Abstract
The genetic architecture of nitrogen use efficiency (NUE) and its two component traits i.e. NUpE (N uptake efficiency) and NUtE (N utilization efficiency) was studied using a bi-parental RIL mapping population derived from a cross HUW468 (high NUE)/C306 (low NUE). The mapping population, two parental genotypes and three check genotypes were evaluated under four different N levels (0, 60, 120, and 180 kg/ha) over three years. A genetic map containing 456 SNP markers (2571.38 cM length) was used for QTL analysis. Thirty six main effect QTLs (17 QTLs for NUE, 13 NUpE and 6 QTLs for NUtE) distributed on 12 chromosomes (1B, 1D, 2A, 2B, 3A, 4B, 5A, 5B, 5D, 6A, 6D, and 7A) were identified at 2.52–9.27 LOD scores. Individual QTLs explained 6.65–22.89% phenotypic variation. Multi-traits QTLs (Mt-QTLs) and epistatic QTLs involving first-order epistatic (QTL × QTL) interactions were also discovered. Candidate genes (CGs, as many as 737) were mined from QTL regions which were mainly involved in metabolic process, cellular process and catalytic activity, etc.; differential expression was observed for 49 CGs in roots and 34 in shoots. The CGs encoded important transcription factors, transporters, etc. having a role in NUE. QTLs and CGs reported in this study enriched the available knowledge. Seven QTLs (including three Mt-QTLs) and QTLs involved in six epistatic interactions are recommended for MAS for improvement of NUE in wheat.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
An D, Su J, Liu Q et al (2006) Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant Soil 284:73–84. https://doi.org/10.1007/s11104-006-0030-3
Balyan HS, Gahlaut V, Kumar A et al (2016) Nitrogen and phosphorus use efficiencies in wheat: physiology, phenotyping, genetics and breeding. Plant Breed 40:169–216. https://doi.org/10.1002/9781119279723.ch4
Barraclough PB, Howarth JR, Jones J et al (2010) Nitrogen efficiency of wheat: genotypic and environmental variation and prospects for improvement. Eur J Agron 33:1–11. https://doi.org/10.1016/j.eja.2010.01.005
Basten CJ, Weir BS, Zeng ZB (2002) QTL Cartographer, version 1.17. Department of Statistics, North Carolina State University, Raleigh, NC
Brasier K, Ward B, Smith J et al (2020) Identification of quantitative trait loci associated with nitrogen use efficiency in winter wheat. PLoS ONE 15:e0228775
Cai H, Lu Y, Xie W et al (2012) Transcriptome response to nitrogen starvation in rice. J Biosci 37(4):731–747. https://doi.org/10.1007/s12038-012-9242-2
Chen L, Storey JD (2006) Relaxed significance criteria for linkage analysis. Genetics 173:2371–2381. https://doi.org/10.1534/genetics.105.052506
Churchill GA, Doerge R (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971. https://doi.org/10.1093/genetics/138.3.963
Cormier F, Le-Gouis J, Dubreuil P et al (2014) A genome-wide identification of chromosomal regions determining nitrogen use efficiency components in wheat (Triticum aestivum L.). Theor Appl Genet 127:2679–2693. https://doi.org/10.1007/s00122-014-2407-7
Doerge RW, Churchill G (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294. https://doi.org/10.1093/genetics/142.1.285
Effah Z, Li L, Xie J et al (2022) Transcriptome profiling reveals major structural genes, transcription factors and biosynthetic pathways involved in leaf senescence and nitrogen remobilization in rainfed spring wheat under different nitrogen fertilization rates. Genomics 114:110271. https://doi.org/10.1016/j.ygeno.2022.110271
Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10(12):1135–1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x
Fan X, Zhang W, Zhang N et al (2018) Identification of QTL regions for seedling root traits and their effect on nitrogen use efficiency in wheat (Triticum aestivum L.). Theor Appl Genet 131:2677–2698. https://doi.org/10.1007/s00122-018-3183-6
Fan X, Cui F, Ji J et al (2019) Dissection of pleiotropic QTL regions controlling wheat spike characteristics under different nitrogen treatments using traditional and conditional QTL mapping. Front Plant Sci 10:187. https://doi.org/10.3389/fpls.2019.00187
Fradgley NS, Bentley AR, Swarbreck SM et al (2021) Defining the physiological determinants of low nitrogen requirement in wheat. Biochem Soc Trans 49:609–616. https://doi.org/10.1042/BST20200282
Guo Y, Kong FM, Xu YF et al (2012) QTL mapping for seedling traits in wheat grown under varying concentrations of N, P and K nutrients. Theor Appl Genet 124:851–865. https://doi.org/10.1007/s00122-011-1749-7
Habash DZ, Bernard S, Schondelmaier J, Weyen J, Quarrie SA (2007) The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theor Appl Genet 114:403–419. https://doi.org/10.1007/s00122-006-0429-5
Haile D, Nigussie D, Ayana A (2012) Nitrogen use efficiency of bread wheat: effects of nitrogen rate and time of application. J Soil Sci Plant Nutri 12:389–410. https://doi.org/10.4067/S0718-95162012005000002
Hawkesford MJ (2017) Genetic variation in traits for nitrogen use efficiency in wheat. J Exp Bot 68(10):2627–2632. https://doi.org/10.1093/jxb/erx079
He X, Qu B, Li W et al (2015) The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169:1991–2005. https://doi.org/10.1104/pp.15.00568
Hitz K, Clark AJ, Van Sanford DA (2017) Identifying nitrogen-use efficient soft red winter wheat lines in high and low nitrogen environments. Field Crop Res 200:1–9. https://doi.org/10.1016/j.fcr.2016.10.001
Hsieh PH, Kan CC, Wu HY et al (2018) Early molecular events associated with nitrogen deficiency in rice seedling roots. Sci Rep 8(1):1–23. https://doi.org/10.1038/s41598-018-30632-1
Hudson D, Guevara D, Yaish MW et al (2011) GNC and CGA1 modulate chlorophyll biosynthesis and glutamate synthase (GLU1/Fd-GOGAT) expression in Arabidopsis. PLoS ONE 6:26765. https://doi.org/10.1371/journal.pone.0026765
Jagadhesan B, Sathee L, Meena HS et al (2020) Genome wide analysis of NLP transcription factors reveals their role in nitrogen stress tolerance of rice. Sci Rep 10(1):1–16. https://doi.org/10.1038/s41598-020-66338-6
Javed T, Singhal RK, Shabbir R et al (2022) Recent advances in agronomic and physio-molecular approaches for improving nitrogen use efficiency in crop plants. Front Plant Sci 13:877544. https://doi.org/10.3389/fpls.2022.877544
Kaler AS, Purcell LC (2019) Estimation of a significance threshold for genome-wide association studies. BMC Genom 20:1–8
Kang J, Park J, Choi H et al (2011) Plant ABC Transporters. Arabidopsis Book 9:e0153. https://doi.org/10.1199/tab.0153
Klemens PA, Patzke K, Deitmer J (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163:1338–1352
Kumar A, Batra R, Gahlaut V et al (2018a) Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.). PLoS ONE 13(12):e0208409. https://doi.org/10.1371/journal.pone.0208409
Kumar A, Pandeya A, Malik G et al (2018b) A web resource for nutrient use efficiency-related genes, quantitative trait loci and microRNAs in important cereals and model plants. F1000Research. https://doi.org/10.12688/f1000research.14561.1
Lander ES, Botstein D (1989) Mapping mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199
Laperche A, Brancourt-Hulmel M, Heumez E et al (2006) Estimation of genetic parameters of a DH wheat population grown at different N stress levels characterized by probe genotypes. Thoer Appl Genet 112(5):797–807. https://doi.org/10.1007/s00122-005-0176-z
Le Gouis J, Beghin D, Heumez E, Pluchard P (2000) Genetic differences for nitrogen uptake and nitrogen utilisation efficiencies in winter wheat. Eur J Agron 12:163–173. https://doi.org/10.1016/S1161-0301(00)00045-9
Li ZK, Jiang XL, Peng T et al (2014) Mapping quantitative trait loci with additive effects and additive × additive epistatic interactions for biomass yield, grain yield, and straw yield using a doubled haploid population of wheat (Triticum aestivum L.). Genet Mol Res 13:1412–1424. https://doi.org/10.4238/2014.February.28.14
Li S, Tian Y, Wu K et al (2018) Modulating plant growth–metabolism coordination for sustainable agriculture. Nature 560:595–600
Liu KH, Tsay YF (2003) Switching between the two action modes of dual affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–1013. https://doi.org/10.1093/emboj/cdg118
Liu X, Hu B, Chu C (2022) Nitrogen assimilation in plants: current status and future prospects. J Genet Genom 49:394–404. https://doi.org/10.1016/j.jgg.2021.12.006
Mălinaş A, Vidican R, Rotar I et al (2022) Current status and future prospective for nitrogen use efficiency in wheat (Triticum aestivum L.). Plants 11:217. https://doi.org/10.3390/plants11020217
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564. https://doi.org/10.2134/agronj1982.00021962007400030037x
Monostori I, Szira F, Tondelli A et al (2017) Genome-wide association study and genetic diversity analysis on nitrogen use efficiency in a Central European winter wheat (Triticum aestivum L.) collection. PLoS ONE 12:e0189265. https://doi.org/10.1371/journal.pone.0189265
Ortiz-Monasterio I, Sayre KD, Rajaram S, McMahon MA (1997) Genetic progress in wheat yield and nitrogen use efficiency under four nitrogen rates. Crop Sci 37:898–904. https://doi.org/10.2135/cropsci1997.0011183X003700030033x
Perneger TV (1998) What's wrong with Bonferroni adjustments. BMJ 316:1236–1238
Quraishi UM, Abrouk M, Murat F et al (2011) Cross-genome map based dissection of a nitrogen use efficiency ortho-meta QTL in bread wheat unravels concerted cereal genome evolution. Plant J 65:745–756. https://doi.org/10.1111/j.1365-313X.2010.04461.x
Raffo MA, Sarup P, Guo X et al (2022) Improvement of genomic prediction in advanced wheat breeding lines by including additive-by-additive epistasis. Theor Appl Genet 135:965–978
Raigar OP, Mondal K, Sethi M et al (2022) Nitrogen use efficiency in wheat: genome to field. In Ansari MP (ed) Wheat-recent advances, pp 89–120. IntechOpen. https://doi.org/10.5772/intechopen.103126
Ranjan R, Yadav R, Pandey R et al (2019) Variation in wheat (Triticum aestivum) advance lines and released cultivars for traits associated with nitrogen use efficiency under N limiting environment. Indian J Agric Sci 89:99–104
Ranjan R, Yadav R, Jain N et al (2021) Epistatic QTLs play a major role in nitrogen use efficiency and its component traits in indian spring wheat. Agriculture 11:1149. https://doi.org/10.3390/agriculture11111149
Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91:357–363. https://doi.org/10.2134/agronj2002.8150
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS ONE 8:e66428. https://doi.org/10.1371/journal.pone.0066428
Razaq M, Zhang P, Shen HL (2017) Influence of nitrogen and phosphorous on the growth and root morphology of Acer mono. PLoS ONE 12:e0171321. https://doi.org/10.1371/journal.pone.0171321
Ren Y, Qian Y, Xu Y et al (2017) Characterization of QTLs for root traits of wheat grown under different nitrogen and phosphorus supply levels. Front Plant Sci 8:2096. https://doi.org/10.3389/fpls.2017.02096
Ren D, Fang X, Jiang P et al (2018) Genetic architecture of nitrogen-deficiency tolerance in wheat seedlings based on a nested association mapping (NAM) population. Front Plant Sci 9:845. https://doi.org/10.3389/fpls.2018.00845
Rubin G, Tohge T, Matsuda F et al (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21(11):3567–3584. https://doi.org/10.1105/tpc.109.067041
Saini DK, Chopra Y, Pal N et al (2021) Meta-QTLs, ortho-MQTLs and candidate genes for nitrogen use efficiency and root system architecture in bread wheat (Triticum aestivum L.). Physiol Mol Biol Plants 27:2245–2267. https://doi.org/10.1007/s12298-021-01085-0
Sharma N, Schneider-Canny R, Chekhovskiy K et al (2020) Opportunities for increased nitrogen use efficiency in wheat for forage use. Plants 9(12):1738. https://doi.org/10.3390/plants9121738
Singh K, Batra R, Sharma S et al (2021) WheatQTLdb: a QTL database for wheat. Mol Genet Genom 296:1051–1056. https://doi.org/10.1007/s00438-021-01812-y
Singh K, Saini DK, Saripalli GK et al (2022) WheatQTLdb V2. 0: a supplement to the database for wheat QTL. Mol Breed 42:56
Tedone L, Ali SA, Verdini L, De Mastro G (2018) Nitrogen management strategy for optimizing agronomic and environmental performance of rainfed durum wheat under Mediterranean climate. J Clean Prod 172:2058–2074. https://doi.org/10.1016/j.jclepro.2017.11.215
Tian Z, Li Y, Liang Z et al (2016) Genetic improvement of nitrogen uptake and utilization of winter wheat in the Yangtze River Basin of China. Field Crops Res 196:251–260. https://doi.org/10.1016/j.fcr.2016.07.007
Tian X, Yin Y, Zhuang M et al (2022) Bottom-up estimates of reactive nitrogen loss from Chinese wheat production in 2014. Sci Data 9:1–8. https://doi.org/10.1038/s41597-022-01315-4
Van Ooijen JW (1999) LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83:613–624. https://doi.org/10.1038/sj.hdy.6886230
Wang F, Yoshida H, Matsuoka M (2021) Making the ‘Green Revolution’truly green: improving crop nitrogen use efficiency. Plant Cell Physiol 62(6):942–947. https://doi.org/10.1093/pcp/pcab051
White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105:1073–1080. https://doi.org/10.1093/aob/mcq085
Xiong H, Guo H, Zhou C et al (2019) A combined association mapping and t-test analysis of SNP loci and candidate genes involving in resistance to low nitrogen traits by a wheat mutant population. PLoS ONE 14:e0211492. https://doi.org/10.1371/journal.pone.0211492
Xu Y, Wang R, Tong Y et al (2014) Mapping QTLs for yield and nitrogen-related traits in wheat: influence of nitrogen and phosphorus fertilization on QTL expression. Theor Appl Genet 127:59–72. https://doi.org/10.1007/s00122-013-2201-y
Yadav MR, Kumar R, Parihar CM et al (2017) Strategies for improving nitrogen use efficiency: a review. Agric Rev 38:29–40. https://doi.org/10.18805/ag.v0iOF.7306
Yang XL, Lu YL, Ding Y et al (2017) Optimising nitrogen fertilisation: a key to improving nitrogen-use efficiency and minimising nitrate leaching losses in an intensive wheat/maize rotation (2008–2014). Field Crop Res 206:1–10. https://doi.org/10.1016/j.fcr.2017.02.016
Yu L, Wu J, Tang H et al (2016) Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Sci Rep 6:27795. https://doi.org/10.1038/srep27795
Zhang M, Gao M, Zheng H et al (2019) QTL mapping for nitrogen use efficiency and agronomic traits at the seedling and maturity stages in wheat. Mol Breed 39:71. https://doi.org/10.1007/s11032-019-0965-8
Zhao D, Derkx AP, Liu DC et al (2015) Overexpression of a NAC transcription factor delays leaf senescence and increases grain nitrogen concentration in wheat. Plant Biol 17(4):904–913. https://doi.org/10.1111/plb.12296
Zhu X, Wang D, Xie L et al (2022) Rice transcription factors OsLBD37/38/39 regulate nitrate uptake by repressing OsNRT2. 1/2.2/2.3 under high-nitrogen conditions. Crop J. https://doi.org/10.1016/j.cj.2022.03.011
Zuluaga DL, Sonnante G (2019) The use of nitrogen and its regulation in cereals: structural genes, transcription factors, and the role of miRNAs. Plants 8:294. https://doi.org/10.3390/plants8080294
Acknowledgements
Thanks are due to ICAR-Indian Institute of Farming Systems Research (IIFSR), Meerut (Uttar Pradesh) for providing facilities to conduct the field experiments. We are also thankful to Dr. AK Joshi and Dr. VK Mishra for providing the seed material and SNP data of the mapping population. Thanks are also due to Indian National Science Academy (INSA), New Delhi for the award of positions of INSA-Senior Scientist and INSA Honorary Scientist to HSB.
Funding
The authors declare that no funds, grants, or other support were received for this experiment.
Author information
Authors and Affiliations
Contributions
HSB, PKG, PKS, and VKS conceived and designed the experiment. RS prepared first draft of the MS. GS, SK, AK and TG helped in conducting the experiments. SK and VG helped in data analysis.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no competing interests..
Ethical approval
The authors declare that the experiments comply with the current laws of the country in which they were performed.
Additional information
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.
10681_2022_3134_MOESM1_ESM.tif
Violin plots showing distribution of NUE, NUpE, and NUtE for individual years data of RIL population grown over three years under three N levels (N60, N120, N180). The values of the two parental genotypes of the RIL populations are indicated by red (HUW468) and black (C306) dots (TIF 998 kb)
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
Singh, R., Saripalli, G., Kumar, A. et al. QTL analysis for nitrogen use efficiency in wheat (Triticum aestivum L.). Euphytica 219, 9 (2023). https://doi.org/10.1007/s10681-022-03134-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-022-03134-5