Genomic basis of geographical adaptation to soil nitrogen in rice
Abstract
The intensive application of inorganic nitrogen underlies marked increases in crop production, but imposes detrimental effects on ecosystems 1,2: it is therefore crucial for future sustainable agriculture to improve the nitrogen-use efficiency of crop plants. Here we report the genetic basis of nitrogen-use efficiency associated with adaptation to local soils in rice (Oryza sativa L.). Using a panel of diverse rice germplasm collected from different ecogeographical regions, we performed a genome-wide association study on the tillering response to nitrogen-the trait that is most closely correlated with nitrogen-use efficiency in rice-and identified OsTCP19 as a modulator of this tillering response through its transcriptional response to nitrogen and its targeting to the tiller-promoting gene DWARF AND LOW-TILLERING (DLT)3,4. A 29-bp insertion and/or deletion in the OsTCP19 promoter confers a differential transcriptional response and variation in the tillering response to nitrogen among rice varieties. The allele of OsTCP19 associated with a high tillering response to nitrogen is prevalent in wild rice populations, but has largely been lost in modern cultivars: this loss correlates with increased local soil nitrogen content, which suggests that it might have contributed to geographical adaptation in rice. Introgression of the allele associated with a high tillering response into modern rice cultivars boosts grain yield and nitrogen-use efficiency under low or moderate levels of nitrogen, which demonstrates substantial potential for rice breeding and the amelioration of negative environment effects by reducing the application of nitrogen to crops.
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Biochemical conversion converts biomass into liquid fuels, natural gas, bio-products, and chemical building blocks using microbes and enzymes as catalysts.
“Biochemical conversion converts biomass into liquid fuels (e.g., alcohols and alkanes), natural gas (e.g., hydrogen and methane), different types of bio-products (e.g., carotenoids, omega-3 and omega-6 fatty acids), as well as other chemical building blocks (e.g., acetic acid and lactic acid) using microbes and enzymes as the catalyst.66”
From Technologies and perspectives for achieving carbon neutrality (2021) · cites this paper as [66]
Introduction of proliferating cell factor domain proteins such as OsTCP19-H into modern rice varieties has been shown to enhance NUE.
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From Technologies and perspectives for achieving carbon neutrality (2021) · cites this paper as [66]
Cites
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/519795 · Cited by 34,089 · see citing works
Li, H. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr509 · Cited by 6,283 · see citing works
Significant acidification in major Chinese croplands
Guo, J. H., Liu, X. J., Zhang, Y., Shen, J. L., Han, W. X., Zhang, W. F., Christie, P., Goulding, K. W. T., Vitousek, P. M., & Zhang, F. S. (2010) · Science · doi:10.1126/science.1182570 · Cited by 3,960 · see citing works
Self-citationGenome-wide efficient mixed-model analysis for association studies
Zhou, X., & Stephens, M. (2012) · Nature Genetics · doi:10.1038/ng.2310 · Cited by 3,627 · see citing works
Browning, S. R., & Browning, B. L. (2007) · The American Journal of Human Genetics · doi:10.1086/521987 · Cited by 3,138 · see citing works
Managing nitrogen for sustainable development.
Zhang, X., Davidson, E. A., Mauzerall, D. L., Searchinger, T. D., Dumas, P., & Shen, Y. (2015) · Nature · doi:10.1038/nature15743 · Cited by 3,054 · see citing works
ANGSD: Analysis of Next Generation Sequencing Data
Korneliussen, T. S., Albrechtsen, A., & Nielsen, R. (2014) · BMC Bioinformatics · doi:10.1186/s12859-014-0356-4 · Cited by 2,982 · see citing works
Plant Nitrogen Assimilation and Use Efficiency
Xu, G., Fan, X., & Miller, T. (2012) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105532 · Cited by 2,153 · see citing works
Genomic variation in 3,010 diverse accessions of Asian cultivated rice
Wang, W., Mauleon, R., Hu, Z., Chebotarov, D., Tai, S., Wu, Z., Li, M., Zheng, T., Fuentes, R. R., Zhang, F., et al. (2018) · Nature · doi:10.1038/s41586-018-0063-9 · Cited by 1,747 · see citing works
Self-citationAnalysis and Interpretation of Factors Which Contribute to Efficiency of Nitrogen Utilization1
Moll, R. H., Kamprath, E. J., & Jackson, W. A. (1982) · Agronomy Journal · doi:10.2134/agronj1982.00021962007400030037x · Cited by 1,724 · see citing works
A map of rice genome variation reveals the origin of cultivated rice
Huang, X., Kurata, N., Wei, X., Wang, Z.-X., Wang, A., Zhao, Q., Zhao, Y., Liu, K., Lu, H., Li, W., et al. (2012) · Nature · doi:10.1038/nature11532 · Cited by 1,631 · see citing works
Self-citationAn overview of global rice production, supply, trade, and consumption
Muthayya, S., Sugimoto, J. D., Montgomery, S. J., et al. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12540 · Cited by 1,583 · see citing works
Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies
Hu, B., Wang, W., Ou, S., Tang, J., Li, H., Che, R., Zhang, Z., Chai, X., Wang, H., Wang, Y., et al. (2015) · Nature Genetics · doi:10.1038/ng.3337 · Cited by 801 · see citing works
Self-citationProgress in ideotype breeding to increase rice yield potential
Peng, S., Khush, G. S., Virk, P. S., Tang, Q., & Zou, Y. (2008) · Field Crops Research · doi:10.1016/j.fcr.2008.04.001 · Cited by 800 · see citing works
Isozymes and classification of Asian rice varieties
Glaszmann, J.-C. (1987) · Theoretical and Applied Genetics · doi:10.1007/bf00290078 · Cited by 738 · see citing works
Modulating plant growth–metabolism coordination for sustainable agriculture
Li, S., Tian, Y., Wu, K., Ye, Y., Yu, J., Zhang, J., Liu, Q., Hu, M., Li, H., Tong, Y., et al. (2018) · Nature · doi:10.1038/s41586-018-0415-5 · Cited by 718 · see citing works
Rubin, G., Tohge, T., Matsuda, F., Saito, K., & Scheible, W. (2009) · The Plant Cell · doi:10.1105/tpc.109.067041 · Cited by 653 · see citing works
Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice
Wu, K., Wang, S., Song, W., Zhang, J., Wang, Y., Liu, Q., Yu, J., Ye, Y., Li, S., Chen, J., et al. (2020) · Science · doi:10.1126/science.aaz2046 · Cited by 471 · see citing works
Self-citationTong, H., Jin, Y., Liu, W., Li, F., Fang, J., Yin, Y., Qian, Q., Zhu, L., & Chu, C. (2009) · The Plant Journal · doi:10.1111/j.1365-313x.2009.03825.x · Cited by 418 · see citing works
Self-citationTong, H., Liu, L., Jin, Y. H., Du, L., Yin, Y., Qian, Q., Zhu, L., & Chu, C. (2012) · The Plant Cell · doi:10.1105/tpc.112.097394 · Cited by 417 · see citing works
Self-citationSNP-Seek database of SNPs derived from 3000 rice genomes
Alexandrov, N. N., Tai, S., Wang, W., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1039 · Cited by 390 · see citing works
Self-citationBreaking the yield frontier of rice
Khush, G. S. (1995) · GeoJournal · doi:10.1007/bf00989140 · Cited by 338 · see citing works
Russell, J., Mascher, M., Dawson, I. K., Kyriakidis, S., Calixto, C. P. G., Freund, F., Bayer, M., Milne, I., Marshall-Griffiths, T., Heinen, S. J., et al. (2016) · Nature Genetics · doi:10.1038/ng.3612 · Cited by 318 · see citing works
A study of allelic diversity underlying flowering-time adaptation in maize landraces
Navarro, J. A. R., Willcox, M. C., Burgueño, J. A., Romay, M. C., Swarts, K., Trachsel, S., Preciado, E., Terrón, A., Delgado, H. L. V., Vidal, V., et al. (2017) · Nature Genetics · doi:10.1038/ng.3784 · Cited by 307 · see citing works
ngsTools: methods for population genetics analyses from next-generation sequencing data
Fumagalli, M., Vieira, F. G., Linderoth, T. P., & Nielsen, R. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu041 · Cited by 252 · see citing works
TCP factors: new kids on the signaling block
Nicolas, M., & Cubas, P. (2016) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2016.05.006 · Cited by 250 · see citing works
Fang, Z., Ji, Y., Hu, J., Guo, R., Sun, S., & Wang, X. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.12.005 · Cited by 228 · see citing works
Xie, W., Wang, G., Yuan, M., Yao, W., Lyu, K., Zhao, H., Yang, M., Li, P., Zhang, X., Yuan, J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515919112 · Cited by 218 · see citing works
Self-citationQuantifying Population Genetic Differentiation from Next-Generation Sequencing Data
Fumagalli, M., Vieira, F. G., Korneliussen, T. S., Linderoth, T. P., Huerta‐Sánchez, E., Albrechtsen, A., & Nielsen, R. (2013) · Genetics · doi:10.1534/genetics.113.154740 · Cited by 201 · see citing works
OsTCP19 influences developmental and abiotic stress signaling by modulatingABI4-mediated pathways
Mukhopadhyay, P., & Tyagi, A. K. (2015) · Scientific Reports · doi:10.1038/srep09998 · Cited by 163 · see citing works
Wang, H., Xu, X., Vieira, F. G., Xiao, Y., Li, Z., Wang, J., Nielsen, R., & Chu, C. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.04.018 · Cited by 123 · see citing works
Self-citationAsian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated ricePreprint
Wang, H., Vieira, F. G., Crawford, J. E., Chu, C., & Nielsen, R. (2017) · Genome Research · doi:10.1101/gr.204800.116 · Cited by 123 · see citing works
Self-citationNitrogen-efficient rice cultivars can reduce nitrate pollution
Hakeem, K. R., Ahmad, A., Iqbal, M., et al. (2011) · Environmental Science and Pollution Research · doi:10.1007/s11356-010-0434-8 · Cited by 120 · see citing works
Yield potential and nitrogen use efficiency of China's super rice
Wang, F., & Peng, S. (2017) · Journal of Integrative Agriculture · doi:10.1016/s2095-3119(16)61561-7 · Cited by 119 · see citing works
Grain Yield and Yield Attributes of New Plant Type and Hybrid Rice
Yang, W., Peng, S., Laza, R. C., et al. (2007) · Crop Science · doi:10.2135/cropsci2006.07.0457 · Cited by 115 · see citing works
OsASN1 Plays a Critical Role in Asparagine-Dependent Rice Development
Luo, L., Qin, R., Liu, T., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms20010130 · Cited by 81 · see citing works
Li, C., Zhu, S., Zhang, H., Chen, L., Cai, M., Wang, J., Chai, J., Wu, F., Cheng, Z., Guo, X., et al. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.03.104 · Cited by 63 · see citing works
CDKB2 is involved in mitosis and DNA damage response in rice
Endo, M., Nakayama, S., Umeda‐Hara, C., Ohtsuki, N., Saika, H., Umeda, M., & Toki, S. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04847.x · Cited by 53 · see citing works
Guerrero, J., Andrello, M., Burgarella, C., & Manel, S. (2018) · New Phytologist · doi:10.1111/nph.15171 · Cited by 38 · see citing works
Identification and expression analysis of rice histone genes
Hu, Y., & Lai, Y. (2014) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2014.11.012 · Cited by 37 · see citing works
The Genomic Basis of Local Climatic Adaptation
Savolainen, O. (2011) · Science · doi:10.1126/science.1213788 · Cited by 33 · see citing works
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Technologies and perspectives for achieving carbon neutrality
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- Authors
- Liu, Y., Wang, H., Jiang, Z., Wang, W., Xu, R., Wang, Q., Zhang, Z., Li, A., Liang, Y., Ou, S., Liu, X., Cao, S., Tong, H., Wang, Y., Zhou, F., Liao, H., Hu, B., & Chu, C.
- Affiliations
- Chinese Academy of Sciences (CN)
- South China Agricultural University (CN)
- Peking University (CN)
- Chinese Academy of Agricultural Sciences (CN)
- Corresponding author
- Hu, Bin
- Chu, Chengcai
- ORCID
- Venue
- Nature
- Published
- 2021-01-06
- Volume
- 590
- Issue
- 7847
- Pages
- 600-605
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W3119006924
- Cited by
- 468
- References
- 41
- Citations by year
- 2026: 72 · 2025: 91 · 2024: 98 · 2023: 90 · 2022: 79 · 2021: 38
- FWCI
- 47.46
- Type
- journal article
- Language
- en
- Update notices
- correction (2022-09-23)
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Rice Cultivation and Yield Improvement
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
- Keywords
- rice, nitrogen use efficiency, geographical adaptation, soil nitrogen, introgression, grain yield, sustainable agriculture
- MeSH terms
- Genetic Introgression, Adaptation, Physiological, Alleles, Epistasis, Genetic, Nitrogen, Plant Proteins, Promoter Regions, Genetic, Oryza, Soil, Genetic Variation, Gene Expression Regulation, Plant, Crops, Agricultural, INDEL Mutation, Genome-Wide Association Study
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