1932

Abstract

Nitrogen accounts for approximately 60% of the fertilizer consumed each year; thus, it represents one of the major input costs for most nonlegume crops. Nitrate is one of the two major forms of nitrogen that plants acquire from the soil. Mechanistic insights into nitrate transport and signaling have enabled new strategies for enhancing nitrogen utilization efficiency, for lowering input costs for farming, and, more importantly, for alleviating environmental impacts (e.g., eutrophication and production of the greenhouse gas NO). Over the past decade, significant progress has been made in understanding how nitrate is acquired from the surroundings, how it is efficiently distributed into different plant tissues in response to environmental changes, how nitrate signaling is perceived and transmitted, and how shoot and root nitrogen status is communicated. Several key components of these processes have proven to be novel tools for enhancing nitrate- and nitrogen-use efficiency. In this review, we focus on the roles of NRT1 and NRT2 in nitrate uptake and nitrate allocation among different tissues; we describe the functions of the transceptor NRT1.1, transcription factors, and small signaling peptides in nitrate signaling and tissue communication; and we compile the new strategies for improving nitrogen-use efficiency.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-042817-040056
2018-04-29
2024-10-11
Loading full text...

Full text loading...

/deliver/fulltext/arplant/69/1/annurev-arplant-042817-040056.html?itemId=/content/journals/10.1146/annurev-arplant-042817-040056&mimeType=html&fmt=ahah

Literature Cited

  1. Almagro A, Lin SH, Tsay YF. 1.  2008. Characterization of the Arabidopsis nitrate transporter NRT1.6 reveals a role of nitrate in early embryo development. Plant Cell 20:3289–99 [Google Scholar]
  2. Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras-Lopez O. 2.  et al. 2014. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J 80:1–13 [Google Scholar]
  3. Andersen TG, Nour-Eldin HH, Fuller VL, Olsen CE, Burow M, Halkier BA. 3.  2013. Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in vegetative Arabidopsis. Plant Cell 25:3133–45 [Google Scholar]
  4. Araus V, Vidal EA, Puelma T, Alamos S, Mieulet D. 4.  et al. 2016. Members of BTB gene family of scaffold proteins suppress nitrate uptake and nitrogen use efficiency. Plant Physiol 171:1523–32 [Google Scholar]
  5. Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S. 5.  et al. 2014. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. PNAS 111:2029–34 [Google Scholar]
  6. Bellegarde F, Gojon A, Martin A. 6.  2017. Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana. J. Exp. Bot 68:2553–65 [Google Scholar]
  7. Bi YM, Kant S, Clarke J, Gidda S, Ming F. 7.  et al. 2009. Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant Cell Environ 32:1749–60 [Google Scholar]
  8. Bouguyon E, Brun F, Meynard D, Kubes M, Pervent M. 8.  et al. 2015. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1:15015 [Google Scholar]
  9. Bouguyon E, Perrine-Walker F, Pervent M, Rochette J, Cuesta C. 9.  et al. 2016. Nitrate controls root development through posttranscriptional regulation of the NRT1.1/NPF6.3 transporter/sensor. Plant Physiol 172:1237–48 [Google Scholar]
  10. Brauer EK, Rochon A, Bi YM, Bozzo GG, Rothstein SJ, Shelp BJ. 10.  2011. Reappraisal of nitrogen use efficiency in rice overexpressing glutamine synthetase1. Physiol. Plant 141:361–72 [Google Scholar]
  11. Camanes G, Pastor V, Cerezo M, Garcia-Andrade J, Vicedo B. 11.  et al. 2012. A deletion in NRT2.1 attenuates Pseudomonas syringae-induced hormonal perturbation, resulting in primed plant defenses. Plant Physiol 158:1054–66 [Google Scholar]
  12. Camargo A, Llamas A, Schnell RA, Higuera JJ, Gonzalez-Ballester D. 12.  et al. 2007. Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19:3491–503 [Google Scholar]
  13. Canales J, Contreras-Lopez O, Alvarez JM, Gutierrez RA. 13.  2017. Nitrate induction of root hair density is mediated by TGA1/TGA4 and CPC transcription factors in Arabidopsis thaliana. Plant J 92:305–16 [Google Scholar]
  14. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y. 14.  et al. 2009. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–35 [Google Scholar]
  15. Cerezo M, Tillard P, Filleur S, Munos S, Daniel-Vedele F, Gojon A. 15.  2001. Major alterations of the regulation of root NO3 uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol 127:262–71 [Google Scholar]
  16. Chen CZ, Lv XF, Li JY, Yi HY, Gong JM. 16.  2012. Arabidopsis NRT1.5 is another essential component in the regulation of nitrate reallocation and stress tolerance. Plant Physiol 159:1582–90 [Google Scholar]
  17. Chen J, Fan X, Qian K, Zhang Y, Song M. 17.  et al. 2017. pOsNAR2.1:OsNAR2.1 expression enhances nitrogen uptake efficiency and grain yield in transgenic rice plants. Plant Biotechnol. J. 15:1273–83 [Google Scholar]
  18. Chen J, Zhang Y, Tan Y, Zhang M, Zhu L. 18.  et al. 2016. Agronomic nitrogen-use efficiency of rice can be increased by driving OsNRT2.1 expression with the OsNAR2.1 promoter. Plant Biotechnol. J. 14:1705–15 [Google Scholar]
  19. Cheng CL, Dewdney J, Nam HG, den Boer BG, Goodman HM. 19.  1988. A new locus (NIA 1) in Arabidopsis thaliana encoding nitrate reductase. EMBO J 7:3309–14 [Google Scholar]
  20. Chiang CS, Stacey G, Tsay YF. 20.  2004. Mechanisms and functional properties of two peptide transporters, AtPTR2 and fPTR2. J. Biol. Chem. 279:30150–57Identifies the potential substrates of plant hormones for NPF transporters. [Google Scholar]
  21. Chiba Y, Shimizu T, Miyakawa S, Kanno Y, Koshiba T. 21.  et al. 2015. Identification of Arabidopsis thaliana NRT1/PTR FAMILY (NPF) proteins capable of transporting plant hormones. J. Plant Res. 128:679–86 [Google Scholar]
  22. Chiu CC, Lin CS, Hsia AP, Su RC, Lin HL, Tsay YF. 22.  2004. Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant Cell Physiol 45:1139–48 [Google Scholar]
  23. Chopin F, Orsel M, Dorbe MF, Chardon F, Truong HN. 23.  et al. 2007. The Arabidopsis ATNRT2.7 nitrate transporter controls nitrate content in seeds. Plant Cell 19:1590–602 [Google Scholar]
  24. Corratge-Faillie C, Lacombe B. 24.  2017. Substrate (un)specificity of Arabidopsis NRT1/PTR FAMILY (NPF) proteins. J. Exp. Bot. 68:3107–13 [Google Scholar]
  25. Crawford NM.25.  1995. Nitrate: nutrient and signal for plant growth. Plant Cell 7:859–68 [Google Scholar]
  26. Crawford NM, Smith M, Bellissimo D, Davis RW. 26.  1988. Sequence and nitrate regulation of the Arabidopsis thaliana mRNA encoding nitrate reductase, a metalloflavoprotein with three functional domains. PNAS 85:5006–10 [Google Scholar]
  27. David LC, Berquin P, Kanno Y, Seo M, Daniel-Vedele F, Ferrario-Mery S. 27.  2016. N availability modulates the role of NPF3.1, a gibberellin transporter, in GA-mediated phenotypes in Arabidopsis. Planta 244:1315–28 [Google Scholar]
  28. Dechorgnat J, Patrit O, Krapp A, Fagard M, Daniel-Vedele F. 28.  2012. Characterization of the Nrt2.6 gene in Arabidopsis thaliana: a link with plant response to biotic and abiotic stress. PLOS ONE 7:e42491 [Google Scholar]
  29. Deng M, Moureaux T, Caboche M. 29.  1989. Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol 91:304–9 [Google Scholar]
  30. Dietrich D, Hammes U, Thor K, Suter-Grotemeyer M, Fluckiger R. 30.  et al. 2004. AtPTR1, a plasma membrane peptide transporter expressed during seed germination and in vascular tissue of Arabidopsis. Plant J 40:488–99 [Google Scholar]
  31. Dodd AN, Kudla J, Sanders D. 31.  2010. The language of calcium signaling. Annu. Rev. Plant Biol. 61:593–620 [Google Scholar]
  32. Drechsler N, Zheng Y, Bohner A, Nobmann B, von Wiren N. 32.  et al. 2015. Nitrate-dependent control of shoot K homeostasis by the nitrate transporter1/peptide transporter family member NPF7.3/NRT1.5 and the stelar K+ outward rectifier SKOR in Arabidopsis. Plant Physiol 169:2832–47 [Google Scholar]
  33. Fan S-C, Lin C-S, Hsu P-K, Lin S-H, Tsay Y-F. 33.  2009. The Arabidopsis nitrate transporter NRT1.7, expressed in phloem, is responsible for source-to-sink remobilization of nitrate. Plant Cell 21:2750–61 [Google Scholar]
  34. Fan X, Feng H, Tan Y, Xu Y, Miao Q, Xu G. 34.  2016. A putative 6-transmembrane nitrate transporter OsNRT1.1b plays a key role in rice under low nitrogen. J. Integr. Plant Biol. 58:590–99 [Google Scholar]
  35. Fan X, Tang Z, Tan Y, Zhang Y, Luo B. 35.  et al. 2016. Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. PNAS 113:7118–23Shows that the nitrate transporter OsNRT2.3b senses cytosolic pH and that overexpression of OsNRT2.3b improves grain yield and NUE in rice. [Google Scholar]
  36. Fan X, Xie D, Chen J, Lu H, Xu Y. 36.  et al. 2014. Over-expression of OsPTR6 in rice increased plant growth at different nitrogen supplies but decreased nitrogen use efficiency at high ammonium supply. Plant Sci 227:1–11 [Google Scholar]
  37. Fang Z, Bai G, Huang W, Wang Z, Wang X, Zhang M. 37.  2017. The rice peptide transporter OsNPF7.3 is induced by organic nitrogen, and contributes to nitrogen allocation and grain yield. Front. Plant Sci. 8:1338 [Google Scholar]
  38. Fang Z, Xia K, Yang X, Grotemeyer MS, Meier S. 38.  et al. 2013. Altered expression of the PTR/NRT1 homologue OsPTR9 affects nitrogen utilization efficiency, growth and grain yield in rice. Plant Biotechnol. J. 11:446–58 [Google Scholar]
  39. Feng H, Yan M, Fan X, Li B, Shen Q. 39.  et al. 2011. Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J. Exp. Bot. 62:2319–32 [Google Scholar]
  40. Filleur S, Dorbe MF, Cerezo M, Orsel M, Granier F. 40.  et al. 2001. An Arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett 489:220–24 [Google Scholar]
  41. Frommer WB, Hummel S, Rentsch D. 41.  1994. Cloning of an Arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Lett 347:185–89 [Google Scholar]
  42. Fu Y, Yi H, Bao J, Gong J. 42.  2015. LeNRT2.3 functions in nitrate acquisition and long-distance transport in tomato. FEBS Lett 589:1072–79 [Google Scholar]
  43. Gan Y, Bernreiter A, Filleur S, Abram B, Forde BG. 43.  2012. Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol 53:1003–16 [Google Scholar]
  44. Giannino D, Nicolodi C, Testone G, Frugis G, Pace E. 44.  et al. 2007. The overexpression of asparagine synthetase A from E. coli affects the nitrogen status in leaves of lettuce (Lactuca sativa L.) and enhances vegetative growth. Euphytica 162:11–22 [Google Scholar]
  45. Gojon A, Gaymard F. 45.  2010. Keeping nitrate in the roots: an unexpected requirement for cadmium tolerance in plants. J. Mol. Cell Biol. 2:299–301 [Google Scholar]
  46. Good AG, Johnson SJ, De Pauw M, Carroll RT, Savidov N. 46.  et al. 2007. Engineering nitrogen use efficiency with alanine aminotransferase. Can. J. Bot. 85:252–62 [Google Scholar]
  47. Gowri G, Kenis JD, Ingemarsson B, Redinbaugh MG, Campbell WH. 47.  1992. Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol. Biol. 18:55–64 [Google Scholar]
  48. Guan P, Ripoll JJ, Wang R, Vuong L, Bailey-Steinitz LJ. 48.  et al. 2017. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. PNAS 114:2419–24 [Google Scholar]
  49. Guan P, Wang R, Nacry P, Breton G, Kay SA. 49.  et al. 2014. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. PNAS 111:15267–72 [Google Scholar]
  50. Guo FQ, Wang R, Chen M, Crawford NM. 50.  2001. The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13:1761–77 [Google Scholar]
  51. Guo FQ, Young J, Crawford NM. 51.  2003. The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–17 [Google Scholar]
  52. Hammes UZ, Meier S, Dietrich D, Ward JM, Rentsch D. 52.  2010. Functional properties of the Arabidopsis peptide transporters AtPTR1 and AtPTR5. J. Biol. Chem. 285:39710–17 [Google Scholar]
  53. He X, Qu B, Li W, Zhao X, Teng W. 53.  et al. 2015. The nitrate-inducible NAC transcription factor TaNAC2-5A controls nitrate response and increases wheat yield. Plant Physiol 169:1991–2005 [Google Scholar]
  54. He YN, Peng JS, Cai Y, Liu DF, Guan Y. 54.  et al. 2017. Tonoplast-localized nitrate uptake transporters involved in vacuolar nitrate efflux and reallocation in Arabidopsis. Sci. Rep 7:6417 [Google Scholar]
  55. Ho CH, Lin SH, Hu HC, Tsay YF. 55.  2009. CHL1 functions as a nitrate sensor in plants. Cell 138:1184–94Demonstrates that NPF6.3/CHL1 acts as both nitrate transporter and sensor. [Google Scholar]
  56. Hsu PK, Tsay YF. 56.  2013. Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiol 163:844–56 [Google Scholar]
  57. Hu B, Wang W, Ou S, Tang J, Li H. 57.  et al. 2015. Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat. Genet. 47:834–38Discovers that natural variation in single-nucleotide polymorphisms in rice subspecies changes nitrate uptake and nitrate-use efficiency. [Google Scholar]
  58. Hu HC, Wang YY, Tsay YF. 58.  2009. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–78 [Google Scholar]
  59. Hu R, Qiu D, Chen Y, Miller AJ, Fan X. 59.  et al. 2016. Knock-down of a tonoplast localized low-affinity nitrate transporter OsNPF7.2 affects rice growth under high nitrate supply. Front. Plant Sci. 7:1529 [Google Scholar]
  60. Hu TZ, Cao KM, Xia M, Wang XP. 60.  2006. Functional characterization of a putative nitrate transporter gene promoter from rice. Acta Biochim. Biophys. 38:795–802 [Google Scholar]
  61. Huang NC, Chiang CS, Crawford NM, Tsay YF. 61.  1996. CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8:2183–91 [Google Scholar]
  62. Huang NC, Liu KH, Lo HJ, Tsay YF. 62.  1999. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. Plant Cell 11:1381–92 [Google Scholar]
  63. Ishimaru Y, Oikawa T, Suzuki T, Takeishi S, Matsuura H. 63.  et al. 2017. GTR1 is a jasmonic acid and jasmonoyl-l-isoleucine transporter in Arabidopsis thaliana. Biosci. Biotechnol. Biochem 81:249–55 [Google Scholar]
  64. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M. 64.  et al. 2012. Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. PNAS 109:9653–58 [Google Scholar]
  65. Kanno Y, Kamiya Y, Seo M. 65.  2013. Nitrate does not compete with abscisic acid as a substrate of AtNPF4.6/NRT1.2/AIT1 in Arabidopsis. Plant Signal. Behav 8:e26624 [Google Scholar]
  66. Karim S, Holmstrom KO, Mandal A, Dahl P, Hohmann S. 66.  et al. 2007. AtPTR3, a wound-induced peptide transporter needed for defence against virulent bacterial pathogens in Arabidopsis. Planta 225:1431–45 [Google Scholar]
  67. Karim S, Lundh D, Holmström K-O, Mandal A, Pirhonen M. 67.  2005. Structural and functional characterization of AtPTR3, a stress-induced peptide transporter of Arabidopsis. J. Mol. Model 11:226–36 [Google Scholar]
  68. Kechid M, Desbrosses G, Rokhsi W, Varoquaux F, Djekoun A, Touraine B. 68.  2013. The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain Phyllobacterium brassicacearum STM196. New Phytol 198:514–24 [Google Scholar]
  69. Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S. 69.  et al. 2012. The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24:245–58 [Google Scholar]
  70. Komarova NY, Thor K, Gubler A, Meier S, Dietrich D. 70.  et al. 2008. AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol 148:856–69 [Google Scholar]
  71. Konishi M, Yanagisawa S. 71.  2013. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 4:1617 [Google Scholar]
  72. Konishi M, Yanagisawa S. 72.  2014. Emergence of a new step towards understanding the molecular mechanisms underlying nitrate-regulated gene expression. J. Exp. Bot. 65:5589–600 [Google Scholar]
  73. Kotur Z, Mackenzie N, Ramesh S, Tyerman SD, Kaiser BN, Glass AD. 73.  2012. Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol 194:724–31 [Google Scholar]
  74. Krouk G.74.  2017. Nitrate signalling: calcium bridges the nitrate gap. Nat. Plants 3:17095 [Google Scholar]
  75. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K. 75.  et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18:927–37Elucidates the functional interplay of nitrate and auxin in lateral root growth mediated by NPF6.3/NRT1.1. [Google Scholar]
  76. Krouk G, Mirowski P, LeCun Y, Shasha DE, Coruzzi GM. 76.  2010. Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol 11:R123 [Google Scholar]
  77. Krusell L, Madsen LH, Sato S, Aubert G, Genua A. 77.  et al. 2002. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–26 [Google Scholar]
  78. Kumar G, Tuli HS, Mittal S, Shandilya JK, Tiwari A, Sandhu SS. 78.  2015. Isothiocyanates: a class of bioactive metabolites with chemopreventive potential. Tumour Biol 36:4005–16 [Google Scholar]
  79. Léran S, Edel KH, Pervent M, Hashimoto K, Corratge-Faillie C. 79.  et al. 2015. Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci. Signal. 8:ra43 [Google Scholar]
  80. Léran S, Garg B, Boursiac Y, Corratgé-Faillie C, Brachet C. 80.  et al. 2015. AtNPF5.5, a nitrate transporter affecting nitrogen accumulation in Arabidopsis embryo. Sci. Rep. 5:7962 [Google Scholar]
  81. Lezhneva L, Kiba T, Feria-Bourrellier AB, Lafouge F, Boutet-Mercey S. 81.  et al. 2014. The Arabidopsis nitrate transporter NRT2.5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants. Plant J 80:230–41 [Google Scholar]
  82. Li B, Byrt C, Qiu J, Baumann U, Hrmova M. 82.  et al. 2016. Identification of a stelar-localized transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiol 170:1014–29 [Google Scholar]
  83. Li B, Qiu J, Jayakannan M, Xu B, Li Y. 83.  et al. 2017. AtNPF2.5 modulates chloride (Cl) efflux from roots of Arabidopsis thaliana. Front. Plant Sci 7:2013 [Google Scholar]
  84. Li H, Yu M, Du XQ, Wang ZF, Wu WH. 84.  et al. 2017. NRT1.5/NPF7.3 functions as a proton-coupled H+/K+ antiporter for K+ loading into the xylem in Arabidopsis. Plant Cell 29:2016–26 [Google Scholar]
  85. Li JY, Fu YL, Pike SM, Bao J, Tian W. 85.  et al. 2010. The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–46 [Google Scholar]
  86. Li S, Qian Q, Fu Z, Zeng D, Meng X. 86.  et al. 2009. Short panicle1 encodes a putative PTR family transporter and determines rice panicle size. Plant J 58:592–605 [Google Scholar]
  87. Li Y, Ouyang J, Wang YY, Hu R, Xia K. 87.  et al. 2015. Disruption of the rice nitrate transporter OsNPF2.2 hinders root-to-shoot nitrate transport and vascular development. Sci. Rep. 5:9635 [Google Scholar]
  88. Lin CM, Koh S, Stacey G, Yu SM, Lin TY, Tsay YF. 88.  2000. Cloning and functional characterization of a constitutively expressed nitrate transporter gene, OsNRT1, from rice. Plant Physiol 122:379–88 [Google Scholar]
  89. Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M. 89.  et al. 2008. Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–28 [Google Scholar]
  90. Lin YL, Tsay YF. 90.  2017. Influence of differing nitrate and nitrogen availability on flowering control in Arabidopsis. J. Exp. Bot. 68:2603–9 [Google Scholar]
  91. Liu H, Yang H, Wu C, Feng J, Liu X. 91.  et al. 2009. Overexpressing HRS1 confers hypersensitivity to low phosphate-elicited inhibition of primary root growth in Arabidopsis thaliana. J. Integr. Plant Biol 51:382–92 [Google Scholar]
  92. Liu KH, Huang CY, Tsay YF. 92.  1999. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–74 [Google Scholar]
  93. Liu KH, Niu Y, Konishi M, Wu Y, Du H. 93.  et al. 2017. Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature 545:311–16Reveals how calcium regulates CPKs in response to nitrate as a secondary messenger to transmit signals to downstream NLP7. [Google Scholar]
  94. Liu KH, Tsay YF. 94.  2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J 22:1005–13Demonstrates that the dual-affinity transport activity of NPF6.3/CHL1 is mediated by phosphorylation at the Thr101 residue. [Google Scholar]
  95. Liu W, Sun Q, Wang K, Du Q, Li WX. 95.  2017. Nitrogen limitation adaptation (NLA) is involved in source-to-sink remobilization of nitrate by mediating the degradation of NRT1.7 in Arabidopsis. New Phytol 214:734–44 [Google Scholar]
  96. Mandadi KK, Misra A, Ren S, McKnight TD. 96.  2009. BT2, a BTB protein, mediates multiple responses to nutrients, stresses, and hormones in Arabidopsis. Plant Physiol 150:1930–39 [Google Scholar]
  97. Marchive C, Roudier F, Castaings L, Brehaut V, Blondet E. 97.  et al. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4:1713Characterizes NLP7 as a master regulator that binds and regulates numerous nitrate response genes. [Google Scholar]
  98. Medici A, Krouk G. 98.  2014. The primary nitrate response: a multifaceted signalling pathway. J. Exp. Bot. 65:5567–76 [Google Scholar]
  99. Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R. 99.  et al. 2015. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat. Commun. 6:6274 [Google Scholar]
  100. Meng S, Peng JS, He YN, Zhang GB, Yi HY. 100.  et al. 2016. Arabidopsis NRT1.5 mediates the suppression of nitrate starvation-induced leaf senescence by modulating foliar potassium level. Mol. Plant 9:461–70 [Google Scholar]
  101. Mounier E, Pervent M, Ljung K, Gojon A, Nacry P. 101.  2014. 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 Environ 37:162–74 [Google Scholar]
  102. Muños S, Cazettes C, Fizames C, Gaymard F, Tillard P. 102.  et al. 2004. Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell 16:2433–47 [Google Scholar]
  103. Nacry P, Bouguyon E, Gojon A. 103.  2013. Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29 [Google Scholar]
  104. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H. 104.  et al. 2002. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–29 [Google Scholar]
  105. Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jorgensen ME. 105.  et al. 2012. NRT/PTR transporters are essential for translocation of glucosinolate defense compounds to seeds. Nature 488:531–34Identifies NPFs as glucosinolate transporters. [Google Scholar]
  106. Obertello M, Krouk G, Katari MS, Runko SJ, Coruzzi GM. 106.  2010. Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis. BMC Syst. Biol. 4:111 [Google Scholar]
  107. O'Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A. 107.  et al. 2016. Nitrate transport, sensing, and responses in plants. Mol. Plant 9:837–56 [Google Scholar]
  108. O'Connor SE, Maresh JJ. 108.  2006. Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat. Prod. Rep. 23:532–47 [Google Scholar]
  109. Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. 109.  2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3:17029 [Google Scholar]
  110. Okamoto S, Kawaguchi M. 110.  2015. Shoot HAR1 mediates nitrate inhibition of nodulation in Lotus japonicus. Plant Signal. Behav 10:e1000138 [Google Scholar]
  111. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. 111.  2013. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4:2191 [Google Scholar]
  112. Ouyang J, Cai Z, Xia K, Wang Y, Duan J, Zhang M. 112.  2010. Identification and analysis of eight peptide transporter homologs in rice. Plant Sci 179:374–82 [Google Scholar]
  113. Paez-Valencia J, Sanchez-Lares J, Marsh E, Dorneles LT, Santos MP. 113.  et al. 2013. Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in romaine lettuce. Plant Physiol 161:1557–69 [Google Scholar]
  114. Para A, Li Y, Marshall-Colon A, Varala K, Francoeur NJ. 114.  et al. 2014. Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. PNAS 111:10371–76 [Google Scholar]
  115. Parker JL, Newstead S. 115.  2014. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72Together with Reference 143, reveals the protein structure of the nitrate transceptor NPF6.3/NRT1.1. [Google Scholar]
  116. Payne RM, Xu D, Foureau E, Teto Carqueijeiro MI, Oudin A. 116.  et al. 2017. An NPF transporter exports a central monoterpene indole alkaloid intermediate from the vacuole. Nat. Plants 3:16208 [Google Scholar]
  117. Pena PA, Quach T, Sato S, Ge Z, Nersesian N. 117.  et al. 2017. Expression of the maize Dof1 transcription factor in wheat and sorghum. Front. Plant Sci. 8:434 [Google Scholar]
  118. Perchlik M, Tegeder M. 118.  2017. Improving plant nitrogen use efficiency through alteration of amino acid transport processes. Plant Physiol 175:235–47 [Google Scholar]
  119. Pike S, Gao F, Kim MJ, Kim SH, Schachtman DP, Gassmann W. 119.  2014. Members of the NPF3 transporter subfamily encode pathogen-inducible nitrate/nitrite transporters in grapevine and Arabidopsis. Plant Cell Physiol 55:162–70 [Google Scholar]
  120. Qiu D, Hu R, Li Y, Zhang M. 120.  2017. Aromatic dipeptide Trp-Ala can be transported by Arabidopsis peptide transporters AtPTR1 and AtPTR5. Channels 11:283–87 [Google Scholar]
  121. Qu B, He X, Wang J, Zhao Y, Teng W. 121.  et al. 2015. A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiol 167:411–23 [Google Scholar]
  122. Ranathunge K, El-Kereamy A, Gidda S, Bi YM, Rothstein SJ. 122.  2014. AMT1;1 transgenic rice plants with enhanced NH4+ permeability show superior growth and higher yield under optimal and suboptimal NH4+ conditions. J. Exp. Bot. 65:965–79 [Google Scholar]
  123. Remans T, Nacry P, Pervent M, Filleur S, Diatloff E. 123.  et al. 2006. The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. PNAS 103:19206–11 [Google Scholar]
  124. Rentsch D, Laloi M, Rouhara I, Schmelzer E, Delrot S, Frommer WB. 124.  1995. NTR1 encodes a high affinity oligopeptide transporter in Arabidopsis. FEBS Lett 370:264–68 [Google Scholar]
  125. Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutierrez RA. 125.  2015. The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol 169:1397–404Reveals that calcium accumulates in response to nitrate and regulates PNR in calcium-dependent and -independent pathways. [Google Scholar]
  126. Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR. 126.  2009. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21:3567–84 [Google Scholar]
  127. Saito H, Oikawa T, Hamamoto S, Ishimaru Y, Kanamori-Sato M. 127.  et al. 2015. The jasmonate-responsive GTR1 transporter is required for gibberellin-mediated stamen development in Arabidopsis. Nat. Commun 6:6095 [Google Scholar]
  128. Sakakibara H.128.  1997. Partial characterization of the signalling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leaves. Plant Cell Physiol 38:837–43 [Google Scholar]
  129. Sato T, Maekawa S, Konishi M, Yoshioka N, Sasaki Y. 129.  et al. 2017. Direct transcriptional activation of BT genes by NLP transcription factors is a key component of the nitrate response in Arabidopsis. Biochem. Biophys. Res. Commun. 483:380–86 [Google Scholar]
  130. Sawaki N, Tsujimoto R, Shigyo M, Konishi M, Toki S. 130.  et al. 2013. A nitrate-inducible GARP family gene encodes an auto-repressible transcriptional repressor in rice. Plant Cell Physiol 54:506–17 [Google Scholar]
  131. Schauser L, Roussis A, Stiller J, Stougaard J. 131.  1999. A plant regulator controlling development of symbiotic root nodules. Nature 402:191–95 [Google Scholar]
  132. Schauser L, Wieloch W, Stougaard J. 132.  2005. Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J. Mol. Evol 60:229–37 [Google Scholar]
  133. Scheible WR, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M. 133.  1997. Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–98 [Google Scholar]
  134. Schofield RA, Bi YM, Kant S, Rothstein SJ. 134.  2009. Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant Cell Environ 32:271–85 [Google Scholar]
  135. Segonzac C, Boyer JC, Ipotesi E, Szponarski W, Tillard P. 135.  et al. 2007. Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. Plant Cell 19:3760–77 [Google Scholar]
  136. Shrawat AK, Carroll RT, DePauw M, Taylor GJ, Good AG. 136.  2008. Genetic engineering of improved nitrogen use efficiency in rice by the tissue-specific expression of alanine aminotransferase. Plant Biotechnol. J. 6:722–32 [Google Scholar]
  137. Song W, Koh S, Czako M, Marton L, Drenkard E. 137.  et al. 1997. Antisense expression of the peptide transport gene AtPTR2-B delays flowering and arrests seed development in transgenic Arabidopsis plants. Plant Physiol 114:927–35 [Google Scholar]
  138. Song W, Steiner HY, Zhang L, Naider F, Stacey G, Becker JM. 138.  1996. Cloning of a second Arabidopsis peptide transport gene. Plant Physiol 110:171–78 [Google Scholar]
  139. Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M. 139.  2014. Nodule inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. PNAS 111:14607–12 [Google Scholar]
  140. Sueyoshi K, Mitsuyama T, Sugimoto T, Kleinhofs A, Warner RL, Oji Y. 140.  1999. Effects of inhibitors for signaling components on the expression of the genes for nitrate reductase and nitrite reductase in excised barley leaves. Soil Sci. Plant Nutr. 45:1015–19 [Google Scholar]
  141. Sugiura M, Georgescu MN, Takahashi M. 141.  2007. A nitrite transporter associated with nitrite uptake by higher plant chloroplasts. Plant Cell Physiol 48:1022–35 [Google Scholar]
  142. Sun CH, Yu JQ, Hu DG. 142.  2017. Nitrate: a crucial signal during lateral roots development. Front. Plant Sci. 8:485 [Google Scholar]
  143. Sun J, Bankston JR, Payandeh J, Hinds TR, Zagotta WN, Zheng N. 143.  2014. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:73–77Together with Reference 115, reveals the protein structure of the nitrate transceptor NPF6.3/NRT1.1. [Google Scholar]
  144. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 144.  2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46 [Google Scholar]
  145. Tal I, Zhang Y, Jorgensen ME, Pisanty O, Barbosa IC. 145.  et al. 2016. The Arabidopsis NPF3 protein is a GA transporter. Nat. Commun. 7:11486 [Google Scholar]
  146. Tang Z, Chen Y, Chen F, Ji Y, Zhao F-J. 146.  2017. OsPTR7 (OsNPF8.1), a putative peptide transporter in rice, is involved in dimethylarsenate accumulation in rice grain. Plant Cell Physiol 58:904–13 [Google Scholar]
  147. Taochy C, Gaillard I, Ipotesi E, Oomen R, Leonhardt N. 147.  et al. 2015. The Arabidopsis root stele transporter NPF2.3 contributes to nitrate translocation to shoots under salt stress. Plant J 83:466–79 [Google Scholar]
  148. Tong W, Imai A, Tabata R, Shigenobu S, Yamaguchi K. 148.  et al. 2016. Polyamine resistance is increased by mutations in a nitrate transporter gene NRT1.3 (AtNPF6.4) in Arabidopsis thaliana. Front. Plant Sci 7:834 [Google Scholar]
  149. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM. 149.  1993. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–13Isolates the first nitrate transporter, NPF6.3/NRT1.1/CHL1, in higher plants. [Google Scholar]
  150. Urriola J, Rathore KS. 150.  2015. Overexpression of a glutamine synthetase gene affects growth and development in sorghum. Transgenic Res 24:397–407 [Google Scholar]
  151. Vidal EA, Moyano TC, Riveras E, Contreras-Lopez O, Gutierrez RA. 151.  2013. Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. PNAS 110:12840–45 [Google Scholar]
  152. Wang R, Okamoto M, Xing X, Crawford NM. 152.  2003. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132:556–67 [Google Scholar]
  153. Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X. 153.  et al. 2004. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136:2512–22 [Google Scholar]
  154. Wang R, Xing X, Wang Y, Tran A, Crawford NM. 154.  2009. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol 151:472–78 [Google Scholar]
  155. Wang X, Peng F, Li M, Yang L, Li G. 155.  2012. Expression of a heterologous SnRK1 in tomato increases carbon assimilation, nitrogen uptake and modifies fruit development. J. Plant Physiol. 169:1173–82 [Google Scholar]
  156. Wang YY, Tsay YF. 156.  2011. Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–57 [Google Scholar]
  157. Weichert A, Brinkmann C, Komarova NY, Dietrich D, Thor K. 157.  et al. 2012. AtPTR4 and AtPTR6 are differentially expressed, tonoplast-localized members of the peptide transporter/nitrate transporter 1 (PTR/NRT1) family. Planta 235:311–23 [Google Scholar]
  158. Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang NN. 158.  2012. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLOS ONE 7:e37217 [Google Scholar]
  159. Xia X, Fan X, Wei J, Feng H, Qu H. 159.  et al. 2015. Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport. J. Exp. Bot. 66:317–31 [Google Scholar]
  160. Xu N, Wang R, Zhao L, Zhang C, Li Z. 160.  et al. 2016. The Arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. Plant Cell 28:485–504 [Google Scholar]
  161. Yan D, Easwaran V, Chau V, Okamoto M, Ierullo M. 161.  et al. 2016. NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat. Commun 7:13179 [Google Scholar]
  162. Yang T, Hao L, Yao S, Zhao Y, Lu W, Xiao K. 162.  2016. TabHLH1, a bHLH-type transcription factor gene in wheat, improves plant tolerance to Pi and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiol. Biochem. 104:99–113 [Google Scholar]
  163. Yu LH, Wu J, Tang H, Yuan Y, Wang SM. 163.  et al. 2016. Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Sci. Rep. 6:27795 [Google Scholar]
  164. Zhang GB, Yi HY, Gong JM. 164.  2014. The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–98Demonstrates the upstream regulation of nitrate transporters NPF7.2 and NPF7.3 by ethylene/jasmonic acid signaling. [Google Scholar]
  165. Zhang HM, Forde BG. 165.  1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–9 [Google Scholar]
  166. Zheng Y, Drechsler N, Rausch C, Kunze R. 166.  2016. The Arabidopsis nitrate transporter NPF7.3/NRT1.5 is involved in lateral root development under potassium deprivation. Plant Signal. Behav. 11:e1176819 [Google Scholar]
  167. Zhong L, Chen D, Min D, Li W, Xu Z. 167.  et al. 2015. AtTGA4, a bZIP transcription factor, confers drought resistance by enhancing nitrate transport and assimilation in Arabidopsis thaliana. Biochem. Biophys. Res. Commun 457:433–39 [Google Scholar]
  168. Zhou Y, Cai H, Xiao J, Li X, Zhang Q, Lian X. 168.  2009. Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theor. Appl. Genet. 118:1381–90 [Google Scholar]
  169. Zhu C, Fan Q, Wang W, Shen C, Meng X. 169.  et al. 2014. Characterization of a glutamine synthetase gene DvGS2 from Dunaliella viridis and biochemical identification of DvGS2-transgenic Arabidopsis thaliana. Gene 536:407–15 [Google Scholar]
  170. Zhu C, Fan Q, Wang W, Shen C, Wang P. 170.  et al. 2014. Characterization of a glutamine synthetase gene DvGS1 from Dunaliella viridis and investigation of the impact on expression of DvGS1 in transgenic Arabidopsis thaliana. Mol. Biol. Rep 41:477–87 [Google Scholar]
/content/journals/10.1146/annurev-arplant-042817-040056
Loading
/content/journals/10.1146/annurev-arplant-042817-040056
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error