Abstract
Rice production relies on large amounts of synthetic nitrogen fertilizer to meet crop nutritional demands. However, the current fertilizer use efficiency is poor, with an average of 30–50% of total applied nitrogen (N) recovered in grains. Consequently, optimizing N availability and N use efficiency (NUE) has become a major target for rice yield improvement, and looking for quantitative trait loci (QTL) associated with NUE can provide useful information for developing nitrogen efficient rice genotypes. The present study aims to identify QTLs associated with NUE and its two components, agronomic NUE (agNUE) and grain nitrogen increase rate (GIR). A recombinant inbred line population (RIL) derived from a cross between Nipponbare and OM052, consisting of 159 F3 individuals was developed and cultivated in low-N (8 kg N/0.67 ha, N8) and high-N (18 kg N/0.67 ha, N18) conditions. Specific length amplified fragment sequencing (SLAF) was used to genotype the RILs and construct a high-density linkage map spanning 1587.70 cM, consisting 2707 SLAF markers with an average interval of 0.59 cM between adjacent marker loci. QTL analysis confirmed four significant QTLs distributed among chromosome 1, 6, and 11, with the proportion of phenotypic variance explained by each QTL ranging from 2.96 to 11.11% and LOD scores from 1.67 to 3.75. Functional annotation of genes located within the QTL intervals revealed NUE putative candidate genes. Overall, the QTLs identified in this study contribute information that could be useful for NUE improvement in rice.
Similar content being viewed by others
References
Altshuler D et al (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516
Baird NA et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PloS One 3
Broman KW, Hao W, Sen Ś et al (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 7:889–890
Che SG, Zhao BQ, Li YT, Yuan L, Li W, Lin ZA et al (2015) Review grain yield and nitrogen use efficiency in rice production regions in China. J Integr Agric 14:2456–2466
Chen S et al (2013) The development of 7E chromosome-specific molecular markers for Thinopyrum elongatum based on SLAF-seq technology. PLoS One 86:e65122
Chen YY, Fua X, Mei X, Zhou Y et al (2017) Proteolysis of chloroplast proteins is responsible for accumulation of free amino acids in dark-treated tea (Camellia sinensis) leaves. J Proteomics 157:10–17
Cho YI, Jiang WZ, Chin JH, Piao ZZ, Cho YG, McCouch SR et al (2007) Identification of QTLs associated with physiological nitrogen use efficiency in rice. Mol Cells 23:72–79
Dai et al (2015) Mapping quantitative trait loci for nitrogen uptake and utilization efficiency in rice (Oryza sativa L.) at different nitrogen fertilizer levels. Genet Mol Res 14 (3)10404–10414
Darvasi A, Weinreb A, Minke V, Weller JI, Soller M (1993) Detecting marker-QTL linkage and estimating QTL gene effect and map location using a saturated genetic map. Genetics 134:943–951
Davey JW et al (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
Edgerton MD (2009) Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol 149:7–13
Guo Y et al (2015) Using specific length amplified fragment sequencing to construct the high-density genetic map for Vitis (Vitis vinifera L. × Vitis amurensis Rupr.). Front Plant Sci 6, 393
Horrigan LR, Lawrence RS, Walker P (2002) How sustainable agriculture can address the environmental and human health harms of industrial agriculture. Environ Health Perspect 110(5):445
Huang S, Ding J et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4
Jia Q, Tan C, Wang J et al (2016) Marker development using SLAF-seq and whole-genome shotgun strategy to fine-map the semi-dwarf gene ari-e in barley. BMC Genomics 17:911
Kan CC, Chung TY, Juo YA, Hsieh MH (2015) Glutamine rapidly induces the expression of key transcription factor genes involved in nitrogen and stress responses in rice roots. BMC Genomics16 (1):731
Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12(4):656–664
Khoury CK, Bjorkman AD, Dempewolf H, Ramirez-Villegas J, Guarino L, Jarvis A, Rieseberg LH, Struik PC (2014) Increasing homogeneity in global food supplies and the implications for food security. Proc Natl Acad Sci 111(11):4001–4006
Li YF, Li MM, Cao GL, Han LZ (2010) Effects of genetic background on expression of QTL for nitrogen efficiency in irrigated rice and upland rice. Sci Agric Sin 43:4331–4340
Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7(11):e48951. https://doi.org/10.1371/journal.pone.0048951
Liu DY, Ma CX, Hong WG, Huang L, Liu M, Liu H et al (2014) Construction and analysis of high-density linkage map using high-throughput sequencing data. PLoS One 9:e98855
Liu R, Zhang H, Zhao PP, Rep MB et al (2012) Mining of candidate maize genes for nitrogen use efficiency by integrating gene expression and QTL data. Plant Mol Biol Report 30:297. https://doi.org/10.1007/s11105-011-0346-x
Mita P, Boeke JD (2016) How retrotransposons shape genome regulation. Curr Opin Genet Dev 37:90–100
Murray HG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326
Muthayya S, Sugimoto JD, Montgomery S, Maberly GF (2014) An overview of global rice production, supply, trade, and consumption. Ann NY Acad Sci 1324:7–14
Nguyen DT, Dang C, PhamV BertinP (2016) QTL mapping for nitrogen use efficiency and related physiological and agronomical traits during the vegetative phase in rice under hydroponics. Euphytica 212(3):473–500
Obara M, Kajiura M, Fukuta Y, Yano M, Hayashi M, Yamaya T et al (2001) Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.). J Exp Bot 52:1209–1217
Qi ZM, Huang L, Zhu RS, Xin D, Liu CY, Han X et al (2014) A high-density genetic map for soybean based on specific length amplified fragment sequencing. PLoS One 8:e104871
Reyes JC (2014) The many faces of plant SWI/SNF complex. Mol Plant. Mar;7(3):454–8. https://doi.org/10.1093/mp/sst147
Sarnowska EA, Rolicka AT, Bucior E, Cwiek P, Tohge T, Fernie AR, Sarnowski TJ (2013) DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol 163(1):305–317. https://doi.org/10.1104/pp.113.223933
Senthilvel S, Vinod KK, Malarvizhi P, Maheswaran M (2008) QTL and QTL x environment effects on agronomic and nitrogen acquisition traits in rice. J Integr Plant Biol 50:1108–1117
Shan YH, Wang YL, Pan XB (2005) Mapping of QTLs for nitrogen use efficiency and related traits in rice (Oryza sativa L.). Agric Sci Chin 4:721–727
Sun X et al (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8:e58700
Van Ooijen J (2006) JoinMap 4: software for the calculation of genetic linkage maps in experimental populations of diploid species. Plant Research International BV and Kyazma BV, Wageningen, Netherlands
Wang S, Meyer E, McKay JK, Matz MV (2012) 2b-RAD: a simple and flexible method for genome-wide genotyping. Nat Methods 9(8):808–10
Wei D, Cui KH, Pan JF, Ye GY, Xiang J, Nie LX et al (2011) Genetic dissection of grain nitrogen use efficiency and grain yield and their relationship in rice. Field Crops Res 124:340–346
Wei D, Cui KH, Ye GY, Pan JF, Xiang J, Huang JL et al (2012) QTL mapping for nitrogen-use efficiency and nitrogen-deficiency tolerance traits in rice. Plant Soil 359:281–295
Xu F, Sun X, Chen Y, Huang Y, Tong C, Bao J (2015) Rapid identification of major QTLs associated with rice grain weight and their utilization. PLoS One 10(3):e0122206. https://doi.org/10.1371/journal.pone.0122206
Xu, X et al (2014) A high-density genetic map of cucumber derived from Specific Length Amplified Fragment sequencing (SLAF-seq). Front Plant Sci 5
Yang X, Xia X, Zhang Z, Nong B, Zeng Y, Xiong F, Wu Y, Gao J, Deng G, Li D (2017) QTL mapping by whole genome re-sequencing and analysis of candidate genes for nitrogen use efficiency in rice. Front Plant Sci 8:1634. https://doi.org/10.3389/fpls.2017.01634
Yin C, Li H, Li S, Xu L, Zhao Z, Wang J (2015) Genetic dissection on rice grain shape by the two-dimensional image analysis in one japonica × indica population consisting of recombinant inbred lines. TAG. Theor Appl Genet 128(10), 1969–1986. https://doi.org/10.1007/s00122-015-2560-7
Zhang J, Lan T, Müller C, Cai Z (2015) Dissimilatory nitrate reduction to ammonium (DNRA) plays an important role in soil nitrogen conservation in neutral and alkaline but not acidic rice soil. J soils sediments 15(3):523–531
Zhang Q, Yang Z, Zhang H, Yi J (2012) Recovery efficiency and loss of 15N-labelled urea in a rice-soil system in the upper reaches of the Yellow River basin. Agr Ecosyst Environ 158:118–126
Zhang YX, Wang LH, Xin HG, Li DH, Ma CX, Ding X et al (2013) Construction of a high-density genetic map for sesame based on large scale marker development by specific length amplification fragment (SLAF). BMC Plant Biol 13:141
Zhou Y, Tao Y, Tang D Wang J et al (2017) Identification of QTL associated with nitrogen uptake and nitrogen use efficiency using high throughput genotyped CSSLs in rice (Oryza sativa L.). Front Plant Sci 8 (1) 8
Acknowledgements
This work was supported by the National Key Research and Development Program (2017YFD0301304), International cooperation project of Anhui province (1704e1002232), Shanghai Agriculture Applied Technology Development Program (Grant No. T20180201), SAAS Excellent Research Team (No. NKC2017A05), and International Cooperation Project of China and South Korea (PJ013647).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation were performed by Jianjiang Bai, Zhongze Piao, Changzhao Wan, and Gangseob Lee. Data collection and analysis were performed by Jianjiang Bai, Xinmin Ruan, Zhixiang Luo, Fuzhi Shi, Xihan Cong, and Jun Fang. The first draft of the manuscript was written by Jianjiang Bai, Zhongze Piao, Gangseob Lee, and Ruifang Yang. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Additional information
Key message
• Specific length amplified fragment sequencing (SLAF)-based technology was used to build a high-density genetic linkage map, develop high-throughput SNP-based markers and identify four QTLs associated with rice nitrogen use efficiency (NUE). Analysis of gene functions located within the QTL intervals revealed the potential candidate genes involved in rice NUE
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bai, J., Piao, Z., Wan, C. et al. SLAF-Based Linkage Map Construction and QTL Mapping of Nitrogen Use Efficiency in Rice (Oryza sativa L.). Plant Mol Biol Rep 39, 727–738 (2021). https://doi.org/10.1007/s11105-021-01281-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-021-01281-y