1932

Abstract

The Green Revolution of the 1960s improved crop yields in part through the widespread cultivation of semidwarf plant varieties, which resist lodging but require a high-nitrogen (N) fertilizer input. Because environmentally degrading synthetic fertilizer use underlies current worldwide cereal yields, future agricultural sustainability demands enhanced N use efficiency (NUE). Here, we summarize the current understanding of how plants sense, uptake, and respond to N availability in the model plants that can be used to improve sustainable productivity in agriculture. Recent progress in unlocking the genetic basis of NUE within the broader context of plant systems biology has provided insights into the coordination of plant growth and nutrient assimilation and inspired the implementation of a new breeding strategy to cut fertilizer use in high-yield cereal crops. We conclude that identifying fresh targets for N sensing and response in crops would simultaneously enable improved grain productivity and NUE to launch a new Green Revolution and promote future food security.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070121-015752
2022-05-20
2024-04-17
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-070121-015752.html?itemId=/content/journals/10.1146/annurev-arplant-070121-015752&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alfatih A, Wu J, Zhang Z-S, Xia J-Q, Jan SU et al. 2020. Rice NIN-LIKE PROTEIN 1 rapidly responds to nitrogen deficiency and improves yield and nitrogen use efficiency. J. Exp. Bot. 71:6032–42
    [Google Scholar]
  2. 2.
    Almagro A, Lin SH, Tsay YF. 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]
  3. 3.
    Alvarez JM, Moyano TC, Zhang T, Gras DE, Herrera FJ et al. 2019. Local changes in chromatin accessibility and transcriptional networks underlying the nitrate response in Arabidopsis roots. Mol. Plant 12:1545–60
    [Google Scholar]
  4. 4.
    Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras-López O 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]
  5. 5.
    Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S 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. 6.
    Asano K, Hirano K, Ueguchi-Tanaka M, Angeles-Shim RB, Komura T et al. 2009. Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice. Mol. Genet. Genom. 281:223–31
    [Google Scholar]
  7. 7.
    Barbier FF, Dun EA, Kerr SC, Chabikwa TG, Beveridge CA. 2019. An update on the signals controlling shoot branching. Trends Plant Sci. 24:220–36
    [Google Scholar]
  8. 8.
    Beier MP, Obara M, Taniai A, Sawa Y, Ishizawa J et al. 2018. Lack of ACTPK1, an STY kinase, enhances ammonium uptake and use, and promotes growth of rice seedlings under sufficient external ammonium. Plant J. 93:992–1006
    [Google Scholar]
  9. 9.
    Blanco-Touriñán N, Legris M, Minguet EG, Costigliolo-Rojas C, Nohales MA et al. 2020. COP1 destabilizes DELLA proteins in Arabidopsis. PNAS 117:13792–99
    [Google Scholar]
  10. 10.
    Chandler PM, Harding CA. 2013. ‘Overgrowth’ mutants in barley and wheat: new alleles and phenotypes of the ‘Green Revolution’ Della gene. J. Exp. Bot. 64:1603–13
    [Google Scholar]
  11. 11.
    Chellamuthu VR, Ermilova E, Lapina T, Lüddecke J, Minaeva E et al. 2014. A widespread glutamine-sensing mechanism in the plant kingdom. Cell 159:1188–99
    [Google Scholar]
  12. 12.
    Chen J, Fan X, Qian K, Zhang Y, Song M 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]
  13. 13.
    Chen J, Liu X, Liu S, Fan X, Zhao L et al. 2020. Co-overexpression of OsNAR2.1 and OsNRT2.3a increased agronomic nitrogen use efficiency in transgenic rice plants. Front. Plant Sci. 11:1245
    [Google Scholar]
  14. 14.
    Chen J, Zhang Y, Tan Y, Zhang M, Zhu L 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]
  15. 15.
    Chen KE, Chen HY, Tseng CS, Tsay YF. 2020. Improving nitrogen use efficiency by manipulating nitrate remobilization in plants. Nat. Plants 6:1126–35
    [Google Scholar]
  16. 16.
    Chen X, Yao Q, Gao X, Jiang C, Harberd NP, Fu X. 2016. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26:640–46Reveals that shoot-to-root translocated HY5 coordinates plant growth, carbon fixation, and nitrogen assimilation, maintaining whole-plant balance between carbon and nitrogen.
    [Google Scholar]
  17. 17.
    Corratgé-Faillie C, Lacombe B. 2017. Substrate (un)specificity of Arabidopsis NRT1/PTR FAMILY (NPF) proteins. J. Exp. Bot. 68:3107–13
    [Google Scholar]
  18. 18.
    Fan SC, Lin CS, Hsu PK, Lin SH, Tsay YF. 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]
  19. 19.
    Fan X, Tang Z, Tan Y, Zhang Y, Luo B et al. 2016. Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. PNAS 113:7118–23
    [Google Scholar]
  20. 20.
    Fang Z, Bai G, Huang W, Wang Z, Wang X, Zhang M 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]
  21. 21.
    Fang Z, Xia K, Yang X, Grotemeyer MS, Meier S 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]
  22. 22.
    Fichtner F, Dissanayake IM, Lacombe B, Barbier F. 2021. Sugar and nitrate sensing: a multi-billion-year story. Trends Plant Sci. 26:352–74
    [Google Scholar]
  23. 23.
    Flintham JE, Borner A, Worland AJ, Gale MD. 1997. Optimizing wheat grain yield: effects of Rht (gibberellin-insensitive) dwarfing genes. J. Agric. Sci. 128:11–25
    [Google Scholar]
  24. 24.
    Fox T, DeBruin J, Haug Collet K, Trimnell M, Clapp J et al. 2017. A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnol. J. 15:942–52
    [Google Scholar]
  25. 25.
    Fu X, Richards DE, Ait-ali T, Hynes LW, Ougham H et al. 2002. Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–200
    [Google Scholar]
  26. 26.
    Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP 2004. The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–18
    [Google Scholar]
  27. 27.
    Fu X, Sudhakar D, Peng J, Richards DE, Christou P, Harberd NP 2001. Expression of Arabidopsis GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13:1791–802
    [Google Scholar]
  28. 28.
    Gao Y, Xu Z, Zhang L, Li S, Wang S et al. 2020. MYB61 is regulated by GRF4 and promotes nitrogen utilization and biomass production in rice. Nat. Commun. 11:5219
    [Google Scholar]
  29. 29.
    Gao Z, Wang Y, Chen G, Zhang A, Yang S et al. 2019. The indica nitrate reductase gene OsNR2 allele enhances rice yield potential and nitrogen use efficiency. Nat. Commun. 10:5207Reveals that the elite OsNR2 allele promotes nitrogen uptake via feed-forward regulation of OsNRT1.1B and increases nitrogen use efficiency and rice yield.
    [Google Scholar]
  30. 30.
    Gaudinier A, Rodriguez-Medina J, Zhang L, Olson A, Liseron-Monfils C et al. 2018. Transcriptional regulation of nitrogen-associated metabolism and growth. Nature 563:259–64Provides transcriptional regulatory networks and transcription factors that intergrade and coordinate plant growth and metabolism in response to nitrogen availability.
    [Google Scholar]
  31. 31.
    Gaufichon L, Masclaux-Daubresse C, Tcherkez G, Reisdorf-Cren M, Sakakibara Y et al. 2013. Arabidopsis thaliana ASN2 encoding asparagine synthetase is involved in the control of nitrogen assimilation and export during vegetative growth. Plant Cell Environ. 36:328–42
    [Google Scholar]
  32. 32.
    Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wirén N. 1999. Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–48
    [Google Scholar]
  33. 33.
    Ge M, Wang Y, Liu Y, Jiang L, He B et al. 2020. The NIN-like protein 5 (ZmNLP5) transcription factor is involved in modulating the nitrogen response in maize. Plant J. 102:353–68
    [Google Scholar]
  34. 34.
    Giehl RFH, Laginha AM, Duan F, Rentsch D, Yuan L, von Wirén NA. 2017. A critical role of AMT2;1 in root-to-shoot translocation of ammonium in Arabidopsis. Mol. Plant 10:1449–60
    [Google Scholar]
  35. 35.
    Gooding MJ, Addisu M, Uppal RK, Snape JW, Jones HE. 2012. Effect of wheat dwarfing genes on nitrogen-use efficiency. J. Agric. Sci. 150:3–22
    [Google Scholar]
  36. 36.
    Guan P, Ripoll JJ, Wang R, Vuong L, Bailey-Steinitz LJ et al. 2017. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. PNAS 114:2419–24
    [Google Scholar]
  37. 37.
    Guan P, Wang R, Nacry P, Breton G, Kay SA 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]
  38. 38.
    Han M, Okamoto M, Beatty PH, Rothstein SJ, Good AG. 2015. The genetics of nitrogen use efficiency in crop plants. Annu. Rev. Genet. 49:269–89
    [Google Scholar]
  39. 39.
    Han X, Wu K, Fu X, Liu Q. 2020. Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture. aBIOTECH 1:255–75
    [Google Scholar]
  40. 40.
    He X, Qu B, Li W, Zhao X, Teng W 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]
  41. 41.
    Hedden P. 2003. The genes of the Green Revolution. Trends Genet. 19:5–9
    [Google Scholar]
  42. 42.
    Hirano K, Ueguchi-Tanaka M, Matsuoka M. 2008. GID1-mediated gibberellin signaling in plants. Trends Plant Sci. 13:192–99
    [Google Scholar]
  43. 43.
    Hirano K, Yoshida H, Aya K, Kawamura M, Hayashi M et al. 2017. SMALL ORGAN SIZE 1 and SMALL ORGAN SIZE 2/DWARF AND LOW-TILLERING form a complex to integrate auxin and brassinosteroid signaling in rice. Mol. Plant 10:590–604
    [Google Scholar]
  44. 44.
    Ho CH, Lin SH, Hu HC, Tsay YF. 2009. CHL1 functions as a nitrate sensor in plants. Cell 138:1184–94
    [Google Scholar]
  45. 45.
    Hoque MS, Masle J, Udvardi MK, Ryan PR, Upadhyaya NM 2006. Over-expression of the rice OsAMT11 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammonium nutrition. Funct. Plant Biol. 33:153–63
    [Google Scholar]
  46. 46.
    Hsu P-K, Tsay Y-F. 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]
  47. 47.
    Hu B, Jiang Z, Wang W, Qiu Y, Zhang Z et al. 2019. Nitrate–NRT1.1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat. Plants 5:401–13
    [Google Scholar]
  48. 48.
    Hu B, Wang W, Ou S, Tang J, Li H et al. 2015. Variation in NRT1.1B contributes to nitrate-use divergence between rice subspecies. Nat. Genet. 47:834–38Reveals that introgression of the OsNRT1.1Bindica allele into japonica varieties improves yield and nitrogen use efficiency, with potential application in rice breeding.
    [Google Scholar]
  49. 49.
    Hu M, Zhao X, Liu Q, Hong X, Zhang W et al. 2018. Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol. J. 16:1858–67
    [Google Scholar]
  50. 50.
    Huang NC, Liu KH, Lo HJ, Tsay YF. 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]
  51. 51.
    Huang W, Nie H, Feng F, Wang J, Lu K, Fang Z 2019. Altered expression of OsNPF7.1 and OsNPF7.4 differentially regulates tillering and grain yield in rice. Plant Sci. 283:23–31
    [Google Scholar]
  52. 52.
    Huang X, Qian Q, Liu Z, Sun H, He S et al. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nat. Genet. 41:494–97
    [Google Scholar]
  53. 53.
    Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M et al. 2001. slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010
    [Google Scholar]
  54. 54.
    Iwamoto M, Tagiri A. 2016. MicroRNA-targeted transcription factor gene RDD1 promotes nutrient ion uptake and accumulation in rice. Plant J. 85:466–77
    [Google Scholar]
  55. 55.
    James D, Borphukan B, Fartyal D, Ram B, Singh J et al. 2018. Concurrent overexpression of OsGS1;1 and OsGS2 genes in transgenic rice (Oryza sativa L.): impact on tolerance to abiotic stresses. Front. Plant Sci. 9:786
    [Google Scholar]
  56. 56.
    Ji Y, Huang W, Wu B, Fang Z, Wang X 2020. The amino acid transporter AAP1 mediates growth and grain yield by regulating neutral amino acid uptake and reallocation in Oryza sativa. . J. Exp. Bot. 71:4763–77
    [Google Scholar]
  57. 57.
    Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M 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]
  58. 58.
    Kashiwagi T, Ishimaru K. 2004. Identification and functional analysis of a locus for improvement of lodging resistance in rice. Plant Physiol. 134:676–83
    [Google Scholar]
  59. 59.
    Khush GS. 1999. Green revolution: preparing for the 21st century. Genome 42:646–55
    [Google Scholar]
  60. 60.
    Kiba T, Inaba J, Kudo T, Ueda N, Konishi M et al. 2018. Repression of nitrogen starvation responses by members of the Arabidopsis GARP-type transcription factor NIGT1/HRS1 subfamily. Plant Cell 30:925–45
    [Google Scholar]
  61. 61.
    Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R et al. 2013. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol. 163:1338–52
    [Google Scholar]
  62. 62.
    Konishi M, Yanagisawa S. 2013. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 4:1617
    [Google Scholar]
  63. 63.
    Kronzucker HJ, Kirk GJD, Siddiqi MY, Glass ADM. 1998. Effects of hypoxia on 13NH4+ fluxes in rice roots: kinetics and compartmental analysis. Plant Physiol. 116:581–87
    [Google Scholar]
  64. 64.
    Krouk G, Mirowski P, LeCun Y, Shasha DE, Coruzzi GM. 2010. Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol. 11:R123
    [Google Scholar]
  65. 65.
    Kurai T, Wakayama M, Abiko T, Yanagisawa S, Aoki N, Ohsugi R. 2011. Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnol. J. 9:826–37
    [Google Scholar]
  66. 66.
    Landrein B, Formosa-Jordan P, Malivert A, Schuster C, Melnyk CW et al. 2018. Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. PNAS 115:1382–87
    [Google Scholar]
  67. 67.
    Lanquar V, Loqué D, Hörmann F, Yuan L, Bohner A et al. 2009. Feedback inhibition of ammonium uptake by a phospho-dependent allosteric mechanism in Arabidopsis. Plant Cell 21:3610–22
    [Google Scholar]
  68. 68.
    Lantzouni O, Alkofer A, Falter-Braun P, Schwechheimer C. 2020. GROWTH-REGULATING FACTORS interact with DELLAs and regulate growth in cold stress. Plant Cell 32:1018–34
    [Google Scholar]
  69. 69.
    Lee S, Marmagne A, Park J, Fabien C, Yim Y et al. 2020. Concurrent activation of OsAMT1;2 and OsGOGAT1 in rice leads to enhanced nitrogen use efficiency under nitrogen limitation. Plant J. 103:7–20
    [Google Scholar]
  70. 70.
    Léran S, Edel KH, Pervent M, Hashimoto K, Corratgé-Faillie C 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]
  71. 71.
    Li A, Yang W, Lou X, Liu D, Sun J et al. 2013. Novel natural allelic variations at the Rht-1 loci in wheat. J. Integr. Plant Biol. 55:1026–37
    [Google Scholar]
  72. 72.
    Li C, Tang Z, Wei J, Qu H, Xie Y, Xu G. 2016. The OsAMT1.1 gene functions in ammonium uptake and ammonium−potassium homeostasis over low and high ammonium concentration ranges. J. Genet. Genom. 43:639–49
    [Google Scholar]
  73. 73.
    Li JY, Fu YL, Pike SM, Bao J, Tian W 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]
  74. 74.
    Li S, Tian Y, Wu K, Ye Y, Yu J et al. 2018. Modulating plant growth–metabolism coordination for sustainable agriculture. Nature 560:595–600Indicates that the Green Revolution varieties have poor nitrogen use efficiency and that modulating growth–metabolic coordination improves sustainable productivity in high-yield cereal crops.
    [Google Scholar]
  75. 75.
    Li Y, Ouyang J, Wang Y-Y, Hu R, Xia K 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]
  76. 76.
    Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M 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]
  77. 77.
    Liu K-H, Huang C-Y, Tsay Y-F. 1999. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11:865–74
    [Google Scholar]
  78. 78.
    Liu K-H, Niu Y, Konishi M, Wu Y, Du H et al. 2017. Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545:311–16Highlights an important role of nitrate–CPK10/CPK30/CPK32–NLP7 signaling in regulating plant developmental and metabolic adaptations to nitrate availability.
    [Google Scholar]
  79. 79.
    Liu K-H, Tsay Y-F. 2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22:1005–13
    [Google Scholar]
  80. 80.
    Liu Q, Chen X, Wu K, Fu X 2015. Nitrogen signaling and use efficiency in plants: What's new?. Curr. Opin. Plant Biol. 27:192–98
    [Google Scholar]
  81. 81.
    Liu Q, Han R, Wu K, Zhang J, Ye Y et al. 2018. G-protein βγ subunits determine grain size through interaction with MADS-domain transcription factors in rice. Nat. Commun. 9:852
    [Google Scholar]
  82. 82.
    Liu Q, Wu K, Harberd NP, Fu X. 2021. Green Revolution DELLAs: from translational reinitiation to future sustainable agriculture. Mol. Plant 14:547–49
    [Google Scholar]
  83. 83.
    Liu X, Huang D, Tao J, Miller AJ, Fan X, Xu G 2014. Identification and functional assay of the interaction motifs in the partner protein OsNAR2.1 of the two-component system for high-affinity nitrate transport. New Phytol 204:74–80
    [Google Scholar]
  84. 84.
    Liu Y, Wang H, Jiang Z, Wang W, Xu R et al. 2021. Genomic basis of geographical adaptation to soil nitrogen in rice. Nature 590:600–5Indicates that OsTCP19 enhances rice yield and nitrogen use efficiency, unveiling the genomic basis of geographical adaptation of diverse rice types.
    [Google Scholar]
  85. 85.
    Loqué D, Lalonde S, Looger LL, von Wirén N, Frommer WB. 2007. A cytosolic trans-activation domain essential for ammonium uptake. Nature 446:195–98
    [Google Scholar]
  86. 86.
    Loqué D, Yuan L, Kojima S, Gojon A, Wirth J et al. 2006. Additive contribution of AMT1;1 and AMT1;3 to high-affinity ammonium uptake across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 48:522–34
    [Google Scholar]
  87. 87.
    Luo B, Xu M, Zhao L, Xie P, Chen Y et al. 2020. Overexpression of the high-affinity nitrate transporter OsNRT2.3b driven by different promoters in barley improves yield and nutrient uptake balance. Int. J. Mol. Sci. 21:1320
    [Google Scholar]
  88. 88.
    Maeda Y, Konishi M, Kiba T, Sakuraba Y, Sawaki N et al. 2018. A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat. Commun. 9:1376
    [Google Scholar]
  89. 89.
    Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E et al. 2013. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4:1713
    [Google Scholar]
  90. 90.
    Matsumura H, Shiomi K, Yamamoto A, Taketani Y, Kobayashi N et al. 2020. Hybrid Rubisco with complete replacement of rice Rubisco small subunits by sorghum counterparts confers C4 plant-like high catalytic activity. Mol. Plant 13:1570–81
    [Google Scholar]
  91. 91.
    McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM et al. 2003. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–30
    [Google Scholar]
  92. 92.
    Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R et al. 2015. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat. Commun. 6:6274
    [Google Scholar]
  93. 93.
    Miflin BJ, Habash DZ. 2002. The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J. Exp. Bot. 53:979–87
    [Google Scholar]
  94. 94.
    Mo Y, Pearce S, Dubcovsky J 2018. Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b. BMC Plant Biol 18:253
    [Google Scholar]
  95. 95.
    Muños S, Cazettes C, Fizames C, Gaymard F, Tillard P et al. 2004. Transcript profiling in the chl15 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]
  96. 96.
    Murase K, Hirano Y, Sun T-p, Hakoshima T. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–63
    [Google Scholar]
  97. 97.
    Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jørgensen ME et al. 2012. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488:531–34
    [Google Scholar]
  98. 98.
    Ohashi M, Ishiyama K, Kusano M, Fukushima A, Kojima S et al. 2015. Lack of cytosolic glutamine synthetase1;2 in vascular tissues of axillary buds causes severe reduction in their outgrowth and disorder of metabolic balance in rice seedlings. Plant J 81:347–56
    [Google Scholar]
  99. 99.
    Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3:17029
    [Google Scholar]
  100. 100.
    Oldroyd GED, Leyser O. 2020. A plant's diet, surviving in a variable nutrient environment. Science 368:eaba0196
    [Google Scholar]
  101. 101.
    Ota R, Ohkubo Y, Yamashita Y, Ogawa-Ohnishi M, Matsubayashi Y. 2020. Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis. Nat. Commun. 11:641
    [Google Scholar]
  102. 102.
    Parker JL, Newstead S. 2014. Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507:68–72
    [Google Scholar]
  103. 103.
    Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP et al. 2011. Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–31
    [Google Scholar]
  104. 104.
    Peña PA, Quach T, Sato S, Ge Z, Nersesian N et al. 2017. Expression of the maize Dof1 transcription factor in wheat and sorghum. Front. Plant Sci. 8:434
    [Google Scholar]
  105. 105.
    Peng J, Carol P, Richards DE, King KE, Cowling RJ et al. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–205
    [Google Scholar]
  106. 106.
    Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM et al. 1999.. ‘ Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–61
    [Google Scholar]
  107. 107.
    Perchlik M, Tegeder M. 2017. Improving plant nitrogen use efficiency through alteration of amino acid transport processes. Plant Physiol. 175:235–47
    [Google Scholar]
  108. 108.
    Poitout A, Crabos A, Petrik I, Novak O, Krouk G et al. 2018. Responses to systemic nitrogen signaling in Arabidopsis roots involve trans-zeatin in shoots. Plant Cell 30:1243–57
    [Google Scholar]
  109. 109.
    Qu B, He X, Wang J, Zhao Y, Teng W 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]
  110. 110.
    Ranathunge K, El-Kereamy A, Gidda S, Bi YM, Rothstein SJ. 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]
  111. 111.
    Remans T, Nacry P, Pervent M, Filleur S, Diatloff E 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]
  112. 112.
    Rubin G, Tohge T, Matsuda F, Saito K, Scheible WR. 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]
  113. 113.
    Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM. 2011. Nitrogen economics of root foraging: transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply versus demand. PNAS 108:18524–29
    [Google Scholar]
  114. 114.
    Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A et al. 2002. Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–2
    [Google Scholar]
  115. 115.
    Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K et al. 2003. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–98
    [Google Scholar]
  116. 116.
    Sawaki N, Tsujimoto R, Shigyo M, Konishi M, Toki S 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]
  117. 117.
    Schofield RA, Bi Y-M, Kant S, Rothstein SJ 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]
  118. 118.
    Shen BR, Wang LM, Lin XL, Yao Z, Xu HW et al. 2019. Engineering a new chloroplastic photorespiratory bypass to increase photosynthetic efficiency and productivity in rice. Mol. Plant 12:199–214
    [Google Scholar]
  119. 119.
    Sonoda Y, Ikeda A, Saiki S, von Wiren N, Yamaya T, Yamaguchi J 2003. Distinct expression and function of three ammonium transporter genes (OsAMT1;11;3) in rice. Plant Cell Physiol 44:726–34
    [Google Scholar]
  120. 120.
    Spielmeyer W, Ellis MH, Chandler PM. 2002. Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. PNAS 99:9043–48
    [Google Scholar]
  121. 121.
    Su W, Huber SC, Crawford NM. 1996. Identification in vitro of a post-translational regulatory site in the hinge 1 region of Arabidopsis nitrate reductase. Plant Cell 8:519–27
    [Google Scholar]
  122. 122.
    Sun H, Qian Q, Wu K, Luo J, Wang S et al. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nat. Genet. 46:652–56Characterizes dep1 as a major contributor to enhance yield and nitrogen use efficiency, suggesting that G proteins are required for nitrogen singling.
    [Google Scholar]
  123. 123.
    Sun J, Bankston JR, Payandeh J, Hinds TR, Zagotta WN, Zheng N. 2014. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:73–77
    [Google Scholar]
  124. 124.
    Sun TP, Gubler F. 2004. Molecular mechanism of gibberellin signaling in plants. Annu. Rev. Plant Biol. 55:197–223
    [Google Scholar]
  125. 125.
    Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46Reveals that root-to-shoot translocated CEP peptides mediate systemic nitrate demand signaling to indicate local nitrogen depletion in split-root experiments.
    [Google Scholar]
  126. 126.
    Tal I, Zhang Y, Jørgensen ME, Pisanty O, Barbosa ICR et al. 2016. The Arabidopsis NPF3 protein is a GA transporter. Nat. Commun. 7:11486
    [Google Scholar]
  127. 127.
    Taleski M, Imin N, Djordjevic MA. 2018. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. J. Exp. Bot. 69:1829–36
    [Google Scholar]
  128. 128.
    Tang W, Ye J, Yao X, Zhao P, Xuan W et al. 2019. Genome-wide associated study identifies NAC42-activated nitrate transporter conferring high nitrogen use efficiency in rice. Nat. Commun. 10:5279
    [Google Scholar]
  129. 129.
    Thomsen HC, Eriksson D, Møller IS, Schjoerring JK. 2014. Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency?. Trends Plant Sci 19:656–63
    [Google Scholar]
  130. 130.
    Tong H, Jin Y, Liu W, Li F, Fang J et al. 2009. DWARF AND LOW-TILLERING, a new member of the GRAS family, plays positive roles in brassinosteroid signaling in rice. Plant J. 58:803–16
    [Google Scholar]
  131. 131.
    Tong Y, Zhou JJ, Li Z, Miller AJ 2005. A two-component high-affinity nitrate uptake system in barley. Plant J 41:442–50
    [Google Scholar]
  132. 132.
    Tsay YF, Ho CH, Chen HY, Lin SH 2011. Integration of nitrogen and potassium signaling. Annu. Rev. Plant Biol. 62:207–26
    [Google Scholar]
  133. 133.
    Tsay YF, Schroeder JI, Feldmann KA, Crawford NM. 1993. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72:705–13
    [Google Scholar]
  134. 134.
    Ueda Y, Kiba T, Yanagisawa S. 2020. Nitrate-inducible NIGT1 proteins modulate phosphate uptake and starvation signalling via transcriptional regulation of SPX genes. Plant J 102:448–66
    [Google Scholar]
  135. 135.
    Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E et al. 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–98
    [Google Scholar]
  136. 136.
    Van De Velde K, Chandler PM, Van Der Straeten D, Rohde A. 2017. Differential coupling of gibberellin responses by Rht-B1c suppressor alleles and Rht-B1b in wheat highlights a unique role for the DELLA N-terminus in dormancy. J. Exp. Bot. 68:443–55
    [Google Scholar]
  137. 137.
    Van De Velde K, Thomas SG, Heyse F, Kaspar R, Van Der Straeten D, Rohde A 2021. N-terminal truncated RHT-1 proteins generated by translational reinitiation cause semi-dwarfing of wheat Green Revolution alleles. Mol. Plant 14:679–87Indicates that the Green Revolution wheat genes Rht-B1b and Rht-D1b encode N-terminally truncated DELLA proteins through translational reinitiation.
    [Google Scholar]
  138. 138.
    Vidal EA, Alvarez JM, Araus V, Riveras E, Brooks MD et al. 2020. Nitrate in 2020: thirty years from transport to signaling networks. Plant Cell 32:2094–119
    [Google Scholar]
  139. 139.
    Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ. 1987. Barley mutants lacking chloroplast glutamine synthetase—biochemical and genetic analysis. Plant Physiol 83:155–58
    [Google Scholar]
  140. 140.
    Wang P, Du Y, Li Y, Ren D, Song CP 2010. Hydrogen peroxide–mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–98
    [Google Scholar]
  141. 141.
    Wang Q, Nian J, Xie X, Yu H, Zhang J et al. 2018. Genetic variations in ARE1 mediate grain yield by modulating nitrogen utilization in rice. Nat. Commun. 9:735
    [Google Scholar]
  142. 142.
    Wang Q, Su Q, Nian J, Zhang J, Guo M et al. 2021. The Ghd7 transcription factor represses ARE1 expression to enhance nitrogen utilization and grain yield in rice. Mol. Plant. 14:1012–23
    [Google Scholar]
  143. 143.
    Wang W, Hu B, Yuan D, Liu Y, Che R et al. 2018. Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. Plant Cell 30:638–51
    [Google Scholar]
  144. 144.
    Wang X, Wang HF, Chen Y, Sun MM, Wang Y, Chen YF 2020. The transcription factor NIGT1.2 modulates both phosphate uptake and nitrate influx during phosphate starvation in Arabidopsis and maize. Plant Cell 32:3519–34
    [Google Scholar]
  145. 145.
    Wang YY, Cheng YH, Chen KE, Tsay YF. 2018. Nitrate transport, signaling, and use efficiency. Annu. Rev. Plant Biol. 69:85–122
    [Google Scholar]
  146. 146.
    Wang YY, Hsu PK, Tsay YF. 2012. Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–67
    [Google Scholar]
  147. 147.
    Wang YY, Tsay YF. 2011. Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. Plant Cell 23:1945–57
    [Google Scholar]
  148. 148.
    Wei J, Zheng Y, Feng H, Qu H, Fan X et al. 2018. OsNRT2.4 encodes a dual-affinity nitrate transporter and functions in nitrate-regulated root growth and nitrate distribution in rice. J. Exp. Bot. 69:1095–107
    [Google Scholar]
  149. 149.
    Wen Z, Tyerman SD, Dechorgnat J, Ovchinnikova E, Dhugga KS, Kaiser BN. 2017. Maize NPF6 proteins are homologs of Arabidopsis CHL1 that are selective for both nitrate and chloride. Plant Cell 29:2581–96
    [Google Scholar]
  150. 150.
    Wu J, Zhang Z-S, Xia J-Q, Alfatih A, Song Y et al. 2021. Rice NIN-LIKE PROTEIN 4 plays a pivotal role in nitrogen use efficiency. Plant Biotechnol. J. 19:448–61
    [Google Scholar]
  151. 151.
    Wu K, Wang S, Song W, Zhang J, Wang Y et al. 2020. Enhanced sustainable green revolution yield via nitrogen-responsive chromatin modulation in rice. Science 367:eaaz2046Indicates that NGR5 enhances nitrogen use efficiency and explains increased tillering of semidwarf plant varieties through gibberellin-dependent and nitrogen-responsive chromatin modulation.
    [Google Scholar]
  152. 152.
    Wu K, Xu H, Gao X, Fu X. 2021. New insights into gibberellin signaling in regulating plant growth–metabolic coordination. Curr. Opin. Plant Biol. 63:102074
    [Google Scholar]
  153. 153.
    Wu Z, Tang D, Liu K, Miao C, Zhuo X et al. 2018. Characterization of a new semi-dominant dwarf allele of SLR1 and its potential application in hybrid rice breeding. J. Exp. Bot. 69:4703–13
    [Google Scholar]
  154. 154.
    Xia X, Fan X, Wei J, Feng H, Qu H 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]
  155. 155.
    Xie W, Wang G, Yuan M, Yao W, Lyu K et al. 2015. Breeding signatures of rice improvement revealed by a genomic variation map from a large germplasm collection. PNAS 112:5411–19
    [Google Scholar]
  156. 156.
    Xu G, Chen W, Song L, Chen Q, Zhang H et al. 2019. FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in response to the carbon/nitrogen ratio. J. Exp. Bot. 70:6375–88
    [Google Scholar]
  157. 157.
    Xu G, Fan X, Miller AJ 2012. Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63:153–82
    [Google Scholar]
  158. 158.
    Xu X, Wu K, Xu R, Yu J, Wang J et al. 2019. Pyramiding of the dep11 and NAL1NJ6 alleles achieves sustainable improvements in nitrogen-use efficiency and grain yield in japonica rice breeding. J. Genet. Genom. 46:325–28
    [Google Scholar]
  159. 159.
    Xuan YH, Priatama RA, Huang J, Je BI, Liu JM et al. 2013. Indeterminate domain 10 regulates ammonium-mediated gene expression in rice roots. New Phytol 197:791–804
    [Google Scholar]
  160. 160.
    Yan M, Fan X, Feng H, Miller AJ, Shen Q, Xu G. 2011. Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant Cell Environ 34:1360–72
    [Google Scholar]
  161. 161.
    Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T. 2004. Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. PNAS 101:7833–38
    [Google Scholar]
  162. 162.
    Yang J, Wang M, Li W, He X, Teng W et al. 2019. Reducing expression of a nitrate-responsive bZIP transcription factor increases grain yield and N use in wheat. Plant Biotechnol. J. 17:1823–33
    [Google Scholar]
  163. 163.
    Yang L, Xu M, Koo Y, He J, Poethig RS 2013. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2:e00260
    [Google Scholar]
  164. 164.
    Yang X, Nian J, Xie Q, Feng J, Zhang F et al. 2016. Rice ferredoxin-dependent glutamate synthase regulates nitrogen–carbon metabolomes and is genetically differentiated between japonica and indica subspecies. Mol. Plant 9:1520–34
    [Google Scholar]
  165. 165.
    Yasuda S, Aoyama S, Hasegawa Y, Sato T, Yamaguchi J. 2017. Arabidopsis CBL-interacting protein kinases regulate carbon/nitrogen-nutrient response by phosphorylating ubiquitin ligase ATL31. Mol. Plant 10:605–18
    [Google Scholar]
  166. 166.
    Yasuda S, Sato T, Maekawa S, Aoyama S, Fukao Y, Yamaguchi J. 2014. Phosphorylation of Arabidopsis ubiquitin ligase ATL31 is critical for plant carbon/nitrogen nutrient balance response and controls the stability of 14-3-3 proteins. J. Biol. Chem. 289:15179–93
    [Google Scholar]
  167. 167.
    Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP 2007. Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr. Biol. 17:1225–30
    [Google Scholar]
  168. 168.
    Yu J, Xuan W, Tian Y, Fan L, Sun J et al. 2021. Enhanced OsNLP4-OsNiR cascade confers nitrogen use efficiency by promoting tiller number in rice. Plant Biotechnol. J. 19:167–76
    [Google Scholar]
  169. 169.
    Yuan L, Graff L, Loqué D, Kojima S, Tsuchiya YN et al. 2009. AtAMT1;4, a pollen-specific high-affinity ammonium transporter of the plasma membrane in Arabidopsis. Plant Cell Physiol. 50:13–25
    [Google Scholar]
  170. 170.
    Yuan L, Loqué D, Kojima S, Rauch S, Ishiyama K et al. 2007. The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–52
    [Google Scholar]
  171. 171.
    Yuan L, Loqué D, Ye F, Frommer WB, von Wirén N. 2007. Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol 143:732–44
    [Google Scholar]
  172. 172.
    Zhang HM, Forde BG. 1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–9
    [Google Scholar]
  173. 173.
    Zhang J, Fengler KA, Van Hemert JL, Gupta R, Mongar N et al. 2019. Identification and characterization of a novel stay-green QTL that increases yield in maize. Plant Biotechnol. J. 17:2272–85
    [Google Scholar]
  174. 174.
    Zhang J, Liu YX, Zhang N, Hu B, Jin T et al. 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37:676–84Reveals that an indicaOsNRT1.1B variant is associated with increasing diverse bacterial taxa and enriching genera with nitrogen metabolism functions.
    [Google Scholar]
  175. 175.
    Zhang K, Novak O, Wei Z, Gou M, Zhang X et al. 2014. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 5:3274
    [Google Scholar]
  176. 176.
    Zhang M, Wang Y, Chen X, Xu F, Ding M et al. 2021. Plasma membrane H+-ATPase overexpression increases rice yield via simultaneous enhancement of nutrient uptake and photosynthesis. Nat. Commun. 12:735
    [Google Scholar]
  177. 177.
    Zhang S, Zhu L, Shen C, Ji Z, Zhang H et al. 2021. Natural allelic variation in a modulator of auxin homeostasis improves grain yield and nitrogen use efficiency in rice. Plant Cell 33:566–80
    [Google Scholar]
  178. 178.
    Zhang X, Cui Y, Yu M, Su B, Gong W et al. 2019. Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth. Plant Physiol. 181:480–98
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-070121-015752
Loading
/content/journals/10.1146/annurev-arplant-070121-015752
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • 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