Please wait a minute...
Frontiers of Agricultural Science and Engineering

ISSN 2095-7505

ISSN 2095-977X(Online)

CN 10-1204/S

Postal Subscription Code 80-906

Front. Agr. Sci. Eng.    2022, Vol. 9 Issue (3) : 316-332    https://doi.org/10.15302/J-FASE-2022441
REVIEW
ROLE OF NITROGEN SENSING AND ITS INTEGRATIVE SIGNALING PATHWAYS IN SHAPING ROOT SYSTEM ARCHITECTURE
Hui LIU1, Qian LIU1, Xiuhua GAO1(), Xiangdong FU1,2()
1. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
2. College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
 Download: PDF(3958 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

● The Green Revolution broadened the trade-off between yield and nitrogen-use efficiency.

● Root developmental and metabolic adaptations to nitrogen availability.

● Mechanisms of nitrogen uptake and assimilation have been extensively studied.

● Modulating plant growth-metabolic coordination improves nitrogen-use efficiency in crops.

The Green Revolution of the 1960s boosted crop yields in part through widespread production of semidwarf plant cultivars and extensive use of mineral fertilizers. The beneficial semidwarfism of cereal Green Revolution cultivars is due to the accumulation of plant growth-repressing DELLA proteins, which increases lodging resistance but requires a high-nitrogen fertilizer to obtain high yield. Given that environmentally degrading fertilizer use underpins current worldwide crop production, future agricultural sustainability needs a sustainable Green Revolution through reducing N fertilizer use while boosting grain yield above what is currently achievable. Despite a great deal of research efforts, only a few genes have been demonstrated to improve N-use efficiency in crops. The molecular mechanisms underlying the coordination between plant growth and N metabolism is still not fully understood, thus preventing significant improvement. Recent advances of how plants sense, capture and respond to varying N supply in model plants have shed light on how to improve sustainable productivity in agriculture. This review focuses on the current understanding of root developmental and metabolic adaptations to N availability, and discuss the potential approaches to improve N-use efficiency in high-yielding cereal crops.

Keywords Nitrogen      root system architecture      phytohormone      crosstalk      nitrogen-use efficiency      breeding strategy     
Corresponding Author(s): Xiuhua GAO,Xiangdong FU   
About author:

Tongcan Cui and Yizhe Hou contributed equally to this work.

Just Accepted Date: 15 March 2022   Online First Date: 11 April 2022    Issue Date: 09 September 2022
 Cite this article:   
Hui LIU,Qian LIU,Xiuhua GAO, et al. ROLE OF NITROGEN SENSING AND ITS INTEGRATIVE SIGNALING PATHWAYS IN SHAPING ROOT SYSTEM ARCHITECTURE[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 316-332.
 URL:  
https://academic.hep.com.cn/fase/EN/10.15302/J-FASE-2022441
https://academic.hep.com.cn/fase/EN/Y2022/V9/I3/316
Fig.1  The absorption, transport and assimilation of inorganic nitrogen in Arabidopsis.
Fig.2  Root developmental adaptations to nitrogen availability. (a) The diagrams of the root responses of Arabidopsis plants under different nitrogen levels. (b) Schematic representation of integrative NO3 signaling.
Fig.3  Systemic nitrate signaling and its role in whole-plant responses in Arabidopsis split-root system. (a) Differential responses of primary and lateral roots of Arabidopsis plants under nitrate (NO3) heterogeneous conditions. (b) A simplified model of systemic NO3 signaling in root foraging responses.
Gene name Species Phenotype
OsAMT1;1[138] Rice Enhancing the permeability of NH4+ and improving grain yield under low NH4+ conditions
OsAMT1;3[139] Rice AMT1;3-overexpression lines exhibit C and N metabolic imbalance, resulting in a poor growth and reduced grain yield
OsNRT1.1a[140] Rice Overexpression of OsNRT1.1a enhances N uptake and grain yield with early flowering
OsNRT1.1b[141] Rice The upregulation of OsNRT1.1b enhances NUE and grain yield in rice
OsNRT2.3b[142] Rice Enhancing pH homeostasis, grain yield and NUE
OsNAR2.1[143] Rice Promoting NO3 absorption and transport, and improving drought resistance
OsNR2[144] Rice The upregulation of OsNR2 increases tiller numbers, grain yield and NUE
OsGS1;1[145] Rice Promoting grain filling
OsGS1;2[146] Rice Improving uptake and assimilation of NH4+
OsNLP4[147] Rice Increasing tillering, grain yield and NUE under different N conditions
OsFd-GOGAT[148] Rice Involved in N remobilization during leaf senescence
OsTCP19[149] Rice N-regulated OsTCP19 negatively regulates rice tillering
AlaAT[150] Rice Promoting biomass accumulation, tiller numbers, N content and grain yield
OsMYB305[151] Rice Increasing N assimilation, tiller numbers and shoot dry weight
DEP1[152] Rice N-regulated dep1 allele improves N assimilation, NUE and grain yield
MADS25[153] Rice Increasing primary root length, lateral root number and shoot fresh weight
OsBT1/2[154] Rice Negative regulator of N uptake and utilization
GRF4[5] Rice Integrating and coordinating plant growth, C fixation and N assimilation, reducing N fertilizer use while boosting grain yield without affecting semidwarfism
OsNAP[155] Rice Regulating nutrient uptake capacity and affecting plant senescence
NGR5[156] Rice N-regulated NGR5 enhances tillering, NUE and grain yield in rice
DNR1[157] Rice Involved in auxin biosynthesis, enhancing N metabolism and NUE in rice
TOND1[158] Rice Increasing primary root length, N uptake, shoot dry weight, grain number and yield
OsDRO1[159] Rice Modulating root growth angle, enhancing N uptake and grain yield
TaNAC2-5A[160] Wheat Promoting root branching and NO3 uptake, increasing N harvest index and grain yield
TaNFYA-B1[161] Wheat Promoting root branching and NO3 uptake, Increasing spike number and grain yield
TaGS2-2Ab[162] Wheat Enhancing N uptake and remobilization, grain number, grain weight, and grain yield
TaARE1[163] Wheat Increasing N uptake, grain weight and grain yield under low N conditions
TaTAR2.1[164] Wheat Enhancing lateral root length, spike number and grain yield
Ms44[165] Maize Improving grain yield and NUE
Tab.1  The genes associated with the improvements of yield and NUE in crops
1 H C, Godfray J R, Beddington I R, Crute L, Haddad D, Lawrence J F, Muir J, Pretty S, Robinson S M, Thomas C Toulmin. Food security: the challenge of feeding 9 billion people. Science , 2010, 327( 5967): 812–818
https://doi.org/10.1126/science.1185383 pmid: 20110467
2 P L Pingali. Green revolution: impacts, limits, and the path ahead. Proceedings of the National Academy of Sciences of the United States of America , 2012, 109( 31): 12302–12308
https://doi.org/10.1073/pnas.0912953109 pmid: 22826253
3 W R, Raun G V Johnson. Improving nitrogen use efficiency for cereal production. Agronomy Journal , 1999, 91( 3): 357–363
https://doi.org/10.2134/agronj1999.00021962009100030001x
4 M J, Gooding M, Addisu R K, Uppal J W, Snape H E Jones. Effect of wheat dwarfing genes on nitrogen-use efficiency. Journal of Agricultural Science , 2012, 150( 1): 3–22
https://doi.org/10.1017/S0021859611000414
5 S, Li Y, Tian K, Wu Y, Ye J, Yu J, Zhang Q, Liu M, Hu H, Li Y, Tong N P, Harberd X Fu. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature , 2018, 560( 7720): 595–600
https://doi.org/10.1038/s41586-018-0415-5 pmid: 30111841
6 A, Krapp L C, David C, Chardin T, Girin A, Marmagne A S, Leprince S, Chaillou S, Ferrario-Méry C, Meyer F Daniel-Vedele. Nitrate transport and signalling in Arabidopsis . Journal of Experimental Botany , 2014, 65(3): 789–798
7 S Kant. Understanding nitrate uptake, signaling and remobilisation for improving plant nitrogen use efficiency. Seminars in Cell & Developmental Biology , 2018, 74 : 89–96
https://doi.org/10.1016/j.semcdb.2017.08.034 pmid: 28838687
8 T C Shen. The induction of nitrate reductase and the preferential assimilation of ammonium in germinating rice seedlings. Plant Physiology , 1969, 44( 11): 1650–1655
https://doi.org/10.1104/pp.44.11.1650 pmid: 16657253
9 H M Reisenauer. Mineral nutrients in soil solution. In: Altman P L, Dittmer D S, eds. Bethesda: Federation of American Societies for Experiement Biology , 1966, 507–508
10 R M, Lark A E, Milne T M, Addiscott K W T, Goulding C P, Webster S O’Flaherty. Scale-and location-dependent correlation of nitrous oxide emissions with soil properties: an analysis using wavelets. European Journal of Soil Science , 2004, 55( 3): 611–627
https://doi.org/10.1111/j.1365-2389.2004.00620.x
11 N M, Crawford A D M Glass. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science , 1998, 3( 10): 389–395
https://doi.org/10.1016/S1360-1385(98)01311-9
12 B G Forde. Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta , 2000, 1465( 1−2): 219–235
https://doi.org/10.1016/S0005-2736(00)00140-1 pmid: 10748256
13 A J, Miller X, Fan M, Orsel S J, Smith D M Wells. Nitrate transport and signalling. Journal of Experimental Botany , 2007, 58( 9): 2297–2306
https://doi.org/10.1093/jxb/erm066 pmid: 17519352
14 D T, Britto M Y, Siddiqi A D M, Glass H J Kronzucker. Futile transmembrane NH4+ cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences of the United States of America , 2001, 98( 7): 4255–4258
https://doi.org/10.1073/pnas.061034698 pmid: 11274450
15 A Krapp. Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Current Opinion in Plant Biology , 2015, 25 : 115–122
https://doi.org/10.1016/j.pbi.2015.05.010 pmid: 26037390
16 Y F, Tsay J I, Schroeder K A, Feldmann N M Crawford. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell , 1993, 72( 5): 705–713
https://doi.org/10.1016/0092-8674(93)90399-B pmid: 8453665
17 C H, Ho S H, Lin H C, Hu Y F Tsay. CHL1 functions as a nitrate sensor in plants. Cell , 2009, 138( 6): 1184–1194
https://doi.org/10.1016/j.cell.2009.07.004 pmid: 19766570
18 J L, Parker S Newstead. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature , 2014, 507( 7490): 68–72
https://doi.org/10.1038/nature13116 pmid: 24572366
19 K H, Liu Y F Tsay. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO Journal , 2003, 22( 5): 1005–1013
https://doi.org/10.1093/emboj/cdg118 pmid: 12606566
20 J, Sun J R, Bankston J, Payandeh T R, Hinds W N, Zagotta N Zheng. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature , 2014, 507( 7490): 73–77
https://doi.org/10.1038/nature13074 pmid: 24572362
21 H C, Hu Y Y, Wang Y F Tsay. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant Journal , 2009, 57( 2): 264–278
https://doi.org/10.1111/j.1365-313X.2008.03685.x pmid: 18798873
22 Y F, Tsay C C, Chiu C B, Tsai C H, Ho P K Hsu. Nitrate transporters and peptide transporters. FEBS Letters , 2007, 581( 12): 2290–2300
https://doi.org/10.1016/j.febslet.2007.04.047 pmid: 17481610
23 C S, Chiang G, Stacey Y F Tsay. Mechanisms and functional properties of two peptide transporters, AtPTR2 and fPTR2. Journal of Biological Chemistry , 2004, 279( 29): 30150–30157
https://doi.org/10.1074/jbc.M405192200 pmid: 15138259
24 J J, Zhou F L, Theodoulou I, Muldin B, Ingemarsson A J Miller. Cloning and functional characterization of a Brassica napus transporter that is able to transport nitrate and histidine. Journal of Biological Chemistry , 1998, 273( 20): 12017–12023
https://doi.org/10.1074/jbc.273.20.12017 pmid: 9575142
25 N Y, Komarova K, Thor A, Gubler S, Meier D, Dietrich A, Weichert Grotemeyer M, Suter M, Tegeder D Rentsch. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology , 2008, 148( 2): 856–869
https://doi.org/10.1104/pp.108.123844 pmid: 18753286
26 M, Sugiura M N, Georgescu M Takahashi. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant & Cell Physiology , 2007, 48( 7): 1022–1035
https://doi.org/10.1093/pcp/pcm073 pmid: 17566055
27 H H, Nour-Eldin T G, Andersen M, Burow S R, Madsen M E, Jørgensen C E, Olsen I, Dreyer R, Hedrich D, Geiger B A Halkier. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature , 2012, 488( 7412): 531–534
https://doi.org/10.1038/nature11285 pmid: 22864417
28 G, Krouk B, Lacombe A, Bielach F, Perrine-Walker K, Malinska E, Mounier K, Hoyerova P, Tillard S, Leon K, Ljung E, Zazimalova E, Benkova P, Nacry A Gojon. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell , 2010, 18( 6): 927–937
https://doi.org/10.1016/j.devcel.2010.05.008 pmid: 20627075
29 Y, Kanno A, Hanada Y, Chiba T, Ichikawa M, Nakazawa M, Matsui T, Koshiba Y, Kamiya M Seo. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America , 2012, 109( 24): 9653–9658
https://doi.org/10.1073/pnas.1203567109 pmid: 22645333
30 I, Tal Y, Zhang M E, Jørgensen O, Pisanty I C R, Barbosa M, Zourelidou T, Regnault C, Crocoll Olsen C, Erik R, Weinstain C, Schwechheimer B A, Halkier H H, Nour-Eldin M, Estelle E Shani. The Arabidopsis NPF3 protein is a GA transporter. Nature Communications , 2016, 7( 1): 11486
https://doi.org/10.1038/ncomms11486 pmid: 27139299
31 Angeli A, De D, Monachello G, Ephritikhine J M, Frachisse S, Thomine F, Gambale H Barbier-Brygoo. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature , 2006, 442( 7105): 939–942
https://doi.org/10.1038/nature05013 pmid: 16878138
32 D, Geelen C, Lurin D, Bouchez J M, Frachisse F, Lelièvre B, Courtial H, Barbier-Brygoo C Maurel. Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. Plant Journal , 2000, 21( 3): 259–267
https://doi.org/10.1046/j.1365-313x.2000.00680.x pmid: 10758477
33 T, Maierhofer C, Lind S, Hüttl S, Scherzer M, Papenfuß J, Simon K A S, Al-Rasheid P, Ache H, Rennenberg R, Hedrich T D, Müller D Geiger. A single-pore residue renders the Arabidopsis root anion channel SLAH2 highly nitrate selective. Plant Cell , 2014, 26( 6): 2554–2567
https://doi.org/10.1105/tpc.114.125849 pmid: 24938289
34 N M Crawford. Nitrate: nutrient and signal for plant growth. Plant Cell , 1995, 7( 7): 859–868
pmid: 7640524
35 S, Quaggiotti B, Ruperti P, Borsa T, Destro M Malagoli. Expression of a putative high-affinity NO3– transporter and of an H+-ATPase in relation to whole plant nitrate transport physiology in two maize genotypes differently responsive to low nitrogen availability. Journal of Experimental Botany , 2003, 54( 384): 1023–1031
https://doi.org/10.1093/jxb/erg106 pmid: 12598572
36 J A, O’Brien A, Vega E, Bouguyon G, Krouk A, Gojon G, Coruzzi R A Gutiérrez. Nitrate transport, sensing, and responses in plants. Molecular Plant , 2016, 9( 6): 837–856
https://doi.org/10.1016/j.molp.2016.05.004 pmid: 27212387
37 A, Iqbal D, Qiang M, Alamzeb W, Xiangru G, Huiping Z, Hengheng P, Nianchang Z, Xiling S Meizhen. Untangling the molecular mechanisms and functions of nitrate to improve nitrogen use efficiency. Journal of the Science of Food and Agriculture , 2020, 100( 3): 904–914
https://doi.org/10.1002/jsfa.10085 pmid: 31612486
38 N C, Huang K H, Liu H J, Lo Y F Tsay. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell , 1999, 11( 8): 1381–1392
https://doi.org/10.1105/tpc.11.8.1381 pmid: 10449574
39 G, Vert J Chory. A toggle switch in plant nitrate uptake. Cell , 2009, 138( 6): 1064–1066
https://doi.org/10.1016/j.cell.2009.09.005 pmid: 19766561
40 W, Li Y, Wang M, Okamoto N M, Crawford M Y, Siddiqi A D M Glass. Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiology , 2007, 143( 1): 425–433
https://doi.org/10.1104/pp.106.091223 pmid: 17085507
41 T, Kiba A B, Feria-Bourrellier F, Lafouge L, Lezhneva S, Boutet-Mercey M, Orsel V, Bréhaut A, Miller F, Daniel-Vedele H, Sakakibara A Krapp. The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell , 2012, 24( 1): 245–258
https://doi.org/10.1105/tpc.111.092221 pmid: 22227893
42 Z, Kotur N, Mackenzie S, Ramesh S D, Tyerman B N, Kaiser A D M Glass. Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytologist , 2012, 194( 3): 724–731
https://doi.org/10.1111/j.1469-8137.2012.04094.x pmid: 22432443
43 M, Okamoto A, Kumar W, Li Y, Wang M Y, Siddiqi N M, Crawford A D M Glass. High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1 . Plant Physiology , 2006, 140(3): 1036–1046
44 W, Xuan T, Beeckman G Xu. Plant nitrogen nutrition: sensing and signaling. Current Opinion in Plant Biology , 2017, 39 : 57–65
https://doi.org/10.1016/j.pbi.2017.05.010 pmid: 28614749
45 S H, Lin H F, Kuo G, Canivenc C S, Lin M, Lepetit P K, Hsu P, Tillard H L, Lin Y Y, Wang C B, Tsai A, Gojon Y F Tsay. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell , 2008, 20( 9): 2514–2528
https://doi.org/10.1105/tpc.108.060244 pmid: 18780802
46 J Y, Li Y L, Fu S M, Pike J, Bao W, Tian Y, Zhang C Z, Chen Y, Zhang H M, Li J, Huang L G, Li J I, Schroeder W, Gassmann J M Gong. The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell , 2010, 22( 5): 1633–1646
https://doi.org/10.1105/tpc.110.075242 pmid: 20501909
47 Y Y, Wang Y F Tsay. Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell , 2011, 23( 5): 1945–1957
https://doi.org/10.1105/tpc.111.083618 pmid: 21571952
48 C, Taochy I, Gaillard E, Ipotesi R, Oomen N, Leonhardt S, Zimmermann J B, Peltier W, Szponarski T, Simonneau H, Sentenac R, Gibrat J C Boyer. The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress. Plant Journal , 2015, 83( 3): 466–479
https://doi.org/10.1111/tpj.12901 pmid: 26058834
49 C, Segonzac J C, Boyer E, Ipotesi W, Szponarski P, Tillard B, Touraine N, Sommerer M, Rossignol R Gibrat. Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell , 2007, 19( 11): 3760–3777
https://doi.org/10.1105/tpc.106.048173 pmid: 17993627
50 P K, Hsu Y F Tsay. Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiology , 2013, 163( 2): 844–856
https://doi.org/10.1104/pp.113.226563 pmid: 24006285
51 S C, Fan C S, Lin P K, Hsu S H, Lin Y F Tsay. The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell , 2009, 21( 9): 2750–2761
https://doi.org/10.1105/tpc.109.067603 pmid: 19734434
52 M, Okamoto J J, Vidmar A D M Glass. Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant & Cell Physiology , 2003, 44( 3): 304–317
https://doi.org/10.1093/pcp/pcg036 pmid: 12668777
53 M, Tegeder C Masclaux-Daubresse. Source and sink mechanisms of nitrogen transport and use. New Phytologist , 2018, 217( 1): 35–53
https://doi.org/10.1111/nph.14876 pmid: 29120059
54 A, Almagro S H, Lin Y F Tsay. Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell , 2008, 20( 12): 3289–3299
https://doi.org/10.1105/tpc.107.056788 pmid: 19050168
55 F, Chopin M, Orsel M F, Dorbe F, Chardon H N, Truong A J, Miller A, Krapp F Daniel-Vedele. The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell , 2007, 19( 5): 1590–1602
https://doi.org/10.1105/tpc.107.050542 pmid: 17540716
56 S, Léran B, Garg Y, Boursiac C, Corratgé-Faillie C, Brachet P, Tillard A, Gojon B Lacombe. AtNPF5.5, a nitrate transporter affecting nitrogen accumulation in Arabidopsis embryo. Scientific Reports , 2015, 5( 1): 7962
https://doi.org/10.1038/srep07962 pmid: 25608465
57 M Y, Wang M Y, Siddiqi T J, Ruth A Glass. Ammonium uptake by rice roots (II. Kinetics of 15NH4+ influx across the plasmalemma). Plant Physiology , 1993, 103( 4): 1259–1267
https://doi.org/10.1104/pp.103.4.1259 pmid: 12232018
58 M, Cerezo P, Tillard A, Gojon E, Primo-Millo P García-Agustín. Characterization and regulation of ammonium transport systems in Citrus plants. Planta , 2001, 214( 1): 97–105
https://doi.org/10.1007/s004250100590 pmid: 11762176
59 U, Ludewig Wirén N, von D, Rentsch W B Frommer. Rhesus factors and ammonium: a function in efflux. Genome Biology , 2001, 2( 3): reviews1010
60 D, Loqué L, Yuan S, Kojima A, Gojon J, Wirth S, Gazzarrini K, Ishiyama H, Takahashi Wirén N von. Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant Journal , 2006, 48( 4): 522–534
https://doi.org/10.1111/j.1365-313X.2006.02887.x pmid: 17026539
61 D, Loqué S, Lalonde L L, Looger Wirén N, von W B Frommer. A cytosolic trans-activation domain essential for ammonium uptake. Nature , 2007, 446( 7132): 195–198
https://doi.org/10.1038/nature05579 pmid: 17293878
62 V, Lanquar D, Loqué F, Hörmann L, Yuan A, Bohner W R, Engelsberger S, Lalonde W X, Schulze Wirén N, von W B Frommer. Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis . Plant Cell , 2009, 21(11): 3610–3622
63 W, Wang A, Li Z, Zhang C Chu. Posttranslational modifications: regulation of nitrogen utilization and signaling. Plant & Cell Physiology , 2021, 62( 4): 543–552
https://doi.org/10.1093/pcp/pcab008 pmid: 33493288
64 C, Sohlenkamp C C, Wood G W, Roeb M K Udvardi. Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiology , 2002, 130( 4): 1788–1796
https://doi.org/10.1104/pp.008599 pmid: 12481062
65 P, Goel A K Singh. Abiotic stresses downregulate key genes involved in nitrogen uptake and assimilation in Brassica juncea L. PLoS One , 2015, 10( 11): e0143645
https://doi.org/10.1371/journal.pone.0143645 pmid: 26605918
66 G, Xu X, Fan A J Miller. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology , 2012, 63( 1): 153–182
https://doi.org/10.1146/annurev-arplant-042811-105532 pmid: 22224450
67 P J, Lea B J Miflin. Alternative route for nitrogen assimilation in higher plants. Nature , 1974, 251( 5476): 614–616
https://doi.org/10.1038/251614a0 pmid: 4423889
68 C, Meyer M Stitt. Nitrate reduction and signalling. In: Lea P J, Morot-Gaudry J F, eds. Plant Nitrogen. Springer , 2001, 37–59
69 J Q, Wilkinson N M Crawford. Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2 . Molecular & General Genetics , 1993, 239(1–2): 289–297
70 H, Unno T, Uchida H, Sugawara G, Kurisu T, Sugiyama T, Yamaya H, Sakakibara T, Hase M Kusunoki. Atomic structure of plant glutamine synthetase: a key enzyme for plant productivity. Journal of Biological Chemistry , 2006, 281( 39): 29287–29296
https://doi.org/10.1074/jbc.M601497200 pmid: 16829528
71 S M, Swarbreck M, Defoin-Platel M, Hindle M, Saqi D Z Habash. New perspectives on glutamine synthetase in grasses. Journal of Experimental Botany , 2011, 62( 4): 1511–1522
https://doi.org/10.1093/jxb/erq356 pmid: 21172814
72 R M, Wallsgrove J C, Turner N P, Hall A C, Kendall S W Bright. Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiology , 1987, 83( 1): 155–158
https://doi.org/10.1104/pp.83.1.155 pmid: 16665193
73 P J, Lea S A, Robinson G R Stewart. The enzymology and metabolism of glutamine, glutamate, and asparagine. In: Miflin B J, Lea P J, eds. Biochemistry of Plants, Intermediary Nitrogen Metabolism. Academic Press , 1990, 16 : 121–159
74 S J, Temple C P, Vance Gantt J Stephen. Glutamate synthase and nitrogen assimilation. Trends in Plant Science , 1998, 3( 2): 51–56
https://doi.org/10.1016/S1360-1385(97)01159-X
75 F L, Chen J V Cullimore. Two isoenzymes of NADH-dependent glutamate synthase in root nodules of Phaseolus vulgaris L.: purification, properties and activity changes during nodule development. Plant Physiology , 1988, 88( 4): 1411–1417
https://doi.org/10.1104/pp.88.4.1411 pmid: 16666475
76 M, García-Calderón C M, Pérez-Delgado A, Credali J M, Vega M, Betti A J Márquez. Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration. BMC Genomics , 2017, 18( 1): 781
https://doi.org/10.1186/s12864-017-4200-x pmid: 29025409
77 H K, Wong H K, Chan G M, Coruzzi H M Lam. Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis . Plant Physiology , 2004, 134(1): 332–338
78 H M, Lam P, Wong H K, Chan K M, Yam L, Chen C M, Chow G M Coruzzi. Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis . Plant Physiology , 2003, 132(2): 926–935
79 Y L, Jiang X P, Wang H, Sun S J, Han W F, Li N, Cui G M, Lin J Y, Zhang W, Cheng D D, Cao Z Y, Zhang C C, Zhang Y, Chen C Z Zhou. Coordinating carbon and nitrogen metabolic signaling through the cyanobacterial global repressor NdhR. Proceedings of the National Academy of Sciences of the United States of America , 2018, 115( 2): 403–408
https://doi.org/10.1073/pnas.1716062115 pmid: 29279392
80 B D, Gruber R F H, Giehl S, Friedel Wirén N von. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology , 2013, 163( 1): 161–179
https://doi.org/10.1104/pp.113.218453 pmid: 23852440
81 J E Malamy. Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell & Environment , 2005, 28( 1): 67–77
https://doi.org/10.1111/j.1365-3040.2005.01306.x pmid: 16021787
82 E, Mounier M, Pervent K, Ljung A, Gojon P Nacry. Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant, Cell & Environment , 2014, 37( 1): 162–174
https://doi.org/10.1111/pce.12143 pmid: 23731054
83 T, Kiba A Krapp. Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant & Cell Physiology , 2016, 57( 4): 707–714
https://doi.org/10.1093/pcp/pcw052 pmid: 27025887
84 M D, Boer Teixeira J, Santos Tusscher K H Ten. Modeling of root nitrate responses suggests preferential foraging arises from the integration of demand, supply and local presence signals. Frontiers in Plant Science , 2020, 11 : 708
https://doi.org/10.3389/fpls.2020.00708 pmid: 32536935
85 R F H, Giehl Wirén N von. Root nutrient foraging. Plant Physiology , 2014, 166( 2): 509–517
https://doi.org/10.1104/pp.114.245225 pmid: 25082891
86 M C, Drew L R Saker. Nutrient supply and the growth of the seminal root system in barley: II. Localized, compensatory increases in lateral root growth and rates op nitrate uptake when nitrate supply is restricted to only part of the root system. Journal of Experimental Botany , 1975, 26( 1): 79–90
https://doi.org/10.1093/jxb/26.1.79
87 B I, Linkohr L C, Williamson A H, Fitter H M O Leyser. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis . Plant Journal , 2002, 29(6): 751–760
88 W J, Sutherland R A Stillman. The foraging tactics of plants. Oikos , 1988, 52( 3): 239–244
https://doi.org/10.2307/3565196
89 H, Zhang A, Jennings P W, Barlow B G Forde. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America , 1999, 96( 11): 6529–6534
https://doi.org/10.1073/pnas.96.11.6529 pmid: 10339622
90 Q, Tian F, Chen J, Liu F, Zhang G Mi. Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. Journal of Plant Physiology , 2008, 165( 9): 942–951
https://doi.org/10.1016/j.jplph.2007.02.011 pmid: 17928098
91 Y, Tao J L, Ferrer K, Ljung F, Pojer F, Hong J A, Long L, Li J E, Moreno M E, Bowman L J, Ivans Y, Cheng J, Lim Y, Zhao C L, Ballaré G, Sandberg J P, Noel J Chory. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell , 2008, 133( 1): 164–176
https://doi.org/10.1016/j.cell.2008.01.049 pmid: 18394996
92 Y Zhao. Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Molecular Plant , 2012, 5( 2): 334–338
https://doi.org/10.1093/mp/ssr104 pmid: 22155950
93 W, Ma J, Li B, Qu X, He X, Zhao B, Li X, Fu Y Tong. Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis . Plant Journal , 2014, 78(1): 70–79
94 L H, Yu Z Q, Miao G F, Qi J, Wu X T, Cai J L, Mao C B Xiang. MADS-box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals. Molecular Plant , 2014, 7( 11): 1653–1669
https://doi.org/10.1093/mp/ssu088 pmid: 25122697
95 C, Luschnig R A, Gaxiola P, Grisafi G R Fink. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana . Genes & Development , 1998, 12(14): 2175–2187
96 A, Martinière I, Lavagi G, Nageswaran D J, Rolfe L, Maneta-Peyret D T, Luu S W, Botchway S E D, Webb S, Mongrand C, Maurel M L, Martin-Fernandez J, Kleine-Vehn J, Friml P, Moreau J Runions. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proceedings of the National Academy of Sciences of the United States of America , 2012, 109( 31): 12805–12810
https://doi.org/10.1073/pnas.1202040109 pmid: 22689944
97 I, Blilou J, Xu M, Wildwater V, Willemsen I, Paponov J, Friml R, Heidstra M, Aida K, Palme B Scheres. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature , 2005, 433( 7021): 39–44
https://doi.org/10.1038/nature03184 pmid: 15635403
98 K, Ötvös M, Marconi A, Vega J, O’Brien A, Johnson R, Abualia L, Antonielli J C, Montesinos Y, Zhang S, Tan C, Cuesta C, Artner E, Bouguyon A, Gojon J, Friml R A, Gutiérrez K, Wabnik E Benková. Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO Journal , 2021, 40( 3): e106862
https://doi.org/10.15252/embj.2020106862 pmid: 33399250
99 S, Huang S, Chen Z, Liang C, Zhang M, Yan J, Chen G, Xu X, Fan Y Zhang. Knockdown of the partner protein OsNAR2.1 for high-affinity nitrate transport represses lateral root formation in a nitrate-dependent manner. Scientific Reports , 2015, 5( 1): 18192
https://doi.org/10.1038/srep18192 pmid: 26644084
100 Z, Jia R F H, Giehl R C, Meyer T, Altmann Wirén N von. Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen. Nature Communications , 2019, 10( 1): 2378
https://doi.org/10.1038/s41467-019-10331-9 pmid: 31147541
101 Z, Jia R F H, Giehl Wirén N von. Local auxin biosynthesis acts downstream of brassinosteroids to trigger root foraging for nitrogen. Nature Communications , 2021, 12( 1): 5437
https://doi.org/10.1038/s41467-021-25250-x pmid: 34521826
102 Z, Jia R F H, Giehl Wirén N von. The root foraging response under low nitrogen depends on DWARF1-mediated brassinosteroid biosynthesis. Plant Physiology , 2020, 183( 3): 998–1010
https://doi.org/10.1104/pp.20.00440 pmid: 32398320
103 J, Chaiwanon Z Y Wang. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Current Biology , 2015, 25( 8): 1031–1042
https://doi.org/10.1016/j.cub.2015.02.046 pmid: 25866388
104 Y, Fridman L, Elkouby N, Holland K, Vragović R, Elbaum S Savaldi-Goldstein. Root growth is modulated by differential hormonal sensitivity in neighboring cells. Genes & Development , 2014, 28( 8): 912–920
https://doi.org/10.1101/gad.239335.114 pmid: 24736847
105 L, Camut B, Gallova L, Jilli M, Sirlin-Josserand E, Carrera L, Sakvarelidze-Achard S, Ruffel G, Krouk S G, Thomas P, Hedden A L, Phillips J M, Davière P Achard. Nitrate signaling promotes plant growth by upregulating gibberellin biosynthesis and destabilization of DELLA proteins. Current Biology , 2021, 31( 22): 4971–4982.e4
https://doi.org/10.1016/j.cub.2021.09.024 pmid: 34614391
106 A, Lokdarshi W C, Conner C, McClintock T, Li D M Roberts. Arabidopsis CML38, a calcium sensor that localizes to ribonucleoprotein complexes under hypoxia stress. Plant Physiology , 2016, 170( 2): 1046–1059
https://doi.org/10.1104/pp.15.01407 pmid: 26634999
107 X, Song J, Li M, Lyu X, Kong S, Hu Q, Song K Zuo. CALMODULIN-LIKE-38 and PEP1 RECEPTOR 2 integrate nitrate and brassinosteroid signals to regulate root growth. Plant Physiology , 2021, 187( 3): 1779–1794
https://doi.org/10.1093/plphys/kiab323 pmid: 34618046
108 J M, Alvarez E, Riveras E A, Vidal D E, Gras O, Contreras-López K P, Tamayo F, Aceituno I, Gómez S, Ruffel L, Lejay X, Jordana R A Gutiérrez. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant Journal , 2014, 80( 1): 1–13
https://doi.org/10.1111/tpj.12618 pmid: 25039575
109 K H, Liu C Y, Huang Y F Tsay. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell , 1999, 11( 5): 865–874
https://doi.org/10.1105/tpc.11.5.865 pmid: 10330471
110 E A, Vidal T C, Moyano E, Riveras O, Contreras-López R A Gutiérrez. Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proceedings of the National Academy of Sciences of the United States of America , 2013, 110( 31): 12840–12845
https://doi.org/10.1073/pnas.1310937110 pmid: 23847199
111 E A, Vidal J M, Álvarez R A Gutiérrez. Nitrate regulation of AFB3 and NAC4 gene expression in Arabidopsis roots depends on NRT1.1 nitrate transport function. Plant Signaling & Behavior , 2014, 9( 3): e28501
https://doi.org/10.4161/psb.28501 pmid: 24642706
112 J M, Harris C A Ondzighi-Assoume. Environmental nitrate signals through abscisic acid in the root tip. Plant Signaling & Behavior , 2017, 12( 1): e1273303
https://doi.org/10.1080/15592324.2016.1273303 pmid: 28067583
113 L, Signora Smet I, De C H, Foyer H Zhang. ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis . Plant Journal , 2001, 28(6): 655–662
114 S, Léran K H, Edel M, Pervent K, Hashimoto C, Corratgé-Faillie J N, Offenborn P, Tillard A, Gojon J, Kudla B Lacombe. Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Science Signaling , 2015, 8( 375): ra43
https://doi.org/10.1126/scisignal.aaa4829 pmid: 25943353
115 J Y, Jung R, Shin D P Schachtman. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis . Plant Cell , 2009, 21(2): 607–621
116 Q Y, Tian P, Sun W H Zhang. Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana . New Phytologist , 2009, 184(4): 918–931
117 H, Zhang B G Forde. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science , 1998, 279( 5349): 407–409
https://doi.org/10.1126/science.279.5349.407 pmid: 9430595
118 A, Medici G Krouk. The primary nitrate response: a multifaceted signalling pathway. Journal of Experimental Botany , 2014, 65( 19): 5567–5576
https://doi.org/10.1093/jxb/eru245 pmid: 24942915
119 K H, Liu A, Diener Z, Lin C, Liu J Sheen. Primary nitrate responses mediated by calcium signalling and diverse protein phosphorylation. Journal of Experimental Botany , 2020, 71( 15): 4428–4441
https://doi.org/10.1093/jxb/eraa047 pmid: 31985788
120 S F, Undurraga C, Ibarra-Henríquez I, Fredes J M, Álvarez R A Gutiérrez. Nitrate signaling and early responses in Arabidopsis roots. Journal of Experimental Botany , 2017, 68( 10): 2541–2551
https://doi.org/10.1093/jxb/erx041 pmid: 28369507
121 C, Marchive F, Roudier L, Castaings V, Bréhaut E, Blondet V, Colot C, Meyer A Krapp. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications , 2013, 4( 1): 1713
https://doi.org/10.1038/ncomms2650 pmid: 23591880
122 K H, Liu Y, Niu M, Konishi Y, Wu H, Du Chung H, Sun L, Li M, Boudsocq M, McCormack S, Maekawa T, Ishida C, Zhang K, Shokat S, Yanagisawa J Sheen. Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature , 2017, 545( 7654): 311–316
https://doi.org/10.1038/nature22077 pmid: 28489820
123 L, Liu H, Gao S, Li Z, Han B Li. Calcium signaling networks mediate nitrate sensing and responses in Arabidopsis . Plant Signaling & Behavior , 2021, 16(10): 1938441
124 X, Wang C, Feng L, Tian C, Hou W, Tian B, Hu Q, Zhang Z, Ren Q, Niu J, Song D, Kong L, Liu Y, He L, Ma C, Chu S, Luan L Li. A transceptor-channel complex couples nitrate sensing to calcium signaling in Arabidopsis . Molecular Plant , 2021, 14(5): 774–786
125 S, Ruffel G, Krouk D, Ristova D, Shasha K D, Birnbaum G M Coruzzi. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proceeding of the National Academy of Sciences of the United States of America , 2011, 108( 45): 18524–18529
126 P, Guan R, Wang P, Nacry G, Breton S A, Kay J L, Pruneda-Paz A, Davani N M Crawford. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proceedings of the National Academy of Sciences of the United States of America , 2014, 111( 42): 15267–15272
https://doi.org/10.1073/pnas.1411375111 pmid: 25288754
127 T, Remans P, Nacry M, Pervent S, Filleur E, Diatloff E, Mounier P, Tillard B G, Forde A Gojon. The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences of the United States of America , 2006, 103( 50): 19206–19211
https://doi.org/10.1073/pnas.0605275103 pmid: 17148611
128 P, Guan J J, Ripoll R, Wang L, Vuong L J, Bailey-Steinitz D, Ye N M Crawford. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proceedings of the National Academy of Sciences of the United States of America , 2017, 114( 9): 2419–2424
https://doi.org/10.1073/pnas.1615676114 pmid: 28202720
129 X, Chen Q, Yao X, Gao C, Jiang N P, Harberd X Fu. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Current Biology , 2016, 26( 5): 640–646
https://doi.org/10.1016/j.cub.2015.12.066 pmid: 26877080
130 T, Araya M, Miyamoto J, Wibowo A, Suzuki S, Kojima Y N, Tsuchiya S, Sawa H, Fukuda Wirén N, von H Takahashi. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proceedings of the National Academy of Sciences of the United States of America , 2014, 111( 5): 2029–2034
https://doi.org/10.1073/pnas.1319953111 pmid: 24449877
131 W, Dong Y, Wang H Takahashi. CLE-CLAVATA1 signaling pathway modulates lateral root development under sulfur deficiency. Plants , 2019, 8( 4): 103
https://doi.org/10.3390/plants8040103 pmid: 31003469
132 T, Araya Wirén N, von H Takahashi. CLE peptides regulate lateral root development in response to nitrogen nutritional status of plants. Plant Signaling & Behavior , 2014, 9( 7): e29302
https://doi.org/10.4161/psb.29302 pmid: 25763500
133 R, Tabata K, Sumida T, Yoshii K, Ohyama H, Shinohara Y Matsubayashi. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science , 2014, 346( 6207): 343–346
https://doi.org/10.1126/science.1257800 pmid: 25324386
134 Y, Ohkubo M, Tanaka R, Tabata M, Ogawa-Ohnishi Y Matsubayashi. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants , 2017, 3( 4): 17029
https://doi.org/10.1038/nplants.2017.29 pmid: 28319056
135 R, Ota Y, Ohkubo Y, Yamashita M, Ogawa-Ohnishi Y Matsubayashi. Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis . Nature Communications , 2020, 11(1): 641
136 M, Taleski N, Imin M A Djordjevic. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. Journal of Experimental Botany , 2018, 69( 8): 1829–1836
https://doi.org/10.1093/jxb/ery037 pmid: 29579226
137 X, Han K, Wu X, Fu Q Liu. Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture. aBIOTECH , 2020, 1 : 1–21
138 K, Ranathunge A, El-Kereamy S, Gidda Y M, Bi S J Rothstein. AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. Journal of Experimental Botany , 2014, 65( 4): 965–979
https://doi.org/10.1093/jxb/ert458 pmid: 24420570
139 A, Bao Z, Liang Z, Zhao H Cai. Overexpressing of OsAMT1-3, a high affinity ammonium transporter gene, modifies rice growth and carbon-nitrogen metabolic status. International Journal of Molecular Sciences , 2015, 16( 5): 9037–9063
https://doi.org/10.3390/ijms16059037 pmid: 25915023
140 W, Wang B, Hu D, Yuan Y, Liu R, Che Y, Hu S, Ou Y, Liu Z, Zhang H, Wang H, Li Z, Jiang Z, Zhang X, Gao Y, Qiu X, Meng Y, Liu Y, Bai Y, Liang Y, Wang L, Zhang L, Li , Sodmergen H, Jing J, Li C Chu. Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. Plant Cell , 2018, 30( 3): 638–651
https://doi.org/10.1105/tpc.17.00809 pmid: 29475937
141 X, Fan H, Feng Y, Tan Y, Xu Q, Miao G Xu. A putative 6-transmembrane nitrate transporter OsNRT1.1b plays a key role in rice under low nitrogen. Journal of Integrative Plant Biology , 2016, 58( 6): 590–599
https://doi.org/10.1111/jipb.12382 pmid: 26220694
142 X, Fan Z, Tang Y, Tan Y, Zhang B, Luo M, Yang X, Lian Q, Shen A J, Miller G Xu. Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proceedings of the National Academy of Sciences of the United States of America , 2016, 113( 26): 7118–7123
https://doi.org/10.1073/pnas.1525184113 pmid: 27274069
143 J, Chen X, Liu S, Liu X, Fan L, Zhao M, Song X, Fan G Xu. Co-overexpression of OsNAR2.1 and OsNRT2.3a increased agronomic nitrogen use efficiency in transgenic rice plants. Frontiers in Plant Science , 2020, 11 : 1245
https://doi.org/10.3389/fpls.2020.01245 pmid: 32903417
144 Z, Gao Y, Wang G, Chen A, Zhang S, Yang L, Shang D, Wang B, Ruan C, Liu H, Jiang G, Dong L, Zhu J, Hu G, Zhang D, Zeng L, Guo G, Xu S, Teng N P, Harberd Q Qian. The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nature Communications , 2019, 10( 1): 5207
https://doi.org/10.1038/s41467-019-13110-8 pmid: 31729387
145 M, Tabuchi K, Sugiyama K, Ishiyama E, Inoue T, Sato H, Takahashi T Yamaya. Severe reduction in growth rate and grain filling of rice mutants lacking OsGS1;1, a cytosolic glutamine synthetase1;1. Plant Journal , 2005, 42( 5): 641–651
https://doi.org/10.1111/j.1365-313X.2005.02406.x pmid: 15918879
146 K, Funayama S, Kojima M, Tabuchi-Kobayashi Y, Sawa Y, Nakayama T, Hayakawa T Yamaya. Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant & Cell Physiology , 2013, 54( 6): 934–943
https://doi.org/10.1093/pcp/pct046 pmid: 23509111
147 M, Wang T, Hasegawa M, Beier M, Hayashi Y, Ohmori K, Yano S, Teramoto T, Kamiya T Fujiwara. Growth and nitrate reductase activity are impaired in rice osnlp4 mutants supplied with nitrate. Plant & Cell Physiology , 2021, 62( 7): 1156–1167
https://doi.org/10.1093/pcp/pcab035 pmid: 33693871
148 D D, Zeng R, Qin M, Li M, Alamin X L, Jin Y, Liu C H Shi. The ferredoxin-dependent glutamate synthase (OsFd-GOGAT) participates in leaf senescence and the nitrogen remobilization in rice. Molecular Genetics and Genomics , 2017, 292( 2): 385–395
https://doi.org/10.1007/s00438-016-1275-z pmid: 28012016
149 Y, Liu H, Wang Z, Jiang W, Wang R, Xu Q, Wang Z, Zhang A, Li Y, Liang S, Ou X, Liu S, Cao H, Tong Y, Wang F, Zhou H, Liao B, Hu C Chu. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature , 2021, 590( 7847): 600–605
https://doi.org/10.1038/s41586-020-03091-w pmid: 33408412
150 A, Sisharmini A, Apriana N, Khumaida K R, Trijatmiko B S Purwoko. Expression of a cucumber alanine aminotransferase2 gene improves nitrogen use efficiency in transgenic rice. Journal of Genetic Engineering and Biotechnology , 2019, 17( 1): 9
https://doi.org/10.1186/s43141-019-0010-7 pmid: 31712914
151 D, Wang T, Xu Z, Yin W, Wu H, Geng L, Li M, Yang H, Cai X Lian. Overexpression of OsMYB305 in rice enhances the nitrogen uptake under low-nitrogen condition. Frontiers in Plant Science , 2020, 11 : 369
https://doi.org/10.3389/fpls.2020.00369 pmid: 32351516
152 H, Sun Q, Qian K, Wu J, Luo S, Wang C, Zhang Y, Ma Q, Liu X, Huang Q, Yuan R, Han M, Zhao G, Dong L, Guo X, Zhu Z, Gou W, Wang Y, Wu H, Lin X Fu. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nature Genetics , 2014, 46( 6): 652–656
https://doi.org/10.1038/ng.2958 pmid: 24777451
153 C, Yu Y, Liu A, Zhang S, Su A, Yan L, Huang I, Ali Y, Liu B G, Forde Y Gan. MADS-box transcription factor OsMADS25 regulates root development through affection of nitrate accumulation in rice. PLoS One , 2015, 10( 8): e0135196
https://doi.org/10.1371/journal.pone.0135196 pmid: 26258667
154 V, Araus E A, Vidal T, Puelma S, Alamos D, Mieulet E, Guiderdoni R A Gutiérrez. Members of BTB gene family of scaffold proteins suppress nitrate uptake and nitrogen use efficiency. Plant Physiology , 2016, 171( 2): 1523–1532
pmid: 27208309
155 C, Liang Y, Wang Y, Zhu J, Tang B, Hu L, Liu S, Ou H, Wu X, Sun J, Chu C Chu. OsNAP connects abscisic acid and leaf senescence by fine-tuning abscisic acid biosynthesis and directly targeting senescence-associated genes in rice. Proceedings of the National Academy of Sciences of the United States of America , 2014, 111( 27): 10013–10018
https://doi.org/10.1073/pnas.1321568111 pmid: 24951508
156 K, Wu S, Wang W, Song J, Zhang Y, Wang Q, Liu J, Yu Y, Ye S, Li J, Chen Y, Zhao J, Wang X, Wu M, Wang Y, Zhang B, Liu Y, Wu N P, Harberd X Fu. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science , 2020, 367( 6478): eaaz2046
https://doi.org/10.1126/science.aaz2046 pmid: 32029600
157 S, Zhang L, Zhu C, Shen Z, Ji H, Zhang T, Zhang Y, Li J, Yu N, Yang Y, He Y, Tian K, Wu J, Wu N P, Harberd Y, Zhao X, Fu S, Wang S Li. Natural allelic variation in a modulator of auxin homeostasis improves grain yield and nitrogen use efficiency in rice. Plant Cell , 2021, 33( 3): 566–580
https://doi.org/10.1093/plcell/koaa037 pmid: 33955496
158 Y, Zhang L, Tan Z, Zhu L, Yuan D, Xie C Sun. TOND1 confers tolerance to nitrogen deficiency in rice. Plant Journal , 2015, 81( 3): 367–376
https://doi.org/10.1111/tpj.12736 pmid: 25439309
159 Y, Arai-Sanoh T, Takai S, Yoshinaga H, Nakano M, Kojima H, Sakakibara M, Kondo Y Uga. Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Scientific Reports , 2014, 4( 1): 5563
https://doi.org/10.1038/srep05563 pmid: 24988911
160 X, He B, Qu W, Li X, Zhao W, Teng W, Ma Y, Ren B, Li Z, Li Y Tong. The nitrate-inducible NAC transcription factor TaNAC2–5A controls nitrate response and increases wheat yield. Plant Physiology , 2015, 169( 3): 1991–2005
https://doi.org/10.1104/pp.15.00568 pmid: 26371233
161 B, Qu X, He J, Wang Y, Zhao W, Teng A, Shao X, Zhao W, Ma J, Wang B, Li Z, Li Y Tong. A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiology , 2015, 167( 2): 411–423
https://doi.org/10.1104/pp.114.246959 pmid: 25489021
162 M, Hu X, Zhao Q, Liu X, Hong W, Zhang Y, Zhang L, Sun H, Li Y Tong. Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnology Journal , 2018, 16( 11): 1858–1867
https://doi.org/10.1111/pbi.12921 pmid: 29577547
163 M, Guo Q, Wang Y, Zong J, Nian H, Li J, Li T, Wang C, Gao J Zuo. Genetic manipulations of TaARE1 boost nitrogen utilization and grain yield in wheat. Journal of Genetics and Genomics , 2021, 48( 10): 950–953
https://doi.org/10.1016/j.jgg.2021.07.003 pmid: 34373219
164 A, Shao W, Ma X, Zhao M, Hu X, He W, Teng H, Li Y Tong. The auxin biosynthetic TRYPTOPHAN AMINOTRANSFERASE RELATED TaTAR2.1–3A increases grain yield of wheat. Plant Physiology , 2017, 174( 4): 2274–2288
https://doi.org/10.1104/pp.17.00094 pmid: 28626005
165 T, Fox J, DeBruin Collet K, Haug M, Trimnell J, Clapp A, Leonard B, Li E, Scolaro S, Collinson K, Glassman M, Miller J, Schussler D, Dolan L, Liu C, Gho M, Albertsen D, Loussaert B Shen. A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnology Journal , 2017, 15( 8): 942–952
https://doi.org/10.1111/pbi.12689 pmid: 28055137
166 X, Huang Q, Qian Z, Liu H, Sun S, He D, Luo G, Xia C, Chu J, Li X Fu. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics , 2009, 41( 4): 494–497
https://doi.org/10.1038/ng.352 pmid: 19305410
167 K, Wu H, Xu X, Gao X Fu. New insights into gibberellin signaling in regulating plant growth-metabolic coordination. Current Opinion in Plant Biology , 2021, 63 : 102074
https://doi.org/10.1016/j.pbi.2021.102074 pmid: 34217918
[1] Tom MISSELBROOK, Zhaohai BAI, Zejiang CAI, Weidong CAO, Alison CARSWELL, Nicholas COWAN, Zhenling CUI, David CHADWICK, Bridget EMMETT, Keith GOULDING, Rui JIANG, Davey JONES, Xiaotang JU, Hongbin LIU, Yuelai LU, Lin MA, David POWLSON, Robert M. REES, Ute SKIBA, Pete SMITH, Roger SYLVESTER-BRADLEY, John WILLIAMS, Lianhai WU, Minggang XU, Wen XU, Fusuo ZHANG, Junling ZHANG, Jianbin ZHOU, Xuejun LIU. PROGRESS ON IMPROVING AGRICULTURAL NITROGEN USE EFFICIENCY: UK-CHINA VIRTUAL JOINT CENTERS ON NITROGEN AGRONOM[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 475-489.
[2] Chaopu TI, Xiaoyuan YAN, Longlong XIA, Jingwen HUANG. IMPROVING NITROGEN SAFETY IN CHINA: NITROGEN FLOWS, POLLUTION AND CONTROL[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 465-474.
[3] Peter M. VITOUSEK, Xinping CHEN, Zhenling CUI, Xuejun LIU, Pamela A. MATSON, Ivan ORTIZ-MONASTERIO, G. Philip ROBERTSON, Fusuo ZHANG. CLIMATE-CHANGE-INDUCED TEMPORAL VARIATION IN PRECIPITATION INCREASES NITROGEN LOSSES FROM INTENSIVE CROPPING SYSTEMS: ANALYSIS WITH A TOY MODEL[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 457-464.
[4] Enzai DU, Nan XIA, Yuying GUO, Yuehan TIAN, Binghe LI, Xuejun LIU, Wim de VRIES. ECOLOGICAL EFFECTS OF NITROGEN DEPOSITION ON URBAN FORESTS: AN OVERVIEW[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 445-456.
[5] Jianlin SHEN, Yong LI, Yi WANG, Yanyan LI, Xiao ZHU, Wenqian JIANG, Yuyuan LI, Jinshui WU. SOIL NITROGEN CYCLING AND ENVIRONMENTAL IMPACTS IN THE SUBTROPICAL HILLY REGION OF CHINA: EVIDENCE FROM MEASUREMENTS AND MODELING[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 407-424.
[6] Bo ZHU, Zhiyuan YAO, Dongni HU, Hamidou BAH. EFFECTS OF SUBSTITUTION OF MINERAL NITROGEN WITH ORGANIC AMENDMENTS ON NITROGEN LOSS FROM SLOPING CROPLAND OF PURPLE SOIL[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 396-406.
[7] Xueqiang ZHU, Peng ZHOU, Peng MIAO, Haoying WANG, Xinlu BAI, Zhujun CHEN, Jianbin ZHOU. NITROGEN USE AND MANAGEMENT IN ORCHARDS AND VEGETABLE FIELDS IN CHINA: CHALLENGES AND SOLUTIONS[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 386-395.
[8] Fen ZHANG, Xiaopeng GAO, Junjie WANG, Fabo LIU, Xiao MA, Hailin CAO, Xinping CHEN, Xiaozhong WANG. SUSTAINABLE NITROGEN MANAGEMENT FOR VEGETABLE PRODUCTION IN CHINA[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 373-385.
[9] Xia LIANG, Helen SUTER, Shu Kee LAM, Charlie WALKER, Roya KHALIL, Deli CHEN. SUSTAINABLE NITROGEN MANAGEMENT IN AUSTRALIAN AGROECOSYSTEMS: CHALLENGES AND OPPORTUNITIES[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 366-372.
[10] Xin ZHANG, Yanyu WANG, Lena SCHULTE-UEBBING, Wim DE VRIES, Tan ZOU, Eric A. DAVIDSON. SUSTAINABLE NITROGEN MANAGEMENT INDEX: DEFINITION, GLOBAL ASSESSMENT AND POTENTIAL IMPROVEMENTS[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 356-365.
[11] Jingjing PENG, Olatunde OLADELE, Xiaotong SONG, Xiaotang JU, Zhongjun JIA, Hangwei HU, Xuejun LIU, Shuikuan BEI, Anhui GE, Limei ZHANG, Zhenling CUI. OPPORTUNITIES AND APPROACHES FOR MANIPULATING SOIL-PLANT MICROBIOMES FOR EFFECTIVE CROP NITROGEN USE IN AGROECOSYSTEMS[J]. Front. Agr. Sci. Eng. , 2022, 9(3): 333-343.
[12] Cathryn A. O'SULLIVAN, Elliott G. DUNCAN, Margaret M. ROPER, Alan E. RICHARDSON, John A. KIRKEGAARD, Mark B. PEOPLES. ROOT EXUDATES FROM CANOLA EXHIBIT BIOLOGICAL NITRIFICATION INHIBITION AND ARE EFFECTIVE IN INHIBITING AMMONIA OXIDATION IN SOIL[J]. Front. Agr. Sci. Eng. , 2022, 9(2): 177-186.
[13] Emily C. COOLEDGE, David R. CHADWICK, Lydia M. J. SMITH, Jonathan R. LEAKE, Davey L. JONES. AGRONOMIC AND ENVIRONMENTAL BENEFITS OF REINTRODUCING HERB- AND LEGUME-RICH MULTISPECIES LEYS INTO ARABLE ROTATIONS: A REVIEW[J]. Front. Agr. Sci. Eng. , 2022, 9(2): 245-271.
[14] Yandan FU, Jiahui KANG, Ziyue LI, Xuejun LIU, Wen XU. CONCENTRATIONS AND FLUXES OF DISSOLVED NUTRIENTS IN THE YANGTZE RIVER: LONG-TERM TRENDS AND ECOLOGICAL IMPACTS[J]. Front. Agr. Sci. Eng. , 2021, 8(4): 559-567.
[15] Yinglin JI, Mingyang XU, Aide WANG. RECENT ADVANCES IN THE REGULATION OF CLIMACTERIC FRUIT RIPENING: HORMONE, TRANSCRIPTION FACTOR AND EPIGENETIC MODIFICATIONS[J]. Front. Agr. Sci. Eng. , 2021, 8(2): 314-334.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed