Rep 10(1):5328. https://doi.org/10.1038/s41598-020-62170-0
Tavares OCH, Santos LA, Ferreira LM, Sperandio MVL, Da Rocha JG, García AC, Dobbss LB, Berbara RLL, Souza SR, Fernandes MS (2017) Humic acid differentially improves nitrate kinetics under low-and high-affinity systems and alters the expression of plasma membrane H+-ATPases and nitrate transporters in rice. Ann Appl Biol 170(1):89–103. https://doi.org/10.1111/aab.12317
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 196:251–260. https://doi.org/10.1016/j.fcr.2016.07.007
Tian Z, Chai H, Guo H, Lu Y, Yang S, Liu X, Jiang D, Dai T (2024) Genetic improvement of photosynthetic nitrogen use efficiency of winter wheat in the Yangtze River Basin of China. Field Crop Res 305:10919. https://doi.org/10.1016/j.fcr.2023.109199
Wang H, Yang Z, Yu Y, Chen S, He Z, Wang Y, Jiang L, Wang G, Yang C, Liu B, Zhang Z (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 J, Li Y, Zhu F, Ming R, Chen LQ (2019) Genome-wide analysis of nitrate transporter (NRT/NPF) family in sugarcane Saccharum spontaneum L. Trop Plant Biol 12:133–149. https://doi.org/10.1007/s12042-019-09220-8
Wang W, Hu B, Li A, Chu C (2020) NRT1.1s in plants: functions beyond nitrate transport. J Exp Bot 71(15):4373–4379. https://doi.org/10.1093/jxb/erz554
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 Genomic 21:17–30. https://doi.org/10.1007/s10142-020-00758-5
Warburton ML, Crossa J, Franco J, Kazi M, Trethowan R, Rajaram S, Pfeiffer W, Zhang P, Dreisigacker S, Ginkel MV (2006) Bringing wild relatives back into the family: recovering genetic diversity in CIMMYT improved wheat germplasm. Euphytica 149:289–301. https://doi.org/10.1007/s10681-005-9077-0
Wen B, Xiao W, Mu Q, Li D, Chen X, Wu H, Li L, Peng F (2020) How does nitrate regulate plant senescence? Plant Physiol Biochem 157:60–69. https://doi.org/10.1016/j.plaphy.2020.08.041
Zaharieva M, Ayana NG, Hakimi AA, Misra SC, Monneveux P (2010) Cultivated emmer wheat (Triticum dicoccon Schrank), an old crop with promising future: a review. Genet Resour Crop Evol 57:937–962. https://doi.org/10.1007/s10722-010-9572-6
Zhang Z, Xiong S, Wei Y, Meng X, Wang X, Ma X (2017) The role of glutamine synthetase isozymes in enhancing nitrogen use efficiency of N-efficient winter wheat. Sci Rep 7(1):1000. https://doi.org/10.1038/s41598-017-01071-1
Zhang J, Liu YX, Zhang N, Hu B, Jin T, Xu H, Qin Y, Yan P, Zhang X, Guo X, Hui J, Cao S, Wang X, Wang C, Wang H, Qu B, Fan J, Yuan L, Garrido-Oter R, Chu C, Bai Y (2019) NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37(6):676–684. https://doi.org/10.1038/s41587-019-0104-4
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
Zhao SS, Lin XP, Dong Y, Niu Y, Xu D, Sun H (2018) High-temperature tensile properties and deformation mechanism of polycrystalline magnesium alloys with specifically oriented columnar grain structures. Mater Sci Eng R Rep 729:300–309. https://doi.org/10.1016/j.msea.2018.05.061
Zorzan M, Collazuol D, Ribaudo G, Ongaro A, Scaroni C, Zagotto G, Armanini D, Barollo S, Galeotti F, Volpi N, Redaelli M, Pezzani R (2019) Biological effects and potential mechanisms of action of Pistacia lentiscus Chios mastic extract in Caco-2 cell model. J Funct Foods 54:92–97. https://doi.org/10.1016/j.jff.2019.01.007
Funding
This study was financially supported by the National Natural Science Foundation of China (Grant no. 32272215), the National Key R&D Program of Jiangsu (BE2021361-1), and Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP), Nanjing Agricultural University.
Author information
Authors and Affiliations
Contributions
Siqi Zhang, Tingbo Dai, and Zhongwei Tian designed the research and were responsible for the project initiation. Siqi Zhang, Libing Xu, Qiaomei Zheng, and Jinling Hu performed the experiments. Data analysis was led by Siqi Zhang, Libing Xu, Qiaomei Zheng, and Jinling Hu. The manuscript was organized, written, and revised by Siqi Zhang, Libing Xu, Qiaomei Zheng, Tingbo Dai, Zhongwei Tian, and Dong Jiang.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
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
Zhang, S., Xu, L., Zheng, Q. et al. The tetraploid wheat (Triticum dicoccum (Schrank) Schuebl.) improves nitrogen uptake and assimilation adaptation to nitrogen-deficit stress. Planta 259, 151 (2024). https://doi.org/10.1007/s00425-024-04432-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04432-z