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      Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice

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          Abstract

          Over-application of nitrogen fertilizer in fields has had a negative impact on both environment and human health. Domesticated rice varieties with high nitrogen use efficiency (NUE) reduce fertilizer for sustainable agriculture. Here, we perform genome-wide association analysis of a diverse rice population displaying extreme nitrogen-related phenotypes over three successive years in the field, and identify an elite haplotype of nitrate transporter OsNPF6.1 HapB that enhances nitrate uptake and confers high NUE by increasing yield under low nitrogen supply. OsNPF6.1 HapB differs in both the protein and promoter element with natural variations, which are differentially trans-activated by OsNAC42, a NUE-related transcription factor. The rare natural allele OsNPF6.1 HapB , derived from variation in wild rice and selected for enhancing both NUE and yield, has been lost in 90.3% of rice varieties due to the increased application of fertilizer. Our discovery highlights this NAC42-NPF6.1 signaling cascade as a strategy for high NUE and yield breeding in rice.

          Abstract

          Improving crop nitrogen use efficiency can facilitate sustainable production, however, the genetic mechanisms have not been fully revealed. Here, the authors discover the NAC42-NPF6.1 signaling cascade mainly derives from  indica and wild rice and demonstrate the potential of using the allele for cultivar improvement.

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          Most cited references34

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          Plant nitrogen assimilation and use efficiency.

          Crop productivity relies heavily on nitrogen (N) fertilization. Production and application of N fertilizers consume huge amounts of energy, and excess is detrimental to the environment; therefore, increasing plant N use efficiency (NUE) is essential for the development of sustainable agriculture. Plant NUE is inherently complex, as each step-including N uptake, translocation, assimilation, and remobilization-is governed by multiple interacting genetic and environmental factors. The limiting factors in plant metabolism for maximizing NUE are different at high and low N supplies, indicating great potential for improving the NUE of current cultivars, which were bred in well-fertilized soil. Decreasing environmental losses and increasing the productivity of crop-acquired N requires the coordination of carbohydrate and N metabolism to give high yields. Increasing both the grain and N harvest index to drive N acquisition and utilization are important approaches for breeding future high-NUE cultivars.
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            Association mapping in structured populations.

            The use, in association studies, of the forthcoming dense genomewide collection of single-nucleotide polymorphisms (SNPs) has been heralded as a potential breakthrough in the study of the genetic basis of common complex disorders. A serious problem with association mapping is that population structure can lead to spurious associations between a candidate marker and a phenotype. One common solution has been to abandon case-control studies in favor of family-based tests of association, such as the transmission/disequilibrium test (TDT), but this comes at a considerable cost in the need to collect DNA from close relatives of affected individuals. In this article we describe a novel, statistically valid, method for case-control association studies in structured populations. Our method uses a set of unlinked genetic markers to infer details of population structure, and to estimate the ancestry of sampled individuals, before using this information to test for associations within subpopulations. It provides power comparable with the TDT in many settings and may substantially outperform it if there are conflicting associations in different subpopulations.
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              CHL1 functions as a nitrate sensor in plants.

              Ions serve as essential nutrients in higher plants and can also act as signaling molecules. Little is known about how plants sense changes in soil nutrient concentrations. Previous studies showed that T101-phosphorylated CHL1 is a high-affinity nitrate transporter, whereas T101-dephosphorylated CHL1 is a low-affinity transporter. In this study, analysis of an uptake- and sensing-decoupled mutant showed that the nitrate transporter CHL1 functions as a nitrate sensor. Primary nitrate responses in CHL1T101D and CHLT101A transgenic plants showed that phosphorylated and dephosphorylated CHL1 lead to a low- and high-level response, respectively. In vitro and in vivo studies showed that, in response to low nitrate concentrations, protein kinase CIPK23 can phosphorylate T101 of CHL1 to maintain a low-level primary response. Thus, CHL1 uses dual-affinity binding and a phosphorylation switch to sense a wide range of nitrate concentrations in the soil, thereby functioning as an ion sensor in higher plants. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.
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                Author and article information

                Contributors
                wangchm@njau.edu.cn
                wanjianmin@caas.cn
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                21 November 2019
                21 November 2019
                2019
                : 10
                : 5279
                Affiliations
                [1 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Jiangsu Collaborative Innovation Center for Modern Crop Production, , Nanjing Agricultural University, ; Nanjing, 210095 China
                [2 ]Key Laboratory of Biology, Genetics and Breeding of Japonica Rice in the Mid-lower Yangtze River, Ministry of Agriculture, Jiangsu Plant Gene Engineering Research Center, Nanjing, 210095 China
                [3 ]ISNI 0000000119573309, GRID grid.9227.e, State Key Laboratory of Plant Genomics, Institute of Microbiology, , Chinese Academy of Sciences, ; Beijing, 100101 China
                [4 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, CAS Center for Excellence in Biotic Interactions, , University of Chinese Academy of Sciences, ; Beijing, 100049 China
                [5 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, , Nanjing Agricultural University, ; Nanjing, 210095 China
                [6 ]ISNI 0000 0000 8510 1943, GRID grid.268256.d, Department of Biology, , Wilkes University, ; Wilkes-Barre, PA 18766 USA
                [7 ]ISNI 0000 0001 0526 1937, GRID grid.410727.7, National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, , Chinese Academy of Agricultural Sciences, ; Beijing, 100081 China
                Author information
                http://orcid.org/0000-0002-7741-4354
                http://orcid.org/0000-0002-9228-2687
                http://orcid.org/0000-0003-2704-6677
                http://orcid.org/0000-0002-7536-6432
                Article
                13187
                10.1038/s41467-019-13187-1
                6872725
                31754193
                994aab5c-5726-453c-857c-c8f53d116d95
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 26 March 2019
                : 24 October 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001809, National Natural Science Foundation of China (National Science Foundation of China);
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                agricultural genetics,plant breeding
                Uncategorized
                agricultural genetics, plant breeding

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