Cellular and Molecular Life Sciences

, Volume 76, Issue 19, pp 3753–3764 | Cite as

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

  • Xiaohuan Mu
  • Jie LuoEmail author


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.


Interaction NIN-like protein Nodule formation Nitrogen use efficiency Phosphorus Symbiosis 



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.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Supplementary material

18_2019_3164_MOESM1_ESM.xlsx (276 kb)
Supplementary material 1 (XLSX 275 kb)


  1. 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 7:699Google Scholar
  2. 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 18:2624Google Scholar
  3. 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 105:1141–1157Google Scholar
  4. 4.
    Tegeder M, Masclaux-Daubresse C (2018) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53Google Scholar
  5. 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 497:60–66Google Scholar
  6. 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 129:27–34Google Scholar
  7. 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 61:260–265Google Scholar
  8. 8.
    Ibarra-Henríquez C, Fredes I, Álvarez JM, Undurraga SF, Gutiérrez RA (2017) Nitrate signaling and early responses in Arabidopsis roots. J Exp Bot 68:2541–2551Google Scholar
  9. 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 162:247–255Google Scholar
  10. 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 150:198–208Google Scholar
  11. 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 9:054002Google Scholar
  12. 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 16:2657–2673Google Scholar
  13. 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 60:343–352Google Scholar
  14. 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 77–93Google Scholar
  15. 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 63:55–61Google Scholar
  16. 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 164:40–51Google Scholar
  17. 17.
    Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122Google Scholar
  18. 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 19:3491–3503Google Scholar
  19. 19.
    Fredes I, Moreno S, Díaz FP, Gutiérrez RA (2019) Nitrate signaling and the control of Arabidopsis growth and development. Curr Opin Plant Biol 47:112–118Google Scholar
  20. 20.
    Armijo G, Gutiérrez RA (2017) Emerging players in the nitrate signaling pathway. Mol Plant 10:1019–1022Google Scholar
  21. 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 169:1397–1404Google Scholar
  22. 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 28:485–504Google Scholar
  23. 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 8:1487Google Scholar
  24. 24.
    Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402:191–195Google Scholar
  25. 25.
    Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60:229–237Google Scholar
  26. 26.
    Yokota K, Hayashi M (2011) Function and evolution of nodulation genes in legumes. Cell Mol Life Sci 68:1341–1351Google Scholar
  27. 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 65:5577–5587Google Scholar
  28. 28.
    Konishi M, Yanagisawa S (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat Commun 4:1617Google Scholar
  29. 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:e0208409Google Scholar
  30. 30.
    Konishi M, Yanagisawa S (2014) Emergence of a new step towards understanding the molecular mechanisms underlying nitrate-regulated gene expression. J Exp Bot 65:5589–5600Google Scholar
  31. 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 19:90Google Scholar
  32. 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):311–316Google Scholar
  33. 33.
    Zhao L, Liu F, Crawford N, Wang Y (2018) Molecular regulation of nitrate responses in plants. Int J Mol Sci 19:2039Google Scholar
  34. 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 114:2419–2424Google Scholar
  35. 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 563:259–264Google Scholar
  36. 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 4:1713Google Scholar
  37. 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 111:15267–15272Google Scholar
  38. 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 9:1376Google Scholar
  39. 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 6:27795Google Scholar
  40. 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 6:6274Google Scholar
  41. 41.
    Karve R, Suárez-Román F, Iyer-Pascuzzi AS (2016) The transcription factor NIN-LIKE PROTEIN7 controls border-like cell release. Plant Physiol 171:2101–2111Google Scholar
  42. 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 163:269–281Google Scholar
  43. 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 8:1703Google Scholar
  44. 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 19:2270Google Scholar
  45. 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 84:95–105Google Scholar
  46. 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 26:1775–1781Google Scholar
  47. 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 19:259Google Scholar
  48. 48.
    Zhou J-J, Luo J (2018) The PIN-FORMED auxin efflux carriers in plants. Int J Mol Sci 19:2759Google Scholar
  49. 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 164:101–113Google Scholar
  50. 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 324:268–272Google Scholar
  51. 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 103:11647–11652Google Scholar
  52. 52.
    Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35Google Scholar
  53. 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 48:657–666Google Scholar
  54. 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 33:524–530Google Scholar
  55. 55.
    Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604Google Scholar
  56. 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 72:461–473Google Scholar
  57. 57.
    Badouin H, Gouzy J, Grassa CJ et al (2017) The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 546:148–152Google Scholar
  58. 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:e25975Google Scholar
  59. 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 181:1–20Google Scholar
  60. 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–W38Google Scholar
  61. 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–D203Google Scholar
  62. 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 19:5288–5299Google Scholar
  63. 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 426:1539–1553Google Scholar
  64. 64.
    Shi R, McDonald L, Cygler M, Ekiel I (2014) Coiled-coil helix rotation selects repressing or activating state of transcriptional regulator DhaR. Structure 22:478–487Google Scholar
  65. 65.
    Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282–1294Google Scholar
  66. 66.
    Soyano T, Shimoda Y, Hayashi M (2015) NODULE INCEPTION antagonistically regulates gene expression with nitrate in Lotus japonicus. Plant Cell Physiol 56:368–376Google Scholar
  67. 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 290:12868–12878Google Scholar
  68. 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:re6Google Scholar
  69. 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 4:942–952Google Scholar
  70. 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 91:304–309Google Scholar
  71. 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 18:55–64Google Scholar
  72. 72.
    Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194Google Scholar
  73. 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 57:264–278Google Scholar
  74. 74.
    Krouk G (2017) Nitrate signalling: calcium bridges the nitrate gap. Nat Plants 3:17095Google Scholar
  75. 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 59:612–620Google Scholar
  76. 76.
    Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409Google Scholar
  77. 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 21:3567–3584Google Scholar
  78. 78.
    Gojon A, Nacry P, Davidian J-C (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Curr Opin Plant Biol 12:328–338Google Scholar
  79. 79.
    Vidal EA, Álvarez JM, Moyano TC, Gutiérrez RA (2015) Transcriptional networks in the nitrate response of Arabidopsis thaliana. Curr Opin Plant Biol 27:125–132Google Scholar
  80. 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 111:10371–10376Google Scholar
  81. 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 178:1473–1488Google Scholar
  82. 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 237:919–931Google Scholar
  83. 83.
    Hachiya T, Sakakibara H (2016) Interactions between nitrate and ammonium in their uptake, allocation, assimilation, and signaling in plants. J Exp Bot 68:2501–2512Google Scholar
  84. 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 171:1523–1532Google Scholar
  85. 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 483:380–386Google Scholar
  86. 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:e1001102Google Scholar
  87. 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 88:717–734Google Scholar
  88. 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 51:382–392Google Scholar
  89. 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 57:426–435Google Scholar
  90. 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 15:107–117Google Scholar
  91. 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 141:97–107Google Scholar
  92. 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 7:13179Google Scholar
  93. 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 30:638–651Google Scholar
  94. 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 144:324–335Google Scholar
  95. 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 27:3410–3424Google Scholar
  96. 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 179:1704–1722Google Scholar
  97. 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 31:68–83Google Scholar
  98. 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 9:499Google Scholar
  99. 99.
    Nishida H, Suzaki T (2018) Two negative regulatory systems of root nodule symbiosis: how are symbiotic benefits and costs balanced? Plant Cell Physiol 59:1733–1738Google Scholar
  100. 100.
    Nishida H, Suzaki T (2018) Nitrate-mediated control of root nodule symbiosis. Curr Opin Plant Biol 44:129–136Google Scholar
  101. 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 208:887–903Google Scholar
  102. 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):86–93Google Scholar
  103. 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 9:1494Google Scholar
  104. 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:e1414122Google Scholar
  105. 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 9:12Google Scholar
  106. 106.
    Gutiérrez RA (2012) Systems biology for enhanced plant nitrogen nutrition. Science 336:1673–1675Google Scholar
  107. 107.
    Ueda Y, Yanagisawa S (2019) Delineation of nitrogen signaling networks: computational approaches in the big data era. Mol Plant 12:50–152Google Scholar
  108. 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 115:6494–6499Google Scholar
  109. 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 64:4207–4224Google Scholar
  110. 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 35:1283–1302Google Scholar
  111. 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 129:48–56Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Wheat and Maize Crop Science, College of AgronomyHenan Agricultural UniversityZhengzhouChina
  2. 2.College of Horticulture and Forestry Sciences, Hubei Engineering Technology Research Center for Forestry InformationHuazhong Agricultural UniversityWuhanChina

Personalised recommendations