ROLE OF NITROGEN SENSING AND ITS INTEGRATIVE SIGNALING PATHWAYS IN SHAPING ROOT SYSTEM ARCHITECTURE

Highlights

● 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.

Abstract

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.

Graphical abstract

Keywords

Nitrogen / root system architecture / phytohormone / crosstalk / nitrogen-use efficiency / breeding strategy

References

[1] GodfrayH C, BeddingtonJ R, CruteI R, HaddadL, LawrenceD, MuirJ F, PrettyJ, RobinsonS, ThomasS M, ToulminC. Food security: the challenge of feeding 9 billion people. Science , 2010, 327( 5967): 812–818

[2] PingaliP L. 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

[3] RaunW R, JohnsonG V. Improving nitrogen use efficiency for cereal production. Agronomy Journal , 1999, 91( 3): 357–363

[4] GoodingM J, AddisuM, UppalR K, SnapeJ W, JonesH E. Effect of wheat dwarfing genes on nitrogen-use efficiency. Journal of Agricultural Science , 2012, 150( 1): 3–22

[5] LiS, Tian Y, WuK, YeY, Yu J, ZhangJ, LiuQ, HuM, Li H, TongY, HarberdN P, FuX. Modulating plant growth-metabolism coordination for sustainable agriculture. Nature , 2018, 560( 7720): 595–600

[6] KrappA, DavidL C, ChardinC, GirinT, MarmagneA, LeprinceA S, ChaillouS, Ferrario-MéryS, MeyerC, Daniel-VedeleF. Nitrate transport and signalling in Arabidopsis . Journal of Experimental Botany , 2014, 65(3): 789–798

[7] KantS. Understanding nitrate uptake, signaling and remobilisation for improving plant nitrogen use efficiency. Seminars in Cell & Developmental Biology , 2018, 74 : 89–96

[8] ShenT C. The induction of nitrate reductase and the preferential assimilation of ammonium in germinating rice seedlings. Plant Physiology , 1969, 44( 11): 1650–1655

[9] ReisenauerH M. 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] LarkR M, MilneA E, AddiscottT M, GouldingK W T, WebsterC P, O’FlahertyS. 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

[11] CrawfordN M, GlassA D M. Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science , 1998, 3( 10): 389–395

[12] FordeB G. Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta , 2000, 1465( 1−2): 219–235

[13] MillerA J, FanX, OrselM, SmithS J, WellsD M. Nitrate transport and signalling. Journal of Experimental Botany , 2007, 58( 9): 2297–2306

[14] BrittoD T, SiddiqiM Y, GlassA D M, KronzuckerH J. 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

[15] KrappA. Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Current Opinion in Plant Biology , 2015, 25 : 115–122

[16] TsayY F, SchroederJ I, FeldmannK A, CrawfordN M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell , 1993, 72( 5): 705–713

[17] HoC H, LinS H, HuH C, TsayY F. CHL1 functions as a nitrate sensor in plants. Cell , 2009, 138( 6): 1184–1194

[18] ParkerJ L, NewsteadS. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature , 2014, 507( 7490): 68–72

[19] LiuK H, TsayY F. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO Journal , 2003, 22( 5): 1005–1013

[20] SunJ, BankstonJ R, PayandehJ, HindsT R, ZagottaW N, ZhengN. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature , 2014, 507( 7490): 73–77

[21] HuH C, WangY Y, TsayY F. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant Journal , 2009, 57( 2): 264–278

[22] TsayY F, ChiuC C, TsaiC B, HoC H, HsuP K. Nitrate transporters and peptide transporters. FEBS Letters , 2007, 581( 12): 2290–2300

[23] ChiangC S, StaceyG, TsayY F. Mechanisms and functional properties of two peptide transporters, AtPTR2 and fPTR2. Journal of Biological Chemistry , 2004, 279( 29): 30150–30157

[24] ZhouJ J, TheodoulouF L, MuldinI, IngemarssonB, MillerA J. 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

[25] KomarovaN Y, ThorK, GublerA, MeierS, DietrichD, WeichertA, SuterGrotemeyer M, TegederM, RentschD. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology , 2008, 148( 2): 856–869

[26] SugiuraM, GeorgescuM N, TakahashiM. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant & Cell Physiology , 2007, 48( 7): 1022–1035

[27] Nour-EldinH H, AndersenT G, BurowM, MadsenS R, JørgensenM E, OlsenC E, DreyerI, HedrichR, GeigerD, HalkierB A. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature , 2012, 488( 7412): 531–534

[28] KroukG, LacombeB, BielachA, Perrine-WalkerF, MalinskaK, MounierE, HoyerovaK, TillardP, LeonS, LjungK, ZazimalovaE, BenkovaE, NacryP, GojonA. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell , 2010, 18( 6): 927–937

[29] KannoY, HanadaA, ChibaY, IchikawaT, NakazawaM, MatsuiM, KoshibaT, KamiyaY, SeoM. 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

[30] TalI, ZhangY, JørgensenM E, PisantyO, BarbosaI C R, ZourelidouM, RegnaultT, CrocollC, ErikOlsen C, WeinstainR, SchwechheimerC, HalkierB A, Nour-EldinH H, EstelleM, ShaniE. The Arabidopsis NPF3 protein is a GA transporter. Nature Communications , 2016, 7( 1): 11486

[31] DeAngeli A, MonachelloD, EphritikhineG, FrachisseJ M, ThomineS, GambaleF, Barbier-BrygooH. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature , 2006, 442( 7105): 939–942

[32] GeelenD, LurinC, BouchezD, FrachisseJ M, LelièvreF, CourtialB, Barbier-BrygooH, MaurelC. 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

[33] MaierhoferT, LindC, HüttlS, ScherzerS, PapenfußM, SimonJ, Al-RasheidK A S, AcheP, RennenbergH, HedrichR, MüllerT D, GeigerD. A single-pore residue renders the Arabidopsis root anion channel SLAH2 highly nitrate selective. Plant Cell , 2014, 26( 6): 2554–2567

[34] CrawfordN M. Nitrate: nutrient and signal for plant growth. Plant Cell , 1995, 7( 7): 859–868

[35] QuaggiottiS, RupertiB, BorsaP, DestroT, MalagoliM. 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

[36] O’BrienJ A, VegaA, BouguyonE, KroukG, GojonA, CoruzziG, GutiérrezR A. Nitrate transport, sensing, and responses in plants. Molecular Plant , 2016, 9( 6): 837–856

[37] IqbalA, QiangD, AlamzebM, XiangruW, HuipingG, HenghengZ, NianchangP, XilingZ, MeizhenS. 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

[38] HuangN C, LiuK H, LoH J, TsayY F. 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

[39] VertG, ChoryJ. A toggle switch in plant nitrate uptake. Cell , 2009, 138( 6): 1064–1066

[40] LiW, Wang Y, OkamotoM, CrawfordN M, SiddiqiM Y, GlassA D M. Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiology , 2007, 143( 1): 425–433

[41] KibaT, Feria-BourrellierA B, LafougeF, LezhnevaL, Boutet-MerceyS, OrselM, BréhautV, MillerA, Daniel-VedeleF, SakakibaraH, KrappA. 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

[42] KoturZ, MackenzieN, RameshS, TyermanS D, KaiserB N, GlassA D M. Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytologist , 2012, 194( 3): 724–731

[43] OkamotoM, KumarA, LiW, Wang Y, SiddiqiM Y, CrawfordN M, GlassA D M. 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] XuanW, BeeckmanT, XuG. Plant nitrogen nutrition: sensing and signaling. Current Opinion in Plant Biology , 2017, 39 : 57–65

[45] LinS H, KuoH F, CanivencG, LinC S, LepetitM, HsuP K, TillardP, LinH L, WangY Y, TsaiC B, GojonA, TsayY F. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell , 2008, 20( 9): 2514–2528

[46] LiJ Y, FuY L, PikeS M, BaoJ, TianW, ZhangY, ChenC Z, ZhangY, LiH M, HuangJ, LiL G, SchroederJ I, GassmannW, GongJ M. 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

[47] WangY Y, TsayY F. Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell , 2011, 23( 5): 1945–1957

[48] TaochyC, GaillardI, IpotesiE, OomenR, LeonhardtN, ZimmermannS, PeltierJ B, SzponarskiW, SimonneauT, SentenacH, GibratR, BoyerJ C. The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress. Plant Journal , 2015, 83( 3): 466–479

[49] SegonzacC, BoyerJ C, IpotesiE, SzponarskiW, TillardP, TouraineB, SommererN, RossignolM, GibratR. Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell , 2007, 19( 11): 3760–3777

[50] HsuP K, TsayY F. 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

[51] FanS C, LinC S, HsuP K, LinS H, TsayY F. 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

[52] OkamotoM, VidmarJ J, GlassA D M. Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant & Cell Physiology , 2003, 44( 3): 304–317

[53] TegederM, Masclaux-DaubresseC. Source and sink mechanisms of nitrogen transport and use. New Phytologist , 2018, 217( 1): 35–53

[54] AlmagroA, LinS H, TsayY F. Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell , 2008, 20( 12): 3289–3299

[55] ChopinF, OrselM, DorbeM F, ChardonF, TruongH N, MillerA J, KrappA, Daniel-VedeleF. The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell , 2007, 19( 5): 1590–1602

[56] LéranS, GargB, BoursiacY, Corratgé-FaillieC, BrachetC, TillardP, GojonA, LacombeB. AtNPF5.5, a nitrate transporter affecting nitrogen accumulation in Arabidopsis embryo. Scientific Reports , 2015, 5( 1): 7962

[57] WangM Y, SiddiqiM Y, RuthT J, GlassA. Ammonium uptake by rice roots (II. Kinetics of ¹⁵NH₄⁺ influx across the plasmalemma). Plant Physiology , 1993, 103( 4): 1259–1267

[58] CerezoM, TillardP, GojonA, Primo-MilloE, García-AgustínP. Characterization and regulation of ammonium transport systems in Citrus plants. Planta , 2001, 214( 1): 97–105

[59] LudewigU, vonWirén N, RentschD, FrommerW B. Rhesus factors and ammonium: a function in efflux. Genome Biology , 2001, 2( 3): reviews1010

[60] LoquéD, YuanL, KojimaS, GojonA, WirthJ, GazzarriniS, IshiyamaK, TakahashiH, vonWirén N. 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

[61] LoquéD, LalondeS, LoogerL L, vonWirén N, FrommerW B. A cytosolic trans-activation domain essential for ammonium uptake. Nature , 2007, 446( 7132): 195–198

[62] LanquarV, LoquéD, HörmannF, YuanL, BohnerA, EngelsbergerW R, LalondeS, SchulzeW X, vonWirén N, FrommerW B. Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis . Plant Cell , 2009, 21(11): 3610–3622

[63] WangW, LiA, Zhang Z, ChuC. Posttranslational modifications: regulation of nitrogen utilization and signaling. Plant & Cell Physiology , 2021, 62( 4): 543–552

[64] SohlenkampC, WoodC C, RoebG W, UdvardiM K. Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiology , 2002, 130( 4): 1788–1796

[65] GoelP, SinghA K. Abiotic stresses downregulate key genes involved in nitrogen uptake and assimilation in Brassica juncea L. PLoS One , 2015, 10( 11): e0143645

[66] XuG, Fan X, MillerA J. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology , 2012, 63( 1): 153–182

[67] LeaP J, MiflinB J. Alternative route for nitrogen assimilation in higher plants. Nature , 1974, 251( 5476): 614–616

[68] MeyerC, StittM. Nitrate reduction and signalling. In: Lea P J, Morot-Gaudry J F, eds. Plant Nitrogen. Springer , 2001, 37–59

[69] WilkinsonJ Q, CrawfordN M. 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] UnnoH, UchidaT, SugawaraH, KurisuG, SugiyamaT, YamayaT, SakakibaraH, HaseT, KusunokiM. Atomic structure of plant glutamine synthetase: a key enzyme for plant productivity. Journal of Biological Chemistry , 2006, 281( 39): 29287–29296

[71] SwarbreckS M, Defoin-PlatelM, HindleM, SaqiM, HabashD Z. New perspectives on glutamine synthetase in grasses. Journal of Experimental Botany , 2011, 62( 4): 1511–1522

[72] WallsgroveR M, TurnerJ C, HallN P, KendallA C, BrightS W. Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiology , 1987, 83( 1): 155–158

[73] LeaP J, RobinsonS A, StewartG R. 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] TempleS J, VanceC P, StephenGantt J. Glutamate synthase and nitrogen assimilation. Trends in Plant Science , 1998, 3( 2): 51–56

[75] ChenF L, CullimoreJ V. 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

[76] García-CalderónM, Pérez-DelgadoC M, CredaliA, VegaJ M, BettiM, MárquezA J. Genes for asparagine metabolism in Lotus japonicus: differential expression and interconnection with photorespiration. BMC Genomics , 2017, 18( 1): 781

[77] WongH K, ChanH K, CoruzziG M, LamH M. Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis . Plant Physiology , 2004, 134(1): 332–338

[78] LamH M, WongP, ChanH K, YamK M, ChenL, ChowC M, CoruzziG M. Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis . Plant Physiology , 2003, 132(2): 926–935

[79] JiangY L, WangX P, SunH, HanS J, LiW F, CuiN, LinG M, ZhangJ Y, ChengW, CaoD D, ZhangZ Y, ZhangC C, ChenY, ZhouC Z. 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

[80] GruberB D, GiehlR F H, FriedelS, vonWirén N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology , 2013, 163( 1): 161–179

[81] MalamyJ E. Intrinsic and environmental response pathways that regulate root system architecture. Plant, Cell & Environment , 2005, 28( 1): 67–77

[82] MounierE, PerventM, LjungK, GojonA, NacryP. 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

[83] KibaT, KrappA. Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant & Cell Physiology , 2016, 57( 4): 707–714

[84] BoerM D, SantosTeixeira J, TenTusscher K H. 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

[85] GiehlR F H, vonWirén N. Root nutrient foraging. Plant Physiology , 2014, 166( 2): 509–517

[86] DrewM C, SakerL R. 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

[87] LinkohrB I, WilliamsonL C, FitterA H, LeyserH M O. Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis . Plant Journal , 2002, 29(6): 751–760

[88] SutherlandW J, StillmanR A. The foraging tactics of plants. Oikos , 1988, 52( 3): 239–244

[89] ZhangH, JenningsA, BarlowP W, FordeB G. 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

[90] TianQ, ChenF, LiuJ, ZhangF, MiG. 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

[91] TaoY, FerrerJ L, LjungK, PojerF, HongF, LongJ A, LiL, Moreno J E, BowmanM E, IvansL J, ChengY, LimJ, ZhaoY, BallaréC L, SandbergG, NoelJ P, ChoryJ. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell , 2008, 133( 1): 164–176

[92] ZhaoY. Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Molecular Plant , 2012, 5( 2): 334–338

[93] MaW, Li J, QuB, HeX, Zhao X, LiB, FuX, Tong Y. Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis . Plant Journal , 2014, 78(1): 70–79

[94] YuL H, MiaoZ Q, QiG F, WuJ, Cai X T, MaoJ L, XiangC B. MADS-box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals. Molecular Plant , 2014, 7( 11): 1653–1669

[95] LuschnigC, GaxiolaR A, GrisafiP, FinkG R. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana . Genes & Development , 1998, 12(14): 2175–2187

[96] MartinièreA, LavagiI, NageswaranG, RolfeD J, Maneta-PeyretL, LuuD T, BotchwayS W, WebbS E D, MongrandS, MaurelC, Martin-FernandezM L, Kleine-VehnJ, FrimlJ, MoreauP, RunionsJ. 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

[97] BlilouI, XuJ, Wildwater M, WillemsenV, PaponovI, FrimlJ, HeidstraR, AidaM, PalmeK, ScheresB. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature , 2005, 433( 7021): 39–44

[98] ÖtvösK, MarconiM, VegaA, O’BrienJ, JohnsonA, AbualiaR, AntonielliL, MontesinosJ C, ZhangY, TanS, CuestaC, ArtnerC, BouguyonE, GojonA, FrimlJ, GutiérrezR A, WabnikK, BenkováE. Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO Journal , 2021, 40( 3): e106862

[99] HuangS, ChenS, LiangZ, ZhangC, YanM, ChenJ, XuG, Fan X, ZhangY. 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

[100] JiaZ, GiehlR F H, MeyerR C, AltmannT, vonWirén N. Natural variation of BSK3 tunes brassinosteroid signaling to regulate root foraging under low nitrogen. Nature Communications , 2019, 10( 1): 2378

[101] JiaZ, GiehlR F H, vonWirén N. Local auxin biosynthesis acts downstream of brassinosteroids to trigger root foraging for nitrogen. Nature Communications , 2021, 12( 1): 5437

[102] JiaZ, GiehlR F H, vonWirén N. The root foraging response under low nitrogen depends on DWARF1-mediated brassinosteroid biosynthesis. Plant Physiology , 2020, 183( 3): 998–1010

[103] ChaiwanonJ, WangZ Y. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Current Biology , 2015, 25( 8): 1031–1042

[104] FridmanY, ElkoubyL, HollandN, VragovićK, ElbaumR, Savaldi-GoldsteinS. Root growth is modulated by differential hormonal sensitivity in neighboring cells. Genes & Development , 2014, 28( 8): 912–920

[105] CamutL, GallovaB, JilliL, Sirlin-JosserandM, CarreraE, Sakvarelidze-AchardL, RuffelS, KroukG, ThomasS G, HeddenP, PhillipsA L, DavièreJ M, AchardP. Nitrate signaling promotes plant growth by upregulating gibberellin biosynthesis and destabilization of DELLA proteins. Current Biology , 2021, 31( 22): 4971–4982.e4

[106] LokdarshiA, ConnerW C, McClintockC, LiT, Roberts D M. Arabidopsis CML38, a calcium sensor that localizes to ribonucleoprotein complexes under hypoxia stress. Plant Physiology , 2016, 170( 2): 1046–1059

[107] SongX, LiJ, Lyu M, KongX, HuS, Song Q, ZuoK. CALMODULIN-LIKE-38 and PEP1 RECEPTOR 2 integrate nitrate and brassinosteroid signals to regulate root growth. Plant Physiology , 2021, 187( 3): 1779–1794

[108] AlvarezJ M, RiverasE, VidalE A, GrasD E, Contreras-LópezO, TamayoK P, AceitunoF, GómezI, RuffelS, LejayL, JordanaX, GutiérrezR A. 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

[109] LiuK H, HuangC Y, TsayY F. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell , 1999, 11( 5): 865–874

[110] VidalE A, MoyanoT C, RiverasE, Contreras-LópezO, GutiérrezR A. 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

[111] VidalE A, ÁlvarezJ M, GutiérrezR A. 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

[112] HarrisJ M, Ondzighi-AssoumeC A. Environmental nitrate signals through abscisic acid in the root tip. Plant Signaling & Behavior , 2017, 12( 1): e1273303

[113] SignoraL, DeSmet I, FoyerC H, ZhangH. 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] LéranS, EdelK H, PerventM, HashimotoK, Corratgé-FaillieC, OffenbornJ N, TillardP, GojonA, KudlaJ, LacombeB. 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

[115] JungJ Y, ShinR, SchachtmanD P. Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis . Plant Cell , 2009, 21(2): 607–621

[116] TianQ Y, SunP, ZhangW H. Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana . New Phytologist , 2009, 184(4): 918–931

[117] ZhangH, FordeB G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science , 1998, 279( 5349): 407–409

[118] MediciA, KroukG. The primary nitrate response: a multifaceted signalling pathway. Journal of Experimental Botany , 2014, 65( 19): 5567–5576

[119] LiuK H, DienerA, LinZ, LiuC, SheenJ. Primary nitrate responses mediated by calcium signalling and diverse protein phosphorylation. Journal of Experimental Botany , 2020, 71( 15): 4428–4441

[120] UndurragaS F, Ibarra-HenríquezC, FredesI, ÁlvarezJ M, GutiérrezR A. Nitrate signaling and early responses in Arabidopsis roots. Journal of Experimental Botany , 2017, 68( 10): 2541–2551

[121] MarchiveC, RoudierF, CastaingsL, BréhautV, BlondetE, ColotV, MeyerC, KrappA. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nature Communications , 2013, 4( 1): 1713

[122] LiuK H, NiuY, KonishiM, WuY, Du H, SunChung H, LiL, Boudsocq M, McCormackM, MaekawaS, IshidaT, ZhangC, ShokatK, YanagisawaS, SheenJ. Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature , 2017, 545( 7654): 311–316

[123] LiuL, GaoH, LiS, Han Z, LiB. Calcium signaling networks mediate nitrate sensing and responses in Arabidopsis . Plant Signaling & Behavior , 2021, 16(10): 1938441

[124] WangX, FengC, TianL, HouC, TianW, HuB, Zhang Q, RenZ, NiuQ, SongJ, KongD, LiuL, HeY, Ma L, ChuC, LuanS, LiL. A transceptor-channel complex couples nitrate sensing to calcium signaling in Arabidopsis . Molecular Plant , 2021, 14(5): 774–786

[125] RuffelS, KroukG, RistovaD, ShashaD, BirnbaumK D, CoruzziG M. 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] GuanP, WangR, NacryP, BretonG, KayS A, Pruneda-PazJ L, DavaniA, CrawfordN M. 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

[127] RemansT, NacryP, PerventM, FilleurS, DiatloffE, MounierE, TillardP, FordeB G, GojonA. 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

[128] GuanP, RipollJ J, WangR, VuongL, Bailey-SteinitzL J, YeD, Crawford N M. 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

[129] ChenX, YaoQ, GaoX, JiangC, HarberdN P, FuX. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Current Biology , 2016, 26( 5): 640–646

[130] ArayaT, MiyamotoM, WibowoJ, SuzukiA, KojimaS, TsuchiyaY N, SawaS, FukudaH, vonWirén N, TakahashiH. 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

[131] DongW, WangY, TakahashiH. CLE-CLAVATA1 signaling pathway modulates lateral root development under sulfur deficiency. Plants , 2019, 8( 4): 103

[132] ArayaT, vonWirén N, TakahashiH. CLE peptides regulate lateral root development in response to nitrogen nutritional status of plants. Plant Signaling & Behavior , 2014, 9( 7): e29302

[133] TabataR, SumidaK, YoshiiT, OhyamaK, ShinoharaH, MatsubayashiY. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science , 2014, 346( 6207): 343–346

[134] OhkuboY, TanakaM, TabataR, Ogawa-OhnishiM, MatsubayashiY. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants , 2017, 3( 4): 17029

[135] OtaR, OhkuboY, YamashitaY, Ogawa-OhnishiM, MatsubayashiY. 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] TaleskiM, IminN, DjordjevicM A. 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

[137] HanX, WuK, Fu X, LiuQ. Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture. aBIOTECH , 2020, 1 : 1–21

[138] RanathungeK, El-KereamyA, GiddaS, BiY M, RothsteinS J. 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

[139] BaoA, LiangZ, ZhaoZ, CaiH. 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

[140] WangW, HuB, Yuan D, LiuY, CheR, HuY, Ou S, LiuY, ZhangZ, WangH, LiH, Jiang Z, ZhangZ, GaoX, QiuY, MengX, LiuY, BaiY, LiangY, WangY, ZhangL, LiL, Sodmergen , JingH, LiJ, Chu C. 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

[141] FanX, FengH, TanY, XuY, Miao Q, XuG. 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

[142] FanX, TangZ, TanY, ZhangY, LuoB, YangM, LianX, ShenQ, MillerA J, XuG. 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

[143] ChenJ, LiuX, LiuS, FanX, ZhaoL, SongM, FanX, XuG. Co-overexpression of OsNAR2.1 and OsNRT2.3a increased agronomic nitrogen use efficiency in transgenic rice plants. Frontiers in Plant Science , 2020, 11 : 1245

[144] GaoZ, WangY, ChenG, ZhangA, YangS, ShangL, WangD, RuanB, LiuC, JiangH, DongG, ZhuL, HuJ, Zhang G, ZengD, GuoL, XuG, Teng S, HarberdN P, QianQ. The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nature Communications , 2019, 10( 1): 5207

[145] TabuchiM, SugiyamaK, IshiyamaK, InoueE, SatoT, TakahashiH, YamayaT. 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

[146] FunayamaK, KojimaS, Tabuchi-KobayashiM, SawaY, NakayamaY, HayakawaT, YamayaT. Cytosolic glutamine synthetase1;2 is responsible for the primary assimilation of ammonium in rice roots. Plant & Cell Physiology , 2013, 54( 6): 934–943

[147] WangM, HasegawaT, BeierM, HayashiM, OhmoriY, YanoK, TeramotoS, KamiyaT, FujiwaraT. Growth and nitrate reductase activity are impaired in rice osnlp4 mutants supplied with nitrate. Plant & Cell Physiology , 2021, 62( 7): 1156–1167

[148] ZengD D, QinR, LiM, Alamin M, JinX L, LiuY, ShiC H. 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

[149] LiuY, WangH, JiangZ, WangW, XuR, Wang Q, ZhangZ, LiA, Liang Y, OuS, LiuX, CaoS, TongH, WangY, ZhouF, LiaoH, HuB, Chu C. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature , 2021, 590( 7847): 600–605

[150] SisharminiA, AprianaA, KhumaidaN, TrijatmikoK R, PurwokoB S. Expression of a cucumber alanine aminotransferase2 gene improves nitrogen use efficiency in transgenic rice. Journal of Genetic Engineering and Biotechnology , 2019, 17( 1): 9

[151] WangD, XuT, Yin Z, WuW, GengH, LiL, Yang M, CaiH, LianX. Overexpression of OsMYB305 in rice enhances the nitrogen uptake under low-nitrogen condition. Frontiers in Plant Science , 2020, 11 : 369

[152] SunH, QianQ, WuK, Luo J, WangS, ZhangC, MaY, Liu Q, HuangX, YuanQ, HanR, ZhaoM, DongG, GuoL, ZhuX, GouZ, WangW, WuY, Lin H, FuX. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nature Genetics , 2014, 46( 6): 652–656

[153] YuC, Liu Y, ZhangA, SuS, Yan A, HuangL, AliI, LiuY, FordeB G, GanY. MADS-box transcription factor OsMADS25 regulates root development through affection of nitrate accumulation in rice. PLoS One , 2015, 10( 8): e0135196

[154] ArausV, VidalE A, PuelmaT, AlamosS, MieuletD, GuiderdoniE, GutiérrezR A. Members of BTB gene family of scaffold proteins suppress nitrate uptake and nitrogen use efficiency. Plant Physiology , 2016, 171( 2): 1523–1532

[155] LiangC, WangY, ZhuY, TangJ, HuB, Liu L, OuS, WuH, Sun X, ChuJ, ChuC. 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

[156] WuK, Wang S, SongW, ZhangJ, WangY, LiuQ, YuJ, Ye Y, LiS, ChenJ, ZhaoY, WangJ, WuX, Wang M, ZhangY, LiuB, WuY, Harberd N P, FuX. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science , 2020, 367( 6478): eaaz2046

[157] ZhangS, ZhuL, ShenC, JiZ, Zhang H, ZhangT, LiY, Yu J, YangN, HeY, Tian Y, WuK, WuJ, Harberd N P, ZhaoY, FuX, Wang S, LiS. 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

[158] ZhangY, TanL, ZhuZ, YuanL, XieD, SunC. TOND1 confers tolerance to nitrogen deficiency in rice. Plant Journal , 2015, 81( 3): 367–376

[159] Arai-SanohY, TakaiT, YoshinagaS, NakanoH, KojimaM, SakakibaraH, KondoM, UgaY. Deep rooting conferred by DEEPER ROOTING 1 enhances rice yield in paddy fields. Scientific Reports , 2014, 4( 1): 5563

[160] HeX, Qu B, LiW, ZhaoX, TengW, MaW, Ren Y, LiB, LiZ, Tong Y. The nitrate-inducible NAC transcription factor TaNAC2–5A controls nitrate response and increases wheat yield. Plant Physiology , 2015, 169( 3): 1991–2005

[161] QuB, He X, WangJ, ZhaoY, TengW, ShaoA, ZhaoX, MaW, Wang J, LiB, LiZ, Tong Y. A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiology , 2015, 167( 2): 411–423

[162] HuM, Zhao X, LiuQ, HongX, ZhangW, ZhangY, SunL, LiH, Tong Y. Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnology Journal , 2018, 16( 11): 1858–1867

[163] GuoM, WangQ, ZongY, NianJ, LiH, Li J, WangT, GaoC, ZuoJ. Genetic manipulations of TaARE1 boost nitrogen utilization and grain yield in wheat. Journal of Genetics and Genomics , 2021, 48( 10): 950–953

[164] ShaoA, MaW, Zhao X, HuM, HeX, Teng W, LiH, TongY. The auxin biosynthetic TRYPTOPHAN AMINOTRANSFERASE RELATED TaTAR2.1–3A increases grain yield of wheat. Plant Physiology , 2017, 174( 4): 2274–2288

[165] FoxT, DeBruinJ, HaugCollet K, TrimnellM, ClappJ, LeonardA, LiB, Scolaro E, CollinsonS, GlassmanK, MillerM, SchusslerJ, DolanD, LiuL, GhoC, AlbertsenM, LoussaertD, ShenB. 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

[166] HuangX, QianQ, LiuZ, SunH, HeS, Luo D, XiaG, ChuC, LiJ, Fu X. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics , 2009, 41( 4): 494–497

[167] WuK, Xu H, GaoX, FuX. New insights into gibberellin signaling in regulating plant growth-metabolic coordination. Current Opinion in Plant Biology , 2021, 63 : 102074

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32020103004, 32170251), and the Strategic Priority Research Program of Chinese Academy of Sciences (XDA24020309), the Youth Innovation Promotion Association CAS (2019100), and Key-Area Research and Development Program of Guangdong Province (2018B020202012). We thank all the colleagues who contributed to the work.

Compliance with ethics guidelines

Hui Liu, Qian Liu, Xiuhua Gao, and Xiangdong Fu declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any study with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2022. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)