Abstract
Nitrogen (N) is the most important macronutrient for plant growth and development. Hence, understanding genetic architectures and functional genes involved in the response to N deficiency can greatly facilitate the development of low-N-tolerant cultivars. In this study, we collected 212 quantitative trait loci (QTL) of agronomically important traits under low-N stress conditions in maize. We then identified 21 consensus QTL (cQTL) strongly induced for low-N tolerance after excluding overlapping cQTL containing QTL simultaneously identified in meta-analyses of studies performed under other environmental conditions. Among the 21 cQTL, 30 candidate maize genes were identified from maize large-scale differential expression data derived from analyses of low-N stress, and the 12 most important maize orthologs were identified using homologous BLAST analyses of genes with known functions in N use efficiency in model plants. Furthermore, maize orthologs associated with low-N tolerance and metabolism were also predicted using large-scale expression data from other model plants. The present genetic loci and candidate genes indicate the molecular mechanisms of low-N tolerance in maize and may provide information for QTL fine mapping and molecular marker-assisted selection.
Similar content being viewed by others
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
Araki R, Hasegawa H (2006) Expression of rice (Oryza sativa L.) genes involved in high-affinity nitrate transport during the period of nitrate induction. Breed Sci 56:295–302
Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genom. doi:10.1186/1471-2164-8-281
Bi YM, Kant S, Clark J, Gidda S, Ming F, Xu JY, Rochon A, Shelp BJ, Hao LX, Zhao R, Mullen R, Zhu T, Rothstein SJ (2009) Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant Cell Environ 32:1749–1760
Cai H, Chu Q, Gu R, Yuan L, Liu J, Zhang X, Chen F, Mi G, Zhang F (2012a) Identification of QTLs for plant height, ear height and grain yield in maize (Zea mays L.) in response to nitrogen and phosphorus supply. Plant Breed 131:502–510
Cai H, Chu Q, Yuan L, Liu J, Chen X, Chen F, Mi G, Zhang F (2012b) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266
Cai H, Lu Y, Xie W, Zhu T, Lian X (2012c) Transcriptome response to nitrogen starvation in rice. J Biosci 37:731–747
Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A (2004) Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168:2169–2185
Chen L, Bush DR (1997) LHTl, a lysine-and histidine-specific transporter in Arabidopsis amino acid. Plant Physiol 115:1127–1134
Chen R, Tian M, Wu X, Huang Y (2011) Differential global gene expression changes in response to low nitrogen stress in two maize inbred lines with contrasting low nitrogen tolerance. Genes Genomics 33:491–497
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
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
Eveland AL, Satoh-Nagasawa N, Goldshmidt A, Meyer S, Beatty M, Sakai H, Ware D, Jackson D (2010) Digital gene expression signatures for maize development. Plant Physiol 154:1024–1039
Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci USA 96:1175–1180
Fu J, Tian H, Gao YJ (2013) Study progress of molecular approaches in improving nitrogen use efficiency of crop plants. Soil Fertil Sci China 4:79–82
Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283
Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci USA 105:803–808
Giles J (2005) Nitrogen study fertilizes fears of pollution. Nature 433:791–791
Goffinet B, Gerber S (2000) Quantitative trait loci: a meta-analysis. Genetics 155:463–473
Hao Z, Li X, Liu X, Xie C, Li M, Zhang D, Zhang S (2010) Meta-analysis of constitutive and adaptive QTL for drought tolerance in maize. Euphytica 174:165–177
Himer A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946
Hirel B, Bertin P, Quilleré I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Catherine R, 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
Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194
Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278
Humbert S, Subedi S, Cohn J, Zeng B, Chen X, Zhu T, McNicholas PD, Rothstein SJ (2013) Genome-wide expression profiling of maize in response to individual and combined water and nitrogen stresses. BMC Genom. doi:10.1186/1471-2164-14-3
Hung HY, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF, Holland JB (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA 109:1913–1921
Ishiyama K, Inoue E, Tabuchi M, Yamaya T, Takahashi H (2004) Biochemical background and compartmentalized functions of cytosolic glutamine synthetase for active ammonium assimilation in rice roots. Plant Cell Physiol 45:1640–1647
Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509
Krapp A, Berthomé R, Orsel M, Mercey-Boutet S, Yu A, Castaings L, Elftieh S, Major H, Renou JP, Daniel-vedele F (2011) Arabidopsis roots and shoots show distinct temporal adaptation patterns toward nitrogen starvation. Plant Physiol 157:1255–1282
Krouk G, Grawford NM, Coruzzi GM, Tsay YF (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273
Kurai T, Wakayama M, Abiko T, Schuichi Y, Aoki N, Ohugi R (2011) Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnol J 9:826–837
Li JY, Fu YL, Pike SM, Bao J, Tian W, Zhang Y, Chen CZ, Zhang Y, Li HM, Huang J, Li LG, Schroeder JI, Gassmann W, Gong JM (2010a) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646
Li L, Li H, Li J, Xu S, Yang X, Li J, Yan J (2010b) A genome-wide survey of maize lipid-related genes: candidate genes mining, digital gene expression profiling and co-location with QTL for maize kernel oil. Sci China Life Sci 53:690–700
Li WJ, Liu ZZ, Shi YS, Song YC, Wang TY, Xu CW, Li Y (2010c) Detection of consensus genomic region of QTLs relevant to drought-tolerance in maize by QTL meta-analysis and bioinformatics approach. Acta Agron Sin 36:1457–1467
Li L, Li H, Li Q, Yang X, Zheng D, Warburton M, Chai Y, Zhang P, Guo Y, Yan J, Li J (2011) An 11-bp insertion in Zea mays fatb reduces the palmitic acid content of fatty acids in maize grain. PLoS One. doi:10.1371/journal.pone.0024699
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One. doi:10.1371/journal.pone.0048951
Liseron-Monfils C, Bi YM, Downs GS, Wu W, Signorelli T, Lu G, Chen X, Bondo E, Zhu T, Lukens LN, Colasanti J, Rothstein SJ, Raizada MN (2013) Nitrogen transporter and assimilation genes exhibit developmental stage-selective expression in maize (Zea mays L.) associated with distinct cis-acting promoter motifs. Plant Signal Behav. doi:10.4161/psb.26056
Liu XH, He SL, Zheng ZP, Huang YB, Tan ZB, Li Z, He C, Wu X, Pu QB (2010a) Identification of the QTLs for grain yield using RIL population under different nitrogen regimes in maize. Afr J Agric Res 5:2002–2007
Liu XH, Zheng ZP, Tan ZB, Li Z, He C (2010b) Quantitative trait locus (QTL) mapping for 100-kernel weight of maize (Zea mays L.) under different nitrogen regimes. Afr J Biotechnol 9:8283–8289
Liu XH, He SL, Zheng ZP, Huang YB, Tan ZB, Wu X (2010c) QTL identification for row number per ear and grain number per row in maize. Maydica 55:127–133
Liu XH, He S, Zheng Z, Tan Z, Liu D (2010d) Identification of the quantitative trait loci for grain rate in maize. Afr J Biotechnol 9:8007–8012
Liu XH, Zheng ZP, Tan ZB, Li Z, He C (2010e) Genetic analysis of two new quantitative trait loci for ear weight in maize inbred line Huangzao4. Genet Mol Res 9:2140–2147
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
Loqué D, Wirén NV (2004) Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 55:1293–1305
Lu H, Xue J, Ma G, Zhang R, Zhang X (2010) Effects of low nitrogen stress on source-sink characters and grain-filling traits of different genotypes summer maize. Chin J Appl Ecol 21:1277–1282
Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Laforgue TT, Quilleré I, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell 18:3252–3274
Peng M, Bi YM, Zhu T, Rothstein SJ (2007) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65:775–797
Plett D, Toubia J, Garnett T, Tester M, Kaiser BN, Ute B (2010) Dichotomy in the NRT gene families of dicots and grass species. PLoS One. doi:10.1371/journal.pone.0015289
Ribaut JM, Frachebound Y, Monneveux P, Banziger M, Vargas M, Jiang C (2007) Quantitative trait loci for yield and correlated traits under high and low soil nitrogen conditions in tropical maize. Mol Breed 20:15–29
Semagn K, Beyene Y, Warburton ML, Tarekegne A, Mugo S, Meisel B, Sehabiague P, Prasanna BM (2013) Meta-analyses of QTL for grain yield and anthesis silking interval in 18 maize populations evaluated under water-stressed and well-watered environments. BMC Genom. doi:10.1186/1471-2164-14-313
Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H (2014) Fu X (2014) Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat Genet 46:652–656
Swamy BPM, Sarla N (2011) Meta-analysis of yield QTLs derived from inter-specific crosses of rice reveals consensus regions and candidate genes. Plant Mol Biol Rep 29:663–680
Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–713
Tuberosa R, Salvi S, Sanguineti MC, Landi P, Maccaferri M, Conti S (2002) Mapping QTL regulating morpho-physiological traits and yield: case studies, shortcomings and perspectives in drought-stressed maize. Ann Bot 89:941–963
Wu X, Liu Y, Tian M, Chen R, Zheng Z, He C, Huang Y, Zhang J, Liu H, Li Z (2011) Genomics analysis of genes expressed reveals differential responses to low chronic nitrogen stress in maize. Afr J Biotechnol 10:939–949
Xu Z, Zhong S, Li X, Li W, Rothstein SJ, Zhang S, Bi Y, Xie C (2011) Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS One. doi:10.1371/journal.pone.0028009
Xu G, Fan X, Miller AJ (2012a) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182
Xu J, Liu Y, Cao M, Wang J, Lan H, Xu Y, Lu Y, Pan G, Rong T (2012b) The genetic architecture of flowering time and photoperiod sensitivity in maize as revealed by QTL review and meta analysis. J Integr Plant Biol 54:358–373
Yao Q, Hu F, Xu J (2011) The effects of low-N stress on plant morphology and photosynthesis of maize landraces at seedling stage. J Henan Agric Sci 40:37–41
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 56:1080–1089
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409
Zhang W, Zhao Z, Bai G, Fu F, Cao S (2007) Response on water stress and low nitrogen in different maize hybrid varieties and evaluation for their adversity-resistance. Sci Agric Sin 40:1361–1370
Zhang H, Zheng Z, Liu X, Li Z, He C, Liu D, Luo Y, Zhang G, Tan Z, Li R (2010a) QTL mapping for ear length and ear diameter under different nitrogen regimes in maize. Afr J Agric Res 5:626–630
Zhang X, Xue J, Liu W, Li F, Zhang R (2010b) Screening and identification of low nitrogen tolerance in different maize hybrids. Acta Agric Boreal Occident Sin 19:65–68
Zhang J, Xu L, Wang F, Deng M, Yi K (2012) Modulating the root elongation by phosphate/nitrogen starvation in an OsGLU3 dependant way in rice. Plant Signal Behav 7:1144–1145
Zhang HW, Uddin MS, Zou C, Xie C, Xu Y, Li WX (2014) Meta-analysis and candidate gene mining of low-phosphorus tolerance in maize. J Integr Plant Biol 56:262–270
Zhao XQ, Shi WM (2006) Expression analysis of the glutamine synthetase and glutamate synthase gene families in young rice (Oryza sativa) seedlings. Plant Sci 170:748–754
Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li WX (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One. doi:10.1371/journal.pone.0029669
Zheng ZP, Liu XH (2013a) Genetic analysis of agronomic traits associated with plant architecture by QTL mapping in maize. Genet Mol Res 12:1243–1253
Zheng ZP, Liu XH (2013b) QTL identification of ear leaf morphometric traits under different nitrogen regimes in maize. Genet Mol Res 12:4342–4351
Zheng Z, He C, Li Z, Huang Y (2005) Detecting QTLs for ear length under two nitrogen levels. J Maize Sci 13:102–104
Zheng ZP, Liu XH, Wu X, Zhang YS, He C (2011) Genetic loci mapping for ear axis weight using recombinant inbred line (RIL) population under different nitrogen regimes in maize. Afr J Biotechnol 10:8255–8259
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31361140364 and 31471511), the 948 Project of Ministry of Agriculture of China (2011-G15-2 and 2013-Z38), and the Key Technologies R&D Program of China during the 12th Five-Year Plan period (2011BAD35B01).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Luo, B., Tang, H., Liu, H. et al. Mining for low-nitrogen tolerance genes by integrating meta-analysis and large-scale gene expression data from maize. Euphytica 206, 117–131 (2015). https://doi.org/10.1007/s10681-015-1481-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-015-1481-5