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Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling

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Abstract

Nitrogen (N) is one of the most important essential macro-elements for plant growth and development, and nitrate represents the most abundant inorganic form of N in soils. The nitrate uptake and assimilation processes are finely tuned according to the available nitrate in the surroundings as well as by the internal finely coordinated signaling pathways. The NIN-like proteins (NLPs) harbor both RWP-RK, and Phox and Bem1 (PB1) domains, and they belong to the well-characterized plant-specific RWP-RK transcription factor gene family. NLPs are known to be involved in the nitrate signaling pathway by activating downstream target genes, and thus they are implicated in the primary nitrate response in the nucleus via their RWP-RK domains. The PB1 domain is a ubiquitous protein–protein interaction domain and it comprises another regulatory layer for NLPs via the protein interactions within NLPs or with other essential components. Recently, Ca2+–Ca2+ sensor protein kinase–NLP signaling cascades have been identified and they allow NLPs to have central roles in mediating the nitrate signaling pathway. NLPs play essential roles in many aspects of plant growth and development via the finely tuned nitrate signaling pathway. Furthermore, recent studies have highlighted the emerging roles played by NLPs in the N starvation response, nodule formation in legumes, N and P interactions, and root cap release in higher plants. In this review, we consider recent advances in the identification, evolution, molecular characteristics, and functions of the NLP gene family in plant growth and development.

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References

  1. Mu X, Chen Q, Chen F, Yuan L, Mi G (2016) Within-leaf nitrogen allocation in adaptation to low nitrogen supply in maize during grain-filling stage. Front Plant Sci 7:699

    Article  PubMed  PubMed Central  Google Scholar 

  2. Mu X, Chen Q, Chen F, Yuan L, Mi G (2017) A RNA-seq analysis of the response of photosynthetic system to low nitrogen supply in maize leaf. Int J Mol Sci 18:2624

    Article  CAS  PubMed Central  Google Scholar 

  3. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105:1141–1157

    Article  PubMed  PubMed Central  Google Scholar 

  4. Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53

    Article  PubMed  Google Scholar 

  5. Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mu X, Chen Q, Chen F, Yuan L, Mi G (2018) Dynamic remobilization of leaf nitrogen components in relation to photosynthetic rate during grain filling in maize. Plant Physiol Biochem 129:27–34

    Article  CAS  PubMed  Google Scholar 

  7. Yang L, Cao W, Thorup-Kristensen K, Bai J, Gao S, Chang D (2015) Effect of Orychophragmus violaceus incorporation on nitrogen uptake in succeeding maize. Plant Soil Environ 61:260–265

    Article  CAS  Google Scholar 

  8. Ibarra-Henríquez C, Fredes I, Álvarez JM, Undurraga SF, Gutiérrez RA (2017) Nitrate signaling and early responses in Arabidopsis roots. J Exp Bot 68:2541–2551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Luo J, Zhou J-J, Masclaux-Daubresse C, Wang N, Wang H, Zheng B (2019) Morphological and physiological responses to contrasting nitrogen regimes in Populus cathayana is linked to resources allocation and carbon/nitrogen partition. Environ Exp Bot 162:247–255

    Article  CAS  Google Scholar 

  10. Mu X, Chen Q, Wu X, Chen F, Yuan L, Mi G (2018) Gibberellins synthesis is involved in the reduction of cell flux and elemental growth rate in maize leaf under low nitrogen supply. Environ Exp Bot 150:198–208

    Article  CAS  Google Scholar 

  11. Mueller ND, West PC, Gerber JS, MacDonald GK, Polasky S, Foley JA (2014) A tradeoff frontier for global nitrogen use and cereal production. Environ Res Lett 9:054002

    Article  CAS  Google Scholar 

  12. Wan T, Xue H, Y-P Tong (2017) Transgenic approaches for improving use efficiency of nitrogen, phosphorus and potassium in crops. J Integr Agric 16:2657–2673

    Article  Google Scholar 

  13. Chen Q, Soulay F, Saudemont B, Elmayan T, Marmagne A, Masclaux-Daubresse C (2019) Overexpression of ATG8 in Arabidopsis stimulates autophagic activity and increases nitrogen remobilization efficiency and grain filling. Plant Cell Physiol 60:343–352

    Article  PubMed  Google Scholar 

  14. Mandal VK, Sharma N, Raghuram N (2018) Molecular targets for improvement of crop nitrogen use efficiency: current and emerging options. Engineering nitrogen utilization in crop plants. Springer, New York, pp 77–93

    Google Scholar 

  15. Mu X, Chen F, Wu Q, Chen Q, Wang J, Yuan L, Mi G (2015) Genetic improvement of root growth increases maize yield via enhanced post-silking nitrogen uptake. Eur J Agron 63:55–61

    Article  CAS  Google Scholar 

  16. Luo J, Zhou J-J (2019) Growth performance, photosynthesis, and root characteristics are associated with nitrogen use efficiency in six poplar species. Environ Exp Bot 164:40–51

    Article  CAS  Google Scholar 

  17. Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122

    Article  CAS  PubMed  Google Scholar 

  18. Camargo A, Llamas Á, Schnell RA, Higuera JJ, González-Ballester D, Lefebvre PA, Fernández E, Galván A (2007) Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19:3491–3503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fredes I, Moreno S, Díaz FP, Gutiérrez RA (2019) Nitrate signaling and the control of Arabidopsis growth and development. Curr Opin Plant Biol 47:112–118

    Article  CAS  PubMed  Google Scholar 

  20. Armijo G, Gutiérrez RA (2017) Emerging players in the nitrate signaling pathway. Mol Plant 10:1019–1022

    Article  CAS  PubMed  Google Scholar 

  21. Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA (2015) The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol 169:1397–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Xu N, Wang R, Zhao L, Zhang C, Li Z, Lei Z, Liu F, Guan P, Chu Z, Crawford NM (2016) The Arabidopsis NRG2 protein mediates nitrate signaling and interacts with and regulates key nitrate regulators. Plant Cell 28:485–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhao L, Zhang W, Yang Y, Li Z, Li N, Qi S, Crawford NM, Wang Y (2018) The Arabidopsis NLP7 gene regulates nitrate signaling via NRT1.1–dependent pathway in the presence of ammonium. Sci Rep 8:1487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195

    Article  CAS  PubMed  Google Scholar 

  25. Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237

    Article  CAS  PubMed  Google Scholar 

  26. Yokota K, Hayashi M (2011) Function and evolution of nodulation genes in legumes. Cell Mol Life Sci 68:1341–1351

    Article  CAS  PubMed  Google Scholar 

  27. Chardin C, Girin T, Roudier F, Meyer C, Krapp A (2014) The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. J Exp Bot 65:5577–5587

    Article  CAS  PubMed  Google Scholar 

  28. Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4:1617

    Article  CAS  PubMed  Google Scholar 

  29. Kumar A, Batra R, Gahlaut V, Gautam T, Kumar S, Sharma M, Tyagi S, Singh KP, Balyan HS, Pandey R, Gupta PK (2018) Genome-wide identification and characterization of gene family for RWP-RK transcription factors in wheat (Triticum aestivum L.). PLoS One 13:e0208409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Konishi M, Yanagisawa S (2014) Emergence of a new step towards understanding the molecular mechanisms underlying nitrate-regulated gene expression. J Exp Bot 65:5589–5600

    Article  CAS  PubMed  Google Scholar 

  31. Konishi M, Yanagisawa S (2019) The role of protein–protein interactions mediated by the PB1 domain of NLP transcription factors in nitrate-inducible gene expression. BMC Plant Biol 19:90

    Article  PubMed  PubMed Central  Google Scholar 

  32. K-H Liu, Niu Y, Konishi M, Wu Y, Du H, Chung HS, Li L, Boudsocq M, McCormack M, Maekawa S (2017) Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545(7654):311–316

    Article  CAS  Google Scholar 

  33. Zhao L, Liu F, Crawford N, Wang Y (2018) Molecular regulation of nitrate responses in plants. Int J Mol Sci 19:2039

    Article  CAS  PubMed Central  Google Scholar 

  34. Guan P, Ripoll J-J, Wang R, Vuong L, Bailey-Steinitz LJ, Ye D, Crawford NM (2017) Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proc Natl Acad Sci USA 114:2419–2424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gaudinier A, Rodriguez-Medina J, Zhang L, Olson A, Liseron-Monfils C, Bågman A-M, Foret J, Abbitt S, Tang M, Li B (2018) Transcriptional regulation of nitrogen-associated metabolism and growth. Nature 563:259–264

    Article  CAS  PubMed  Google Scholar 

  36. Marchive C, Roudier F, Castaings L, Bréhaut V, Blondet E, Colot V, Meyer C, Krapp A (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4:1713

    Article  CAS  PubMed  Google Scholar 

  37. Guan P, Wang R, Nacry P, Breton G, Kay SA, Pruneda-Paz JL, Davani A, Crawford NM (2014) Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc Natl Acad Sci USA 111:15267–15272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Maeda Y, Konishi M, Kiba T, Sakuraba Y, Sawaki N, Kurai T, Ueda Y, Sakakibara H, Yanagisawa S (2018) A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat Commun 9:1376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yu L-H, Wu J, Tang H, Yuan Y, Wang S-M, Wang Y-P, Zhu Q-S, Li S-G, Xiang C-B (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R, Gojon A, Crawford NM, Ruffel S, Coruzzi GM, Krouk G (2015) AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat Commun 6:6274

    Article  CAS  PubMed  Google Scholar 

  41. Karve R, Suárez-Román F, Iyer-Pascuzzi AS (2016) The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release. Plant Physiol 171:2101–2111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wang Z, Zhang L, Sun C, Gu R, Mi G, Yuan L (2018) Phylogenetic, expression and functional characterizations of the maize NLP transcription factor family reveal a role in nitrate assimilation and signaling. Physiol Plant 163:269–281

    Article  CAS  Google Scholar 

  43. Cao H, Qi S, Sun M, Li Z, Yang Y, Crawford NM, Wang Y (2017) Overexpression of the maize ZmNLP6 and ZmNLP8 can complement the Arabidopsis nitrate regulatory mutant nlp7 by restoring nitrate signaling and assimilation. Front Plant Sci 8:1703

    Article  PubMed  PubMed Central  Google Scholar 

  44. Liu M, Chang W, Fan Y et al (2018) Genome-wide identification and characterization of NODULE-INCEPTION-Like Protein (NLP) family genes in Brassica napus. Int J Mol Sci 19:2270

    Article  CAS  PubMed Central  Google Scholar 

  45. Ge M, Liu Y, Jiang L, Wang Y, Lv Y, Zhou L, Liang S, Bao H, Zhao H (2018) Genome-wide analysis of maize NLP transcription factor family revealed the roles in nitrogen response. Plant Growth Regul 84:95–105

    Article  CAS  Google Scholar 

  46. Koi S, Hisanaga T, Sato K, Shimamura M, Yamato KT, Ishizaki K, Kohchi T, Nakajima K (2016) An evolutionarily conserved plant RKD factor controls germ cell differentiation. Curr Biol 26:1775–1781

    Article  CAS  PubMed  Google Scholar 

  47. Luo J, Zhou J-J, Zhang J-Z (2018) Aux/IAA gene family in plants: molecular structure, regulation, and function. Int J Mol Sci 19:259

    Article  CAS  PubMed Central  Google Scholar 

  48. Zhou J-J, Luo J (2018) The PIN-FORMED auxin efflux carriers in plants. Int J Mol Sci 19:2759

    Article  CAS  PubMed Central  Google Scholar 

  49. Luo J, Liang Z, Wu M, Mei L (2019) Genome-wide identification of BOR genes in poplar and their roles in response to various environmental stimuli. Environ Exp Bot 164:101–113

    Article  CAS  Google Scholar 

  50. Worden AZ, Lee J-H, Mock T, Rouzé P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324:268–272

    Article  CAS  PubMed  Google Scholar 

  51. Derelle E, Ferraz C, Rombauts S, Rouzé P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynié S, Cooke R (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35

    Article  CAS  Google Scholar 

  53. Iorizzo M, Ellison S, Senalik D et al (2016) A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution. Nat Genet 48:657–666

    Article  CAS  PubMed  Google Scholar 

  54. Li F, Fan G, Lu C et al (2015) Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33:524–530

    Article  CAS  PubMed  Google Scholar 

  55. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  56. Wang Z, Hobson N, Galindo L et al (2012) The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J 72:461–473

    Article  CAS  PubMed  Google Scholar 

  57. Badouin H, Gouzy J, Grassa CJ et al (2017) The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546:148–152

    Article  CAS  PubMed  Google Scholar 

  58. Suzuki W, Konishi M, Yanagisawa S (2013) The evolutionary events necessary for the emergence of symbiotic nitrogen fixation in legumes may involve a loss of nitrate responsiveness of the NIN transcription factor. Plant Signal Behav 8:e25975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Chase MW, Christenhusz M, Fay M, Byng J, Judd WS, Soltis D, Mabberley D, Sennikov A, Soltis PS, Stevens PF (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Article  Google Scholar 

  60. Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR (2015) HMMER web server: 2015 update. Nucleic Acids Res 43:W30–W38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR (2016) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ho YSJ, Burden LM, Hurley JH (2000) Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor. EMBO J 19:5288–5299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Niemann V, Koch-Singenstreu M, Neu A, Nilkens S, Götz F, Unden G, Stehle T (2014) The NreA protein functions as a nitrate receptor in the Staphylococcal nitrate regulation system. J Mol Biol 426:1539–1553

    Article  CAS  PubMed  Google Scholar 

  64. Shi R, McDonald L, Cygler M, Ekiel I (2014) Coiled-coil helix rotation selects repressing or activating state of transcriptional regulator DhaR. Structure 22:478–487

    Article  CAS  PubMed  Google Scholar 

  65. Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Soyano T, Shimoda Y, Hayashi M (2015) NODULE INCEPTION antagonistically regulates gene expression with nitrate in Lotus japonicus. Plant Cell Physiol 56:368–376

    Article  CAS  PubMed  Google Scholar 

  67. Korasick DA, Chatterjee S, Tonelli M, Dashti H, Lee SG, Westfall CS, Fulton DB, Andreotti AH, Amarasinghe GK, Strader LC (2015) Defining a two-pronged structural model for PB1 (Phox/Bem1p) domain interaction in plant auxin responses. J Biol Chem 290:12868–12878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Sumimoto H, Kamakura S, Ito T (2007) Structure and function of the PB1 domain, a protein interaction module conserved in animals, fungi, amoebas, and plants. Sci STKE 2007:re6

    Article  PubMed  Google Scholar 

  69. Lin J-S, Li X, Luo ZL, Mysore KS, Wen J, Xie F (2018) NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula. Nat Plants 4:942–952

    Article  CAS  PubMed  Google Scholar 

  70. Deng M, Moureaux T, Caboche M (1989) Tungstate, a molybdate analog inactivating nitrate reductase, deregulates the expression of the nitrate reductase structural gene. Plant Physiol 91:304–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Gowri G, Kenis JD, Ingemarsson B, Redinbaugh MG, Campbell WH (1992) Nitrate reductase transcript is expressed in the primary response of maize to environmental nitrate. Plant Mol Biol 18:55–64

    Article  CAS  PubMed  Google Scholar 

  72. Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194

    Article  CAS  PubMed  Google Scholar 

  73. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57:264–278

    Article  CAS  PubMed  Google Scholar 

  74. Krouk G (2017) Nitrate signalling: calcium bridges the nitrate gap. Nat Plants 3:17095

    Article  CAS  PubMed  Google Scholar 

  75. Konishi M, Yanagisawa S (2013) An NLP-binding site in the 3’flanking region of the nitrate reductase gene confers nitrate-inducible expression in Arabidopsis thaliana (L.) Heynh. Soil Sci Plant Nutr 59:612–620

    Article  CAS  Google Scholar 

  76. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409

    Article  CAS  PubMed  Google Scholar 

  77. Rubin G, Tohge T, Matsuda F, Saito K, Scheible W-R (2009) Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21:3567–3584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Gojon A, Nacry P, Davidian J-C (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Curr Opin Plant Biol 12:328–338

    Article  CAS  PubMed  Google Scholar 

  79. Vidal EA, Álvarez JM, Moyano TC, Gutiérrez RA (2015) Transcriptional networks in the nitrate response of Arabidopsis thaliana. Curr Opin Plant Biol 27:125–132

    Article  CAS  PubMed  Google Scholar 

  80. Para A, Li Y, Marshall-Colón A, Varala K, Francoeur NJ, Moran TM, Edwards MB, Hackley C, Bargmann BO, Birnbaum KD (2014) Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. Proc Natl Acad Sci USA 111:10371–10376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Jian S, Liao Q, Song H, Liu Q, Lepo JE, Guan C, Zhang J, Ismail AM, Zhang Z (2018) NRT1.1-related NH4 + toxicity is associated with a disturbed balance between NH4 + uptake and assimilation. Plant Physiol 178:1473–1488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Luo J, Qin J, He F, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013) Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta 237:919–931

    Article  CAS  PubMed  Google Scholar 

  83. Hachiya T, Sakakibara H (2016) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants. J Exp Bot 68:2501–2512

    Google Scholar 

  84. Araus V, Vidal EA, Puelma T, Alamos S, Mieulet D, Guiderdoni E, Gutiérrez RA (2016) Members of BTB gene family of scaffold proteins suppress nitrate uptake and nitrogen use efficiency. Plant Physiol 171:1523–1532

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Sato T, Maekawa S, Konishi M, Yoshioka N, Sasaki Y, Maeda H, Ishida T, Kato Y, Yamaguchi J, Yanagisawa S (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 483:380–386

    Article  CAS  PubMed  Google Scholar 

  86. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6:e1001102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Menz J, Li Z, Schulze WX, Ludewig U (2016) Early nitrogen-deprivation responses in Arabidopsis roots reveal distinct differences on transcriptome and (phospho-) proteome levels between nitrate and ammonium nutrition. Plant J 88:717–734

    Article  CAS  PubMed  Google Scholar 

  88. Liu H, Yang H, Wu C, Feng J, Liu X, Qin H, Wang D (2009) Overexpressing HRS1 confers hypersensitivity to low phosphate-elicited inhibition of primary root growth in Arabidopsis thaliana. J Integr Plant Biol 51:382–392

    Article  CAS  PubMed  Google Scholar 

  89. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57:426–435

    Article  CAS  PubMed  Google Scholar 

  90. Guo F-Q, Young J, Crawford NM (2003) The nitrate transporter AtNRT1. 1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis. Plant Cell 15:107–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Yan D, Easwaran V, Chau V, Okamoto M, Ierullo M, Kimura M, Endo A, Yano R, Pasha A, Gong Y (2016) NIN-like protein 8 is a master regulator of nitrate-promoted seed germination in Arabidopsis. Nat Commun 7:13179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Wang W, Hu B, Yuan D, Liu Y, Che R, Hu Y, Ou S, Liu Y, Zhang Z, Wang H (2018) Expression of the nitrate transporter gene OsNRT1.1A/OsNPF6.3 confers high yield and early maturation in rice. Plant Cell 30:638–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144:324–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Vernié T, Kim J, Frances L, Ding Y, Sun J, Guan D, Niebel A, Gifford ML, de Carvalho-Niebel F, Oldroyd GE (2015) The NIN transcription factor coordinates diverse nodulation programs in different tissues of the Medicago truncatula root. Plant Cell 27:3410–3424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Liu C-W, Breakspear A, Guan D, Cerri MR, Abbs K, Jiang S, Robson FC, Radhakrishnan G, Roy S, Bone C (2019) NIN acts as a network hub controlling a growth module required for rhizobial infection. Plant Physiol 179:1704–1722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Liu J, Rutten L, Limpens E, van der Molen T, van Velzen R, Chen R, Chen Y, Geurts R, Kohlen W, Kulikova O (2019) A remote cis-regulatory region is required for NIN expression in the pericycle to initiate nodule primordium formation in Medicago truncatula. Plant Cell 31:68–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Nishida H, Tanaka S, Handa Y, Ito M, Sakamoto Y, Matsunaga S, Betsuyaku S, Miura K, Soyano T, Kawaguchi M (2018) A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus. Nat Commun 9:499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Nishida H, Suzaki T (2018) Two negative regulatory systems of root nodule symbiosis: how are symbiotic benefits and costs balanced? Plant Cell Physiol 59:1733–1738

    Article  CAS  PubMed  Google Scholar 

  100. Nishida H, Suzaki T (2018) Nitrate-mediated control of root nodule symbiosis. Curr Opin Plant Biol 44:129–136

    Article  CAS  PubMed  Google Scholar 

  101. Clavijo F, Diedhiou I, Vaissayre V, Brottier L, Acolatse J, Moukouanga D, Crabos A, Auguy F, Franche C, Gherbi H (2015) The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals. New Phytol 208:887–903

    Article  CAS  PubMed  Google Scholar 

  102. Chabaud M, Gherbi H, Pirolles E, Vaissayre V, Fournier J, Moukouanga D, Franche C, Bogusz D, Tisa LS, Barker DG (2016) Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209(1):86–93

    Article  CAS  PubMed  Google Scholar 

  103. Cissoko M, Hocher V, Gherbi H et al (2018) Actinorhizal signaling molecules: Frankia root hair deforming factor shares properties with NIN inducing factor. Front Plant Sci 9:1494

    Article  PubMed  PubMed Central  Google Scholar 

  104. Karve RA, Iyer-Pascuzzi AS (2018) Further insights into the role of NIN-LIKE PROTEIN 7 (NLP7) in root cap cell release. Plant Signal Behav 13:e1414122

    Article  CAS  PubMed  Google Scholar 

  105. Luo J, Xia W, Cao P, Za Xiao, Zhang Y, Liu M, Zhan C, Wang N (2019) Integrated transcriptome analysis reveals plant hormones jasmonic acid and salicylic acid coordinate growth and defense responses upon fungal infection in poplar. Biomolecules 9:12

    Article  CAS  PubMed Central  Google Scholar 

  106. Gutiérrez RA (2012) Systems biology for enhanced plant nitrogen nutrition. Science 336:1673–1675

    Article  CAS  PubMed  Google Scholar 

  107. Ueda Y, Yanagisawa S (2019) Delineation of nitrogen signaling networks: computational approaches in the big data era. Mol Plant 12:50–152

    Article  CAS  Google Scholar 

  108. Varala K, Marshall-Colón A, Cirrone J, Brooks MD, Pasquino AV, Léran S, Mittal S, Rock TM, Edwards MB, Kim GJ (2018) Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants. Proc Natl Acad Sci USA 115:6494–6499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Luo J, Li H, Liu T, Polle A, Peng C, Luo Z-B (2013) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Luo J, Zhou J, Li H, Shi W, Polle A, Lu M, Sun X, Luo Z-B (2015) Global poplar root and leaf transcriptomes reveal links between growth and stress responses under nitrogen starvation and excess. Tree Physiol 35:1283–1302

    Article  CAS  PubMed  Google Scholar 

  111. Luo J, Shi W, Li H, Janz D, Luo Z-B (2016) The conserved salt-responsive genes in the roots of Populus × canescens and Arabidopsis thaliana. Environ Exp Bot 129:48–56

    Article  CAS  Google Scholar 

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Acknowledgements

This research was financially supported by the Research Start-up Fund for Henan Agricultural Universities (no. 30500487), Fundamental Research Funds for the Central Universities (no. 2662017QD001) and Hubei Province Natural Science Foundation of China (no. 2017CFB338). Dr. Duncan Jackson from the United Kingdom is sincerely thanked for correcting the English language in this manuscript.

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  1. State Key Laboratory of Wheat and Maize Crop Science, College of Agronomy, Henan Agricultural University, Zhengzhou, 450002, China

    Xiaohuan Mu

  2. College of Horticulture and Forestry Sciences, Hubei Engineering Technology Research Center for Forestry Information, Huazhong Agricultural University, Wuhan, 430070, China

    Jie Luo

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Mu, X., Luo, J. Evolutionary analyses of NIN-like proteins in plants and their roles in nitrate signaling. Cell. Mol. Life Sci. 76, 3753–3764 (2019). https://doi.org/10.1007/s00018-019-03164-8

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  • DOI: https://doi.org/10.1007/s00018-019-03164-8

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