Abstract
Improving the nitrogen use efficiency (NUE) may considerably increase maize yield and decrease the use of nitrogen (N) fertilizer. But the genetic basis of NUE in maize is still poorly understood. In this study, an association panel of 139 maize inbred lines genotyped with 50,790 single nucleotide polymorphism (SNP) was used to dissect the genetic basis of NUE-related traits by genome-wide association study (GWAS). NUE, N uptake efficiency (NupE), N utilization efficiency (NutE), grain N concentration (GNC), stover N concentration (SNC) and N harvest index (NHI) were estimated under two N levels. GWAS was performed using a fixed and random model circulating probability unification (FarmCUP) method. In total, 27 and 23 significant SNP-traits association signals were identified under normal and low N levels. In addition, 10 significant association signals were detected based on the traits relative value (normal N supply / low N supply) of two N levels. Further, 60 candidate genes were predicted for these traits base on linkage disequilibrium (LD) and low nitrogen transcriptome analysis of significant SNP regions. Among the candidate genes identified in this study, 66.7% involved in nitrogen compound metabolic process. Zm00001d025831 and Zm00001d004633 encoded ammonium transporter1 and transmembrane amino acid transporter family protein, respectively, may be important candidate genes for NUE. The markers identified in this study maybe has important significance and could be useful in molecular marker assisted selection in breeding of high-NUE maize varieties, and the candidate genes could deepen the understanding of the genetic basis of NUE.
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References
Agrama HAS, Zakaria AG, Said FB, Tuinstra M (1999) Identification of quantitative trait loci for nitrogen use efficiency in maize. Mol Breed 5:187–195. https://doi.org/10.1023/A:1009669507144
Ahmed M, Rauf M, Mukhtar Z, Saeed NA (2017) Excessive use of nitrogenous fertilizers: an unawareness causing serious threats to environment and human health. Environ Sci Pollut Res Int 24:26983–26987. https://doi.org/10.1007/s11356-017-0589-7
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Anne-Sophie B, Anne L, Christine B B, Cécile B, Jérôme M, Mathieu R G, Jean-Eric D, Pierre G, Xavier P, Thomas F, Olivier M, Damien D, Florent G, Nathalie N (2016) Genetic basis of nitrogen use efficiency and yield stability across environments in winter rapeseed. BMC Genet 17:131. https://doi.org/10.1186/s12863-016-0432-z
Bertin P, Gallais A (2000) Genetic variation for nitrogen use efficiency in a set of recombinant maize inbred lines I. Agrophysiological results Maydica 45:53–66
Bi YM, Meyer A, Downs GS, Shi X, El-Kereamy A, Lukens L, Rothstein SJ (2014) High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation. BMC Genomics 15:77. https://doi.org/10.1186/1471-2164-15-77
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Cai H, Chu Q, Yuan L, Liu J, Chen X, Chen F, Mi G, Zhang F (2012) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays L.) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266. https://doi.org/10.1007/s11032-011-9615-5
Cassman KG, Dobermann A, Waters DT (2002) Agroecosystems, nitrogen use efficiency, and nitrogen management. AMBIO: A J. of the Human Environment 31:132–140. https://doi.org/10.1579/0044-7447-31.2.132
Chen Q, Liu Z, Wang B, Wang X, Lai J, Tian F (2015) Transcriptome sequencing reveals the roles of transcription factors in modulating genotype by nitrogen interaction in maize. Plant Cell Rep 34:1761–1771. https://doi.org/10.1007/s00299-015-1822-9
Coque M, Bertin P, Hirel B, Gallais A (2006) Genetic variation and QTLs for N-15 natural abundance in a set of maize recombinant inbred lines. Field Crop Res 97:310–321. https://doi.org/10.1016/j.fcr.2005.11.002
Coque M, Gallais A (2006) Genomic regions involved in response to grain yield selection at high and low nitrogen fertilization in maize. Theor Appl Genet 112:1205–1220. https://doi.org/10.1007/s00122-006-0222-5
Coque M, Martin A, Veyrieras JB, Hirel B, Gallais A (2008) Genetic variation for N-remobilization and postsilking N-uptake in a set of maize recombinant inbred lines. 3. QTL detection and coincidences. Theor Appl Genet 117:729–747. https://doi.org/10.1007/s00122-008-0815-2
Cormier F, Le GJ, Dubreuil P, Lafarge S, Praud S (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
Gallais A, Hirel B (2004) An approach to the genetics of nitrogen use efficiency in maize. J Exp Bot 55:295–306. https://doi.org/10.1093/jxb/erh006
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674
Ganal MW, Durstewitz G, Polley A, Bérard A, Buckler ES, Charcosset A, Clarke JD, Graner EM, Hansen M, Joets J, Le Paslier MC, McMullen MD, Montalent P, Rose M, Schön CC, Sun Q, Walter H, Martin OC, Falque M (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One 6:e28334. https://doi.org/10.1371/journal.pone.0028334
Giles J (2005) Nitrogen study fertilizes fears of pollution. Nature 433:791. https://doi.org/10.1038/433791a
Gu R, Duan F, An X, Zhang F, Wire’n N, Yuan L (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol 54:1515–1524. https://doi.org/10.1093/pcp/pct099
Guo J, Liu X, Zhang Y, Shen J, Han W, Zhang W, Christie P, Goulding KW, Vitousek PM, Zhang F. (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010. https://doi.org/10.1126/science.1182570
He K, Chang L, Dong Y, Cui T, Qu J, Liu X, Xu S, Xue J, Liu J (2018) Identification of quantitative trait loci for agronomic and physiological traits in maize (Zea mays L.) under high-nitrogen and low-nitrogen conditions. Euphytica 214:15. https://doi.org/10.1007/s10681-017-2094-y
Hirel B, Bertin P, Quilleré I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125:1258–1270. https://doi.org/10.1104/pp.125.3.1258
Kamprath EJ, Moll RH, Rodriguez N (1982) Effects of nitrogen fertilization and recurrent selection on performance of hybrid populations of Corn1. Agron J 74:955–958. https://doi.org/10.2134/agronj1982.00021962007400060007x
Kant S, Bi Y, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509. https://doi.org/10.1093/jxb/erq297
Li F, Chung T, Pennington JG, Federico ML, Kaeppler HF, Kaeppler SM, Otegui MS, Vierstra RD (2015a) Autophagic recycling plays a central role in maize nitrogen remobilization. Plant Cell 27:1389–1408. https://doi.org/10.1105/tpc.15.00158
Li P, Chen F, Cai H, Liu J, Pan Q, Liu Z, Gu R, Mi G, Zhang F, Yuan L (2015b) A genetic relationship between nitrogen use efficiency and seedling root traits in maize as revealed by QTL analysis. J Exp Bot 66:3175–3188. https://doi.org/10.1093/jxb/erv127
Li P, Zhuang Z, Cai H, Cheng S, Soomro AA, Liu Z, Gu R, Mi G, Yuan L, Chen F (2016) Use of genotype-environment interactions to elucidate the pattern of maize root plasticity to nitrogen deficiency. J Integr Plant Biol 58:242–253. https://doi.org/10.1111/jipb.12384
Li P, Zhang Y, Yin S, Zhu P, Pan T, Xu Y, Wang J, Hao D, Fang H, Xu C, Yang Z (2018a) QTL-by-environment interaction in the response of maize root and shoot traits to different water regimes. Front Plant Sci 9:229. https://doi.org/10.3389/fpls.2018.00229
Li T, Qu J, Wang Y, Chang L, He K, Guo D, Zhang X, Xu S, Xue J (2018b) Genetic characterization of inbred lines from Shaan a and B groups for identifying loci associated with maize grain yield. BMC Genet 19:63. https://doi.org/10.1186/s12863-018-0669-9
Liao C, Peng Y, Ma W, Liu R, Li C, Li X (2012) Proteomic analysis revealed nitrogen-mediated metabolic, developmental, and hormonal regulation of maize (Zea mays L.) ear growth. J Exp Bot 63:5275–5288. https://doi.org/10.1093/jxb/ers187
Liu G, Sun A, Li D, Athman A, Gilliham M, Liu L (2015) Molecular identification and functional analysis of a maize (Zea mays L.) DUR3 homolog that transports urea with high affinity. Planta 241:861–874. https://doi.org/10.1007/s00425-014-2219-7
Liu J, Cai H, Chu Q, Chen X, Chen F, Yuan L, Mi G, Zhang F (2011) Genetic analysis of vertical root pulling resistance (VRPR) in maize using two genetic populations. Mol Breed 28:463–474. https://doi.org/10.1007/s11032-010-9496-z
Liu J, Li J, Chen F, Zhang F, Ren T, Zhuang Z, Mi G (2008) Mapping QTLs for root traits under different nitrate levels at the seedling stage in maize (Zea mays L.). Plant and Soil 305:253–265. https://doi.org/10.1007/s11104-008-9562-z
Liu N, Xue Y, Guo Z, Li W, Tang J (2016a) Genome-wide association study identifies candidate genes for starch content regulation in maize kernels. Front Plant Sci 7:1046. https://doi.org/10.3389/fpls.2016.01046
Liu R, Zhang H, Zhao P, Zhang Z, Liang W, Tian Z, Zheng Y (2012) Mining of candidate maize genes for nitrogen use efficiency by integrating gene expression and QTL data. Plant Mol Biol Rep 30:297–308. https://doi.org/10.1007/s11105-011-0346-x
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016b) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767
Liu X, Zhang Y, Han W, Tang A, Shen J, Cui Z, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang F (2013) Enhanced nitrogen deposition over China. Nature 494:459–462. https://doi.org/10.1038/nature11917
Liu Z, Zhu C, Yue J, Tian Y, Yu J, An H, Tang W, Sun J, Tang J, Chen G, Zhai H, Wang C, Wan J (2016c) Association mapping and genetic dissection of nitrogen use efficiency-related traits in rice (Oryza sativa L.). Funct Integr Genomics 16:323–333. https://doi.org/10.1007/s10142-016-0486-z
Luo B, Tang H, Liu H, Shunzong S, Zhang S, Wu L, Liu D, Gao S (2015) Mining for low-nitrogen tolerance genes by integrating meta-analysis and large-scale gene expression data from maize. Euphytica 206:1–15. https://doi.org/10.1007/s10681-015-1481-5
Lupini A, Mercati F, Araniti F, Miller AJ, Sunseri F, Abenavoli MR (2016) NAR2.1/NRT2.1 functional interaction with NO3− and H+ fluxes in high-affinity nitrate transport in maize root regions. Plant Physiol Biochem, 102:107–114. https://doi.org/10.1016/j.plaphy.2016.02.022
Mi G, Liu J, Zhang F (1998) Analysis on agronomic nitrogen efficiency and its components of maize hybrids. J China Agr University 3:97–104
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
Money D, Gardner K, Migicovsky Z, Schwaninger H, Zhong GY, Myles S (2015) LinkImpute: fast and accurate genotype imputation for nonmodel organisms. G3-Genes Genom Genet (Bethesda) 5:2383–2390. https://doi.org/10.1534/g3.115.021667
Monostori I, Szira F, Tondelli A, Arendas T, Gierczik K, Cattivelli L, Galiba G, Vagujfalvi A (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
Morosini JS, Mendonça LDF, Lyra DH, Galli G, Vidotti MS, Fritsche-Neto R (2017) Association mapping for traits related to nitrogen use efficiency in tropical maize lines under field conditions. Plant and Soil 421:1–11. https://doi.org/10.1007/s11104-017-3479-3
Ng JMS, Han M, Beatty PH, Good A (2016) “Genes, meet gases”: the role of plant nutrition and genomics in addressing greenhouse gas emissions. In: Edwards D, Batley J (eds) in plant genomics and climate change. Springer, New York, pp. 149–172. https://doi.org/10.1007/978-1-4939-3536-9_7
Nyquist WE, Baker RJ (1991) Estimation of heritability and prediction of selection response in plant populations. Crit Rev Plant Sci 10:235–322. https://doi.org/10.1080/07352689109382313
Paponov IA, Sambo P, Erley GS, Presterl T, Geiger HH, Engels C (2005) Grain yield and kernel weight of two maize genotypes differing in nitrogen use efficiency at various levels of nitrogen and carbohydrate availability during flowering and grain filling. Plant and Soil 272:111–123. https://doi.org/10.1007/s11104-004-4211-7
Schlüter U, Mascher M, Colmsee C, Scholz U, Bräutigam A, Fahnenstich H, Sonnewald U (2012) Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis. Plant Physiol 160:1384–1406. https://doi.org/10.1104/pp.112.204420
Silva IT, Abbaraju HKR, Fallis LP, Liu H, Lee M, Dhugga KS (2017) Biochemical and genetic analyses of N metabolism in maize testcross seedlings: 1. Leaves. Theor Appl Genet 130:1453–1466. https://doi.org/10.1007/s00122-017-2900-x
Silva IT, Abbaraju HKR, Fallis LP, Liu H, Lee M, Dhugga KS (2018) Biochemical and genetic analyses of N metabolism in maize testcross seedlings: 2. Roots. Theor Appl Genet 131:1191–1205. https://doi.org/10.1007/s00122-018-3071-0
Smil V (1999) Nitrogen in crop production: an account of global flows. Global Biogeochem Cycles 13:647–662. https://doi.org/10.1029/1999GB900015
Swarbreck SM, Defoinplatel M, Hindle M, Saqi M, Habash DZ (2011) New perspectives on glutamine synthetase in grasses. J Exp Bot 62:1511–1522. https://doi.org/10.1093/jxb/erq356
Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45:W122–W129. https://doi.org/10.1093/nar/gkx382
Uribelarrea M, Moose SP, Below FE (2007) Divergent selection for grain protein affects nitrogen use in maize hybrids. Field Crop Res 100:82–90. https://doi.org/10.1016/j.fcr.2006.05.008
Wang P, Wang Z, Pan Q, Sun X, Chen H, Chen F, Yuan L, Mi G (2019) Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis. J Exp Bot 70:1859–1873. https://doi.org/10.1093/jxb/erz047
Wiesler F, Behrens T, Horst WJ (2001) The role of nitrogen-efficient cultivars in sustainable agriculture. Scientific World J 1:61–69
Worku M, Bänziger M, Erley GSA, Friesen D, Diallo AO, Horst WJ (2007) Nitrogen uptake and utilization in contrasting nitrogen efficient tropical maize hybrids. Crop Sci 47:519–528. https://doi.org/10.2135/cropsci2005.05.0070
Xiong H, Guo H, Zhou C, Guo X, Xie Y, Zhao L, Gu J, Zhao S, Ding Y, Liu L (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
Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51:433–449. https://doi.org/10.2135/cropsci2010.04.0233
Zamboni A, Astolfi S, Zuchi S, Pii Y, Guardini K, Tononi P, Varanini Z (2014) Nitrate induction triggers different transcriptional changes in a high and a low nitrogen use efficiency maize inbred line. J Integr Plant Biol 56:1080–1094. https://doi.org/10.1111/jipb.12214
Zhang J, Fengler KA, Van Hemert JL, Gupta R, Mongar N, Sun J, Allen WB, Wang Y, Weers B, Mo H, Lafitte R, Hou Z, Bryant A, Ibraheem F, Arp J, Swaminathan K, Moose SP, Li B, Shen B (2019) Identifification and characterization of a novel stay-green QTL that increases yield in maize. Plant Biotechnol J 17:2272–2285. https://doi.org/10.1111/pbi.13139
Zhao Z, He K, Feng Z, Li Y, Chang L, Zhang X, Xu S, Liu J, Xue J (2019) Evaluation of yield-based low nitrogen tolerance indices for screening maize (Zea mays L.) inbred lines. Agronomy-Basel 9: 240. https://doi.org/10.3390/agronomy9050240
Zhu Z, Chen D (2002) Nitrogen fertilizer use in China-contributions to food production, impacts on the environment and best management strategies. Nutr Cycl Agroecosystems 63:117–127. https://doi.org/10.1023/A:1021107026067
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This study was financially supported by the Natural Key Research and Development Program of China (No.2017YFD010120301) and National Science Foundation of China (No.31301830).
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JL and JX designed the experiments. KH, XZ, YL, LC, YW, YS, TC, YD, TL, XL and YD carried out the experiments. KH, SX and RZ analyzed the data. KH and SX wrote the manuscript. JL and JX revised the manuscript. All authors read and approved the final manuscript.
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He, K., Xu, S., Zhang, X. et al. Mining of candidate genes for nitrogen use efficiency in maize based on genome-wide association study. Mol Breeding 40, 83 (2020). https://doi.org/10.1007/s11032-020-01163-3
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DOI: https://doi.org/10.1007/s11032-020-01163-3